19th-century idealistic morphologists such natural-theological assumptions about a per- gram as one not dominated by a typological

as Carl
F. Kielmeyer and3/30/09
J. F. Meckel
sonified
God who had created a perfectly and linear-recapitulationist mindset but
0403NewsFocus.qxp
5:23 that
PM Page
29
retained their teleology, their typological adapted nature. Bronns translation, though it rather as continuing to wrestle with the need
emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehen- to account for variability and unpredictable
tionism. This story, emphasizing the long per- sible to a German academic audience, was not change in terms of mechanistic laws of
sistence of a German transcendental approach a conservative throwback. It represented the natureamong which Haeckel included, at
to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolo- the top of his list, natural selection. Haeckels
Introduction
history of biology.
gist who had also long been working on many Darwinism
thus shows continuity with early
Gliboff challenges
this
history
right
from
of
the
questions
Darwin
claimed
as
his
own
19th-century
concerns, mediated through
Stockholm. When we started,
2 Darwins Inspiration, Darwins Legacy
the beginning.
ascription
of simple
theThe
search
profile was
bigger, linear a critical yet generous equal, who saw himself Bronn. But those concerns were always more
Andrew Sugden
a magnolia
she
recapitulationism
to the[flower],
views of Romantic
as moving science forward through the modi- flexible than has been acknowledged, and
recalls.
But 30
years
ago,toshe
embryologists,
he notes,
owes
much
a carica- fications he made to Darwins flawed theory. their articulation changed over time. Of
and by
others
ture developed
Karldiscovered
Ernst vontiny
Baer in a Bronns death in 1862 afforded him little course Haeckels Darwinism was not
Articles
ancient flowers by sieving
polemical context,
then adopted uncritically by chance to steer the conversation further.
Darwins own, but it was not an aberration or
through sand and clay sedi3 ofOn
influential historians
suchthis
as E.
S.
a distortion
some
true theory,
any
the Origin
of Life
onmore
Earth
ments. With
technique,
Russell and they
Stephen
Jay collected
Gould. hunthan any otherCarl
post-Darwinian
additions or
Zimmer
have now

Science
9 January
2009
323: 198-199
Gliboffs fresh
reading
the origadjustments
were.
It was
science
moving
on.
dreds
of of
millimeter-size
preserved in
inal sources flowers,
interpretssome
Kielmeyer
Gliboff s overall picture of scientific
dimensions,
from PorOn the
of Art
and Symbolism
and Meckelthree
as far
less rigidly
advance, in5 contrast
to Origin
Richardss
emphasis
on
other locations
Balter
typological intugal
theirand
orientation
and with
charisma andMichael
passion,
is one of scientists
Cretaceous deposits 70 milScience 6 February
2009 323:
709-711
much more lion
attentive
to natures
building and innovating
incrementally,
workto 120 million years old.
variability thanThis
has fossil
been seen
ing
with
what
their
predecessors
have
handed
diversity
8 On the
Origin
of Photosynthesis
before. Bothshows
for these
them and sculpting
it into
something
new yet
that early-19thangiosperms were

Mitch
Leslie
century naturalists
and
for
their
understandable
to
those
around
them. His senthriving, with several groups

Science 6 March 2009 323: 1286-1287
well-established,
by 100 milintellectual heirs,
Gliboff argues,
sitive reading
allows Out
us of
tothe
see
post-1859
past.
page
10
lion
years
ago.
In
some,
the
Tinyrational
Amborellaactors
sits
the critical issue was to understand
German evolutionists as
rather
10 On theatOrigin
of Flowering
Plants
flower parts
are whorled
the
the
natures manifold
variety
while like
than irrationally stuck
inbottom
someof early-19th
Elizabeth
Pennisi
angiosperm
family tree.
those of modern flowers; in
seeking out underlying
strict natucentury moment with unmodern commitothers they are spiraled, con
Science 3 April 2009 324: 28-31
ral laws to account
for
it.
ments. By challenging the very foundations of
sidered by some researchers
This provides
newprimitive
starting arrangement. Some
the standard
narrative
of von
German
morpholas the amore
from
one 14
of the
nonflowering
seed
plants
Alexander
Humboldt
and the General Physics
point for analyzing
Darwins
ogy,
this careful,
compelling
account
does at
flower fossils
havefirst
prescribed numbers of We are realizing that this or
gymnosperms,
whose
heyday
was
200
of the Earth
petals,
anotherpaleonmodern feature, whereas in
ago.
Modern gymnosperms
translator, the
prominent
least asyears
much
as Richardss
to undermine the

Stephen
T. Jackson
huge diversity is probably million
the petal
count
include
conifers,
ginkgoes, andGerman
the cycads,
tologist H. G.others
Bronna
figure
lit-varies.
association
of
19th-century

Science 1 May 2009 324:Darwin596-597
with
their astout
trunks and
large fronds.
tle attended toInin1998,
the Chinese
standardgeologist Ge Sun of the result of one innovaism with
dangerously
exceptional
view of
Jilin University in Changchun, China, came
Before angiosperms came along, these
story but the
lynchpin of Glinature. But
two books
offer
very
different
16 themuch
Making
German
Evolution:
Translation and Tragedy
across what seemed to be a much older tion piled on top of
plants were
more
diverse
and
boffs. Intriguingly
andfossil,
plausibly,
reads. Is cycadlike
scientific
progress
a matter
Lynn K.
Nyhartsuch
flower. The
called Archaefructus, was
included
species,
as theof perGliboff argues
that Bronns
uselooked to be 144 mil- another innovation.
sonal anguish
and triumph,
or ofwoody
intellectual

Science
27
February
2009
323: 1170-1171
an aquatic
plant that
extinct
Bennettitales,
and
many
REPORTS
of terms likelion
vervollkommnet
chuggingcalled
Our conceptofof which
it should be
years old. By 2002, Sun and David
plants
along?Gnetales,
population
expansion
(23)Originality
areboth.
found the
in the
located acapacious
presence
lineages
that co-occur
in the ad- 6.2% divergence). In contrast,
Petersites
Crane,
of of
thetwo
Florida
of Natural
few
representatives,
including
18
Darwins
(perfect) as Dilcher
translations
for
Dar- Museum
enough
to include
unstable
for H.today
albomarginatus
and H.
faber,
the refugiaofare
genetically joint
jacent refugia.
In all species,
average nethad
nucle- outside (south of)
History
(FLMNH)
in Gainesville
University
Chicago
firs, area
survive
(see family
tree,
Peter J. Bowler
wins improved
or
favored
well
as incommon
the Bahia in
refugium
area for were
H. faber
otide differences
across from
localities
(22)
reflects more similar to each other, although to a lesser p. as
described
an
entire
plant,
roots
to
flow31).
Also
the
Jurassic
and
Notes
Science
9 January
323: 223-226
were not abouthigh
dragging
Darwin within refugia (2.6 to extent in H. faber (0.1 to 1.6%). Signatures of andReferences
H. semilineatus.
The
lack gone;
of 2009
signature
geographic
ers, entombed
on astructure
slab of rock unearthed in
These fossils often spark debate because seed
ferns,
a group
long
their of
1. E.
Haeckel,
Generellenow
Morphologie
der Organismen
backward into
a
German
teleopage
16
Liaoning in northeastern China.
specimens tend to be imperfectly preserved most(Georg
famous
member
is Caytonia, which
Reimer,
Berlin, 1866).
22
The
Red
Queenpress
and
the Court Jester: Species Diversity
logical view of
nature
(asArchaefructus
has in putative
2. Theto
reviewer
previously
served as astructures.
reader for both
In one
wasnt much and leave room for interpretation. To help seems
have
precarpel-like
Fig.
2. sense,
Genetic
diversity
C
A
B

and
the
Role
of
Biotic
and Abiotic Factors Through Time
books
at
the
manuscript
stage.
been claimedtoby
those
who
have
refugial
unstableplant
areas before remedy that, Friis and her colleagues have These g roups perceived relevance to
look at.(stable)
Its versus
a flowering

Michael
J. Benton
intowere
the
Brazilian
Atlantic
rainforest.
there
flowers,
Dilcher
notes.
It
lacked
paid attention
Bronn
at all).
begun
to
examine
flowers
using
synchroflower
evolution
and
their
relationships
to
A painter, too. Haeckels oil landscape of highlands in Java, from
(Top)
Species-specific
stability
maps;have an tron radiation to generate a 3D image of angiosperms

Science
6 February
2009 323: 728-732
petals
and
sepals,
it did
have
ping-ponged
between
10.1126/science.1169621
Instead, Gliboff
asserts,
Bronnsbut
Wanderbilder
(1905).

Science funding
Climate regulation
Human rights

CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE, UC SANTA CRUZ; PHOTO BY JENNIFER SVITKO, COURTESY OF WILLIAM L. CREPET, CORNELL UNIVERSITY

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

Contents

ORIGINS

Pernambuco
modeledcarpel.
refugiaWhen
in black.
(A)Nixon
H.
enclosed
Kevin
and their inner structures, allowing the fossil to camps, depending on how the evolutionary
refugium
albomarginatus, (B) H. semilineatus,
colleagues
at Cornell University compared remain intact while Friis peers inside it trees were26
constructed.
Evidence
for
Ecological
Speciation and Its Alternative
(C) H. faber. Note the absence
of large
1171
www.sciencemag.org
SCIENCE
VOL
323
27
FEBRUARY
2009
its stable
traits regions
with those
same
traits
in
173
living
from
many
angles
(Science,
7
December
In
the
mid-1980s,
Peter
Crane,
now
at

Dolph
Schluter
Bahia
refugium
in the southern portion
plants,
Archaefructus
came
out
as
a
sister
to
2007,
p.
1546).
We
can
get
fantastic
resothe
University
of
Chicago
in
Illinois,
pro*
* Science 6 February 2009 323: 737-741
of the forest (south of the Bahia and
living
closerto tothe
the com- lution, says Friis. Its really exciting. But posed a solution, the anthophyte hypothesis.
So angiosperms
Paulo refugia)and
relative
mon
ancestor
than even
Amborella.
so far, the flowers Friis finds are
Using several
evidenceSpecies
and noting
central
and northern
areas.
Asterisks
30 lines
The of
Bacterial
S o Paulo refugium Challenge: Making Sense of Genetic
Archaefructuss
distinction
that both Bennettitales and
denote
refugia inferred
beyond was
the short- too diverse to trace back to a
Gnetales
and Ecological
Diversity
current
ranges Within
of the target
species.
lived,
however.
months,
better dat- particular
ancestor. From
organize their male
5.4%
and
Christophe
Fraser, together
Eric J. Alm, Martin F. Polz, et al.
localities
sampled
for found these fossils, we cannot
ingSymbols
of the indicate
sediments
in which
it was
female organs

Science
6
February
2009
323: 741-746
molecular
analysis.
Scale
bar,
400
km.
yielded younger dates, putting this f irst say what is the basic
in what could be
con(Bottom)
The 50%with
majority-rule
con- fossil form, she says.
flower
squarely
other early
strued as a preflower,
sensus Bayesian phylogenetic trees,
7%
36 Stability
Predicts Genetic
flower parts, about 125 million years old.
he considered
them, Diversity in the Brazilian Atlantic
7.8%
rooted with sequences from the othAlso,
a
2009
phylogenetic
analysis
of
Before
flowers
along
with
angiosperms,

Forest
Hotspot
er two congeneric species studied
67 (root
taxanot
by shown).
Doyle Thick
and Peter
Endress
they have yet
as comprising
a single

Ana
Carolina Carnaval,
Michael J. Hickerson, Clio F. B. Haddad, et al.
page Although
36
internodes
de- of the
5.3
University
Zurich,
Switzerland,
angiosperm
entity
called
note cladesofwith
posterior
probability placed to find the oldest fossil

Science
6 February
323: 785-789
4% 2009
Larger than 5.8%
life. Although merely
thegreater
fossilthan
in with
liliesindicate
rather than at flowers, researchers
anthophytes. For the next
90%.water
Percentages
2.2 millimeters in diameter, this 3D
corrected
distances between
theTamura-Nei
base of the
angiosperms,
although this assume that the ancesdecade, most family trees
fossil flower shows that grasses date
Around the world, governments turn to AAAS as an objective, multidisciplinary scientic authority to
clades (20).is contested.
conclusion
tral angiosperm evolved
based image:
on morphology
supback to 94 million years ago.
Cover
Tui De Roy/Minden
Pictures/FLPA
5.6%
educate public ofcials and judicial gures on todays most pressing issues. Our goal is to promote
Inset: George Richmond/Bridgeman Art Library, London (Superstock)
informed policy decisions that benet society. And this is just one of the ways that AAAS is committed to
www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009
29
advancing science to support a healthy and prosperous world. Join
us. Together we can make a difference. aaas.org/plusyou/policy

2009 by The American Association for the Advancement of Science. All rights reserved.

On the Origin of
of

Introduction

Life on Earth

Darwins Inspiration, Darwins Legacy

in some warm little pond, with all sorts of

ammonia and phosphoric salts, light, heat, electricity, etc., present, that a protein compound
was chemically formed ready to undergo still
more complex changes, at the present day such
matter would be instantly devoured or
absorbed, which would not have been the case
before living creatures were formed.
Scientists today who study the origin of life
do not share Darwins pessimism about our
ability to reconstruct those early moments.
Now is a good time to be doing this research,
because the prospects for success are greater
than they have ever been, says John
Sutherland, a chemist at the University of Manchester in the United Kingdom. He and others
are addressing each of the steps involved in the
transition to life: where the raw materials came
from, how complex organic molecules such as
RNA formed, and how the first cells arose. In
doing so, they are inching their way toward
making life from scratch. When I was in graduate school, people thought investigating the
origin of life was something old scientists did at
the end of their career, when they could sit in an
armchair and speculate, says Henderson
James Cleaves of the Carnegie Institution for
Science in Washington, D.C. Now making an
artificial cell doesnt sound like science fiction
any more. Its a reasonable pursuit.

The day has passed delightfully. Delight itself, however, is a weak term to express
the feeling of a naturalist who, for the first time, has wandered by himself in a
Brazilian forest. The elegance of the grasses, the novelty of the parasitical plants,
the beauty of the flowers, the glossy green of the foliage, but above all the general
luxuriance of the vegetation, filled me with admiration. A most paradoxical mixture
of sound and silence pervades the shady parts of the wood. The noise from the
insects is so loud, that it may be heard even in a vessel anchored several hundred
yards from the shore; yet within the recesses of the forest a universal silence appears
to reign. To a person fond of natural history, such a day as this brings with it a
deeper pleasure than he can ever hope to experience again.
Charles Darwin, The Voyage of the Beagle, Feb 29th [1832]

The collection reprinted here is a sample of the articles published

in 2009 by Science magazine in celebration of the Darwin bicentenary. We start with four of the essays from our On the Origin
of series, prepared by Sciences news writers; further essays in this
series are appearing monthly in Science throughout the year. A Perspective by Stephen Jackson then considers the legacy of Alexander
von Humboldt, for whom, like Darwin, the South American tropics
were a critical inspiration, and who died 150 years ago in the year
of the publication of Darwins Origin. (Humboldts Personal Narrative of his tropical explorations was acknowledged by Darwin as
far exceed[ing] in merit anything I have read on the subject.) A
book review by Lynn Nyhart explores two recent volumes on Ernst
Haeckels work, his interpretations of Darwin and his contributions
to evolutionary thought.
In the first of four Review articles reprinted here, Peter Bowler analyzes the originality of Darwins contribution to the understanding of
the diversity and diversification of the living world. Michael Benton

examines the extent to which biotic and abiotic factors have shaped
species diversity in the fossil record. Dolph Schluter reviews how
research on speciation has shifted in focus from morphological
evolution to reproductive isolation, tracing the links between Darwins ideas and current thinking. Christophe Fraser and colleagues
discuss the contentious area of microbial species formation, an issue that would surely have vexed Darwin horribly had the bewildering diversity of microbes been known in his day.
Finally, with a focus on conservation, a Report by Ana Carnaval et
al., who model evolutionary processes in endemic tree-frog species in the Brazilian Atlantic Forest, the very biodiversity hotspot
that so inspired Darwin on his South American landfall, and that is
now reduced to a collection of small fragments scattered along the
coast. Darwin returned to the Brazilian coast on his final homeward
leg, more than four years after his first landfall there. His enthusiasm for the tropical forested landscape was undiminished.
In my last walk I stopped again and again to gaze on these beauties, and endeavoured to fix in my mind for ever, an impression
which at the time I knew sooner or later must fail they will leave,
like a tale heard in childhood, a picture full of indistinct, but most
beautiful figures.
Charles Darwin, The Voyage of the Beagle, August 1836
Andrew Sugden, Deputy Editor

AN AMAZON OF WORDS FLOWED FROM

Charles Darwins pen. His books covered the
gamut from barnacles to orchids, from geology to domestication. At the same time, he
filled notebooks with his ruminations and
scribbled thousands of letters packed with
observations and speculations on nature. Yet
Darwin dedicated only a few words of his great
verbal flood to one of the biggest questions in
all of biology: how life began.
The only words he published in a book
appeared near the end of On the Origin of Raw ingredients
Species: Probably all the organic beings which Lifeor at least life as we know itappears to
have ever lived on this earth have descended have emerged on Earth only once. Just about all
from some one primordial form, into which life organisms use double-stranded DNA to encode
was first breathed, Darwin wrote.
genetic information, for example. They copy
Darwin believed that life likely emerged their genes into RNA and then translate RNA
spontaneously from the chemicals
into proteins. The genetic code
it is made of today, such as carbon, THE YEAR OF they use to translate DNA into pronitrogen, and phosphorus. But he
teins is identical, whether they are
The English
did not publish these musings.
emus or bread mold. The simplest
naturalist had
The English naturalist had built
explanation for this shared biology
his argument for evolution, in
is that all living things inherited it
built his argularge part, on the processes he
from a common ancestor
ment for evocould observe around him. He did
namely, DNA-based microbes that
lution, in large lived more than 3.5 billion years
not think it would be possible to
see life originating now because
ago. That common ancestor was
part, on the
the life thats already here would
already fairly complex, and many
processes he
prevent it from emerging.
scientists have wondered how it
In 1871, he outlined the prob- This
might have evolved from a simpler
essay isobserve
the first
could
lem in a letter to his friend, botanist in a monthly series, with
predecessor. Some now argue that
more
on evolutionary
around
him.
.
Joseph Hooker: But if (and Oh! roots
membrane-bound cells with only
online at blogs.
what a big if!) we could conceive sciencemag.org/origins RNA inside predated both DNA

DARWIN

CREDIT: KATHARINE SUTLIFF/SCIENCE

ike many other scientists raised in temperate latitudes, Charles

Darwin was enthralled by his first glimpse of the tropical rain
forest. His Beagle diary entry conveyed those immediate and
thrilling first impressions, but the encounter with the Brazilian Atlantic Forest had an enduring influence on the development of his ideas
over the following decades, with resounding echoes even today in
21st century evolutionary science.

198

9 JANUARY 2009

VOL 323

SCIENCE

and proteins. Later, RNA-based life may have

evolved the ability to assemble amino acids into
proteins. Its a small step, biochemically, for
DNA to evolve from RNA.
In modern cells, RNA is remarkably versatile. It can sense the levels of various compounds inside a cell and switch genes on and
off to adjust these concentrations, for example.
It can also join together amino acids, the building blocks of proteins. Thus, the first cells
might have tapped RNA for all the tasks on
which life depends.
For 60 years, researchers have been honing
theories about the sources of the amino acids
and RNAs building blocks. Over time, they
have had to refine their ideas to take into
account an ever-clearer understanding of what
early Earth was like.
In an iconic experiment in 1953, Stanley
Miller, then at the University of Chicago,
ignited a spark that zapped through a chamber
filled with ammonia, methane, and other
gases. The spark created a goo rich in amino
acids, and, based on his results, Miller suggested that lightning on the early Earth could
have created many compounds that would
later be assembled into living things.
By the 1990s, however, the accumulated
evidence indicated that the early Earth was
dominated by carbon dioxide, with a pinch of
nitrogentwo gases not found in Millers
flask. When scientists tried to replicate Millers
experiments with carbon dioxide in the mix,
their sparks seemed to make almost no amino
acids. The raw materials for life would have
had to come from elsewhere, they concluded.
In 2008, however, lightning began to look
promising once again. Cleaves and his colleagues suspected that the failed experiments
were flawed because the sparks might have produced nitrogen compounds that destroyed any
newly formed amino acids. When they added
buffering chemicals that could take up these
nitrogen compounds, the experiments generated hundreds of times more amino acids than
scientists had previously found.
Cleaves suspects that lightning was only
one of several ways in which organic compounds built up on Earth. Meteorites that fall to
Earth contain amino acids and organic carbon
molecules such as formaldehyde. Hydrothermal vents spew out other compounds that
could have been incorporated into the first life
forms. Raw materials were not an issue, he
says: The real hurdle is how you put together
organic compounds into a living system.
Step 1: Make RNA
An RNA molecule is a chain of linked
nucleotides. Each nucleotide in turn consists
of three parts: a base (which functions as a

www.sciencemag.org

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NEWSFOCUS

EVOLUTIONARY ROOTS
ORIGINS

soup. Weve got the molecules in our RNA, producing the first protocells. The goal
sights, he says.
is to have something that can replicate by itself,
Sutherland cant say for sure where these using just chemistry, says Szostak.
reactions took place on the early Earth, but he
After 2 decades, he and his colleagues
notes that they work well at the temperatures have come up with RNA molecules that can
and pH levels found in ponds. If those ponds build copies of other short RNA molecules.
dried up temporarily,
They have been able to
they would concentrate
mix RNA and fatty
Now making an
the nucleotides, making
acids together in such a
conditions for life even
way that the RNA gets
artificial
cell
doesnt
more favorable.
trapped in vesicles. The
Were these Darwins
vesicles are able to add
sound like science
warm little ponds? It
fatty acids to their
might just be that he
fiction any more. Its membranes and grow.
wasnt too far off, says
In July 2008, Szostak
Sutherland.
a reasonable pursuit. reported that he had
figured out how protoHENDERSON JAMES CLEAVES, cells could eat and
Step 2: The cell
CARNEGIE INSTITUTION FOR SCIENCE bring in nucleotides to
If life did start out with
RNA alone, that RNA
build the RNA.
would need to make copies of itself without
All living cells depend on complicated
help from proteins. Online in Science this channels to draw nucleotides across their
week (www.sciencemag.org/cgi/content/ membranes, raising the question of how a
abstract/1167856), Tracey Lincoln and Ger- primitive protocell membrane brought in these
ald Joyce of the Scripps Research Institute in molecules. By experimenting with different
San Diego, California, have shown how that recipes for membranes, Szostak and his colmight have been possible. They designed a leagues have come up with protocells leaky
pair of RNA molecules that join together and enough to let nucleic acids slip inside, where
assemble loose nucleotides to match their they could be assembled into RNA, but not so
partner. Once the replication is complete, old porous that the large RNA could slip out.
and new RNA molecules separate and join
Their experiments also show that these
with new partners to form new RNA. In 30 vesicles survive over a 100C range. At high
hours, Lincoln and Joyce found, a population temperatures, protocells take in nucleotides
of RNA molecules could grow 100 million quickly, and at lower temperatures, Szostak
times bigger.
found, they build RNA molecules faster.
Lincoln and Joyce kept their RNA moleHe speculates that regular temperature
cules in beakers. On the early Earth, however, cycles could have helped simple protocells surreplicating RNA might have been packed in the vive on the early Earth. They could draw in
first cells. Jack Szostak and his colleagues at nucleotides when they were warm and then use
Harvard Medical School in Boston have been them to build RNA when the temperature
investigating how fatty acids and other mole- dropped. In Szostaks protocells, nucleotides
cules on the early Earth might have trapped are arranged along a template of RNA. Strands
of RNA tend to stick together at low temperatures. When the protocell warmed up again, the
heat might cause the two strands to pull apart,
allowing the new RNA molecule to function.
Now Szostak is running experiments to
bring his protocells closer to life. He is developing new forms of RNA that may be able to
replicate longer molecules faster. For him,
the true test of his experiments will be
whether his protocells not only grow and
reproduce, but evolve.
To me, the origin of life and the origin of
Darwinian evolution are essentially the same
thing, says Szostak. And if Darwin was alive
today, he might well be willing to write a lot
Protocell. Researchers at
more about how life began.
Harvard are trying to make

letter in a genes recipe), a sugar molecule, soup. Weve got the molecules in our RNA, producingVenus,
the firstphallus,
protocells.
goal
orThe
pebble?
and a cluster of phosphorus and oxygen sights, he says.
is to have something
thatknow
can replicate
by itself,
I dont
much about
Art, but I know what
atoms, which link one sugar to the next. For
Sutherland cant say for sure where these using just chemistry,
says
Szostak.the humorist and art critic
I like,
quipped
years, researchers have tried in vain to synthe- reactions took place on the early Earth, but he
After 2 decades,
and hisback
colleagues
Geletthe
Burgess
in 1906. For archaeosize RNA by producing sugars and bases, notes that they work well at the temperatures have come up with
RNA
molecules that
logists,
distinguishing
art can
from nonart is still
joining them together, and then adding phos- and pH levels found in ponds. If those ponds build copies of quite
otherashort
RNA Take
molecules.
challenge.
the 6-centimeter-long
phates. It just doesnt work, says Sutherland. dried up temporarily,
have been
able toas the Venus of
piece They
of quartzite
known
This failure has led scientists to consider they would concentrate
mix
RNA
and
fattyin 1999 next to a
Tan-Tan.
Found
in
Morocco
Now
making an
two other hypotheses about how RNA came to the nucleotides, communicate
making
acidsof
together
suchestimated
a
meaning, whether they be the rich trove
stone intools
to be
be. Cleaves and others think RNA-based life conditions for life
eventhat make
way
that
the
RNA
gets
words
up
our
languages,
the
musibetween
300,000
and
500,000
years old, it
artificial
cell
doesnt
may have evolved from organisms that used a more favorable. cal sounds that convey emotion, or the dra- resembles
trapped
in vesicles.
a human
figureThe
with stubby arms
different genetic materialone no longer
Were these Darwins
vesicles
areBednarik,
able to addan independent
matic paintings
that, 30,000
years
after their and legs.
Robert
sound
like
science
found in nature. Chemists have been able to warm little ponds?
It caused the discoverers of the Chau- archaeologist
fatty acids
to intheir
creation,
based
Caulf ield South,
use other compounds to build backbones for might just be vet
thatCave
he to break
membranes
and
grow.
down
in
tears.
Australia,
insists
that
an ancient human
fiction any more. Its
nucleotides (Science, 17 November 2000, wasnt too far off, While
says sites like Chauvet might be vivid deliberately
In Julymodified
2008, Szostak
the stone to
p. 1306). Theyre now investigating whether Sutherland.
had
reasonable
pursuit.
examples ofa what
some researchers
still make itreported
look morethat
likehe
a person.
these humanmade genetic molecules, called
figured
how
protoconsider a creative explosion that began If so, this
objetout
dart
is so
old
JAMES CLEAVES,
PNA and TNA, could have emerged on their Step 2: The cell
cellscreated
couldnot
eat
and
when modern humans HENDERSON
colonized Europe
that it was
by our
CARNEGIE
INSTITUTIONnumFOR SCIENCE
own on the early Earth more easily than RNA. If life did start out
with
bring inwhich
nucleotides
about
40,000 years ago,
an increasing
own species,
first to
According to this hypothesis, RNA evolved RNA alone, that
build
the RNA.
berRNA
of prehistorians are tracing our sym- appears
in Africa
nearly
later and replaced the earlier molecule.
would need to make
copiesmuch
of itself
without
All living cells
depend
complicated
bolic roots
further
back in timeand
200,000
yearsonago,
but
But it could also be that RNA wasnt put help from proteins.
Online
channels
to draw
nucleotides
across their
in some
cases,intoScience
speciesthis
ancestral
to Homo
by one
of our ancestogether the way scientists have thought. If week (www.sciencemag.org/cgi/content/
membranes, raising
question
sapiens. Like modern humans themselves,
tors, the
perhaps
theof how a
you want to get from Boston to New York, abstract/1167856),
Traceybehavior
Lincolnseems
and Gerprimitive
protocell
membrane brought
symbolic
to have
its origins
large-brained
H. in these
there is an obvious way to go. But if you cant ald Joyce of theinScripps
in have
molecules.
with different
Africa.Research
Recent Institute
excavations
turnedBy experimenting
heidelbergensis,
get there that way, there are other ways you San Diego, California,
have shown
how that
for membranes,
Szostak
up elaborate
stone tools,
beads,recipes
and ochre
thought by
someand his colcould go, says Sutherland. He and his col- might have been
possible.
designed
a leagues
have come
up with protocells
leaky
dating
backThey
100,000
or more
years ago,
anthropologists
to
leagues have been trying to build RNA from pair of RNA molecules
thatresearchers
join togetherare
andstillenough
to let nucleic
slip inside, where
although
debating
be theacids
common
simple organic compounds,
such as formaldeloosewhich
nucleotides
to fmatch
their demonstrate
they could be assembled
RNA, but not so
Since their discovery
by Frenchassemble
spelunkers
of these
inds really
ancestor into
of modhyde, that existed
Earth
life began.
replication
is complete,But
old theres
porouswidethat the large
RNA could
slip out.
in on
1994,
thebefore
magnificent
lions, partner.
horses, Once
and the
symbolic
expression.
ern humans
and
They find they rhinos
make better
progress
toward
andwalls
new RNA
molecules
separatethat
andthe
joinbuildingTheir
experiments
also show
that seem
to leap
from the
of spread
agreement
blocks
Neandertals.
That that these
producing RNAChauvet
if they combine
compo- France
with new
partners
to form newpreceded
RNA. In 30
vesicles art.
survivewould
over a 100C
range. At high
Cave inthesouthern
have
of symbolism
full-blown
mean that
nents of sugars reigned
and the components
of bases
hours,paintLincoln and
Joyce
a population
take in nucleotides
as the worlds
oldest cave
When
wefound,
talk about
beads andtemperatures,
art, we are protocells
art is an extremely
together insteadings.
of separately
comRNA and
molecules
could
growabout
100 million
quickly, and at ancient
lower temperatures,
Szostak
Expertly making
composed
in redofochre
actually
talking
material technologies
part of the Homo
plete sugars andblack
bases charcoal,
first.
timesdemonbigger. for symbolic expression that certainly
found, they
RNA molecules
faster.
the vivid drawings
post-buildrepertoire.
Ignoring
the Symmetry in stone.
Over the past
few years,
they
have docuLincoln
Joycethe
kept
their RNA
mole- thought
He speculates
regularwe
temperature
strate
that the
artistic
gift stretches
backanddate
origins
of symbolic
and fewthat
specimens
have Some stone tools
mented almost an
entire
route
from years.
prebiotic
in beakers.communication,
On the early Earth,
however,by acycles
simplepaleoart,
protocells surmore
than
30,000
Thesecules
paintings
potentially
verycould
wide have
ofhelped
very early
require a mental
molecules to RNA
and aresure
preparing
to pub- replicating
RNAmargin,
might have
been
packed in the Dietrich
vive onStout
the early
Earth. They
could
drawimage
in to create.
are almost
to be mentioned
in any artisays
archaeologist
explaining
them
away,
lish even more cle
details
of their
success.
Dis- art.
first
cells.
Jack of
Szostak
and his
colleagues
at nucleotides when
were warm
andout
then use
or paper
about
the earliest
But
what
University
College
London.
orthey
rejecting
them
covering these new
reactions
School
in Boston of
have
been them
build RNA
when
do they
reallymakes
tell usSutherabout theHarvard
originsMedical
of
The evolution
symbolism
wastoonce
of hand
doesthe
nottemperature
serve this discipline well,
land suspect it wouldnt
have been that hard investigating how
fatty acids
andbeen
other
protocells,
nucleotides
artistic expression?
thought
to have
asmolerapid as dropped.
flicking In
on Szostaks
Bednarik
wrote in
a 2003 analysis of the
for RNA to emergeThe
directly
from anhumans
organicwhocules
on the early
Earth
mightashave
trapped Clive
are arranged
a template
of RNA.
StrandsAnthropology.
prehistoric
decorated
a light
switch,
archaeologist
Gamble along
Venus
of Tan-Tan
in Current
of RNA
tend to stick
at low tempera- are skeptical,
Chauvets walls by torchlight arrived at the of the Royal Holloway, University
of LonYettogether
many archaeologists
When
again, resemblance
the
cave with their artistic genius already in full don, put it some years ago. Buttures.
given
newthe protocell
arguing warmed
that theup
stones
to a
heatappears
might causehuman
the two
strands
to pull
flower. And so, most researchers agree that evidence that symbolic behavior
figure
might
be apart,
coincidence. Indeed,
the newthe
RNA
molecule
to Tan-Tan
function.figurine is remthe origins of art cannot simply
long before cave allowing
paintings,
debate
over the
Now
Szostak
is running
to
be pegged to the latest discovery THE YEAR OF Gamble now says that his
muchiniscent
of aexperiments
similar controversy
over a
Recent
protocells
closer
to life.
He is develof ancient paintings or sculpcited comment needsbring
to behis
modsmaller
stone
discovered
in 1981 at the site of
of RNARam
that may
able to
ture. Some of the earliest art
ified: Its a dimmer oping
switchnew
now,forms
Berekhat
in thebeIsraeli-occupied
Golan
excavations
molecules
him,
likely perished over the ages;
a stuttering candle. replicate longerHeights.
Tofaster.
someFor
archaeologists,
this
have turned
the truepintest of
his experiments
will
be
much remains to be found; and
As they more precisely
250,000-year-old
object
resembles
a woman,
whether
his protocells
only
up elaborate
archaeologists dont always
point when symbolic
behavior
but othersnot
argue
thatgrow
it wasand
shaped by natural
reproduce,
but
evolve.
agree on how to interpret what is
began,
scientists
are
hoping
they
forces,
and,
in
any
case,
looks
more like a
stone tools,
To
me, the penguin
origin ofor
life
and the origin
of an exhaustive
unearthed. As a result, instead of
might one day crack the
tougha phallus.
Even after
beads, and
Darwinian
are essentially
same
chasing after arts first appearest question of all: What
was itsevolution
microscopic
studytheconcluded
that the
thing, says
AndRam
if Darwin
ance, many researchers seek to
evolutionary advantage
toSzostak.
Berekhat
objectwas
hadalive
indeed been etched
ochre dating
today,
he mightwith
wellabe
willing
to write what
a lot some consider
understand its symbolic roots.
humans?
Didatsymbols,
as many
tool
to emphasize
Researchers
back 100,000Protocell.
more
about
how
life
began.
After all, art is an aesthetic This essay continuesHarvard
researchers
suspect,
serve
as
a
its
head
and
arms,
many
researchers have
are
trying
to
make
our
more
See more
ZIMMER
simplesocial
life forms,
shown
expression of something more monthlyorseries.
glue
that helped tribes of rejected it as aCARL
work of
art. For some, proof of
on humans evolutionary
here in aearly
computer
image. to survive
Carl Zimmer
is the symbolic
author of Microcosm:
coli and the
fundamental: the cognitive abil- journey
humans
and
behaviorE.requires
evidence that the
years
onlineago.
at blogs.
New Science of Life.symbols had a commonly understood meanity to construct symbols that sciencemag.org/origins. reproduce?

www.sciencemag.org

SCIENCE

VOL 323

CARL ZIMMER

Carl Zimmer is the author of Microcosm: E. coli and the

New Science of Life.

9 JANUARY 2009

Art and Symbolism

199

CREDITS (TOP
(LEFTTO
TOBOTTOM):
RIGHT): KATHERINE
SUTLIFF/SCIENCE;
THE
BOXGROVE
PROJECT
CREDITS
KATHARINE
SUTLIFF/SCIENCE;
THE
BOXGROVE
PROJECT; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)

simple life forms, shown

here in a computer image.

On the Origin of
of

CREDIT: JANET IWASA

CREDIT: JANET IWASA

letter in a genes recipe), a sugar molecule,

and a cluster of phosphorus and oxygen
atoms, which link one sugar to the next. For
years, researchers have tried in vain to synthesize RNA by producing sugars and bases,
joining them together, and then adding phosphates. It just doesnt work, says Sutherland.
This failure has led scientists to consider
two other hypotheses about how RNA came to
be. Cleaves and others think RNA-based life
may have evolved from organisms that used a
different genetic materialone no longer
found in nature. Chemists have been able to
use other compounds to build backbones for
nucleotides (Science, 17 November 2000,
p. 1306). Theyre now investigating whether
these humanmade genetic molecules, called
PNA and TNA, could have emerged on their
own on the early Earth more easily than RNA.
According to this hypothesis, RNA evolved
later and replaced the earlier molecule.
But it could also be that RNA wasnt put
together the way scientists have thought. If
you want to get from Boston to New York,
there is an obvious way to go. But if you cant
get there that way, there are other ways you
could go, says Sutherland. He and his colleagues have been trying to build RNA from
simple organic compounds, such as formaldehyde, that existed on Earth before life began.
They find they make better progress toward
producing RNA if they combine the components of sugars and the components of bases
together instead of separately making complete sugars and bases first.
Over the past few years, they have documented almost an entire route from prebiotic
molecules to RNA and are preparing to publish even more details of their success. Discovering these new reactions makes Sutherland suspect it wouldnt have been that hard
for RNA to emerge directly from an organic

EVOLUTIONARY ROOTS

DARWIN

www.sciencemag.org
SCIENCE VOL
323 9 JANUARY
www.sciencemag.org
SCIENCE
VOL 323 2009
6 FEBRUARY 2009

199

5
709

ORIGINS

ORIGINS
tools, which Wynn and many others argue are
clear examples of an imposed form based on a
mental template. Some have even argued that
these skillfully crafted hand axes had symbolic
meanings, for example to display prestige or
even attract members of the opposite sex.
The half-million-year mark also heralded
the arrival of H. heidelbergensis, which had
a much larger brain than H. erectus. Not
long afterward, our African ancestors began
to create a wide variety of finely crafted
blades and projectile points, which allowed
them to exploit their environment in more
sophisticated ways, and so presumably
enhance their survival and reproduction.
Archaeologists refer to these tools as Middle
Stone Age technology and agree that they
did require mental templates. The tools tell
us that the hominid world was changing,
says Wynn.
ing and were shared within groups of people. ity to hold an abstract concept in ones head
As one moves forward in time, humans
For example, the hundreds of bone and stone and, in the case of the tool, to impose a pre- appear able to imagine and create even more
Venus figurines found at sites across Eura- determined form on raw material based on an elaborate tools, sharpening their evolutionsia beginning about 30,000 years ago were abstract mental template. That kind of ability ary edge in the battle for survival. By
skillfully carved and follow a common motif. was probably not needed to make the earliest 260,000 years ago, for example, ancient
They are widely regarded not only as sym- known tools, say Wynn and other researchers. humans at Twin Rivers in what is now Zambia
bolic expression, but full-fledged art.
These implements, which date back 2.6 mil- could envision a complex finished tool and
Thus many researchers are reluctant to lion years, consist mostly of rocks that have put it together in steps from different compoaccept rare, one-off discoveries like the Tan- been split in two and then sharpened to make nents. They left behind finely made blades
Tan or Berekhat Ram objects as signs of simple chopping and scraping implements.
and other tools that had been modified
symbolic behavior. You can imagine [an
Then, about 1.7 million years ago, large, usually by blunting or backing one edge
ancient human] recognizing a resemblance teardrop-shaped tools called Acheulean hand to be hafted onto handles, presumably made
but [the object] still hav[ing] no symbolic axes appeared in Africa. Likely created by of wood. These so-called backed tools have
meaning at all, says Philip Chase, an anthro- H. erectus and probably used to cut plants and been widely regarded as evidence of sympologist at the University of Pennsylvania. butcher animals, these hand-held tools vary bolic behavior when found at much younger
Thomas Wynn, an anthropologist at the greatly in shape, and archaeologists have sites. This flexibility in stone tool manufacUniversity of Colorado, Colorado Springs, debated whether creating the earliest ones ture [indicates] symbolic capabilities, says
agrees: If its a one-off, I dont think it required an abstract mental template. But by archaeologist Sarah Wurz of the Iziko Musecounts. Its not sending a message to anyone. about 500,000 years ago, ancient humans were ums of Cape Town in South Africa.
creating more symmetrical Late Acheulean
Similar cognitive abilities were possibly
Tools of the imagination
required to make the famous
Given how difficult it is to detect
400,000-year-old wooden spears
If its a one-off, I dont think
the earliest symbolic messages in
from Schningen, Germany. One
the archaeological record, some
recent study concludes that these
it counts. Its not sending a
researchers look instead for proxy
spears creatorsprobably membehaviors that might have
bers of H. heidelbergensiscarmessage to anyone.
required similar cognitive abiliried out at least eight preplanned
ties, such as toolmaking. Charles
steps spanning several days,
THOMAS WYNN, UNIVERSITY OF COLORADO,
Darwin himself saw an evoluincluding chopping tree branches
COLORADO SPRINGS
tionary parallel between toolwith hand axes and shaping the
making and language, probably
spears with stone flakes.
the most sophisticated form of
The idea that sophisticated
symbolic behavior. To chip a
toolmaking and symbolic
flint into the rudest tool, Darwin
thought require similar cognitive
wrote in The Descent of Man,
skills also gets some support
demands a perfect hand as well
from a surprising quarter: brainadapted to that task as the vocal
imaging studies. Stouts team ran
organs are to speaking.
positron emission tomography
To many researchers, making
scans on three archaeologists
sophisticated tools and using Symbolic start. Some scientists argue that this 77,000-year-old engraved ochre all skillful stone knappersas
symbols both require the capac- shows symbolic capacity.
they made pre-Acheulean and

Late Acheulean tools. Both methods turned

on visual and motor areas of the brain. But
only Late Acheulean knapping turned on circuits also linked to language, the team
reported last year.

710

6 FEBRUARY 2009

VOL 323

SCIENCE

www.sciencemag.org

Color me red
At Twin Rivers, its not just the tools that hint
at incipient symbolic behavior. Early humans
there also left behind at least 300 lumps of
ochre and other pigments in a rainbow of colors: yellow, red, pink, brown, purple, and
blue-black, some of which were gathered far
from the site. Excavator Lawrence Barham
of the University of Liverpool in the United
Kingdom thinks they used the ochre to
paint their bodies, though theres little
hard evidence for this. Most archaeologists agree that body painting, as well
as the wearing of personal ornaments such as bead necklaces,
was a key way that early humans
symbolically communicated
social identity such as membership in a particular group, much
as people today declare social
allegiances and individual personalities by their clothing and jewelry.
Yet while the Twin Rivers evidence is
suggestive, its hard to be sure how the ochre
was actually used. Theres little sign that it was
ground into powder, as needed for decoration,
says Ian Watts, an independent ochre expert in
Athens. And even ground ochre could have
had utilitarian uses, says archaeologist Lyn
Wadley of the University of Witwatersrand
in Johannesburg, South Africa. Modern-day
experiments have shown that ground ochre
can be used to tan animal hides, help stone
tools adhere to bone or wooden handles, and Eye of the beholder. Archaeologists debate whether
this modified stone was meant to represent a woman.
even protect skin against mosquito bites.
We simply dont know how ancient people used ochre 300,000 years ago, Wadley consider diagnostic elements of symbolic
says. And since at that date the ochre users behavior came together. And in work now
were not modern humans but our archaic in press, the Blombos team reports finding
ancestors, some experts are leery of assign- engraved ochre in levels dating back to
ing them symbolic savvy.
100,000 years ago (Science,
Yet many archaeologists are
30 January, p. 569).
willing to grant that our species,
There are other hints that the
H. sapiens, was creating and sciencemag.org
modern humans who ventured
Hear author
using certain kinds of symbols
out of Africa around this time
Michael Balter
by 75,000 years ago and per- discuss the roots of art at might also have engaged in symhaps much earlier. At sites such www.sciencemag.org/
bolic behavior. At the Skhul rock
as Blombos Cave on South darwin.
shelter in Israel, humans left
Africas southern Cape, people
100,000-year-old shell beads
left sophisticated tools, including elabo- considered by some to be personal ornarately crafted bone points, as well as perfo- ments (Science, 23 June 2006, p. 1731). At
rated beads made from snail shells and the 92,000-year-old Qafzeh Cave site
pieces of red ochre engraved with what nearby, modern humans apparently strongly
appear to be abstract designs. At this single preferred the color red: Excavators have
site, a number of what many archaeologists studied 71 pieces of bright red ochre associ-

Online

CREDIT: FRANCESCO DERRICO AND APRIL NOWELL

CREDITS (TOP TO BOTTOM): FRENCH MINISTRY OF CULTURE AND COMMUNICATION/DRAC RHONE-ALPES/DEPARTMENT OF ARCHAEOLOGY; CHRIS HENSHILWOOD AND FRANCESCO DERRICO

A roaring start. Researchers agree that Chauvet Caves

magnificent paintings, including these lions, are full-blown art.

www.sciencemag.org

SCIENCE

VOL 323

ated with human burials. Some researchers

argue that this represents an early case of
color symbolism, citing the universal
importance of red in historical cultures
worldwide and the apparently great lengths
to which early humans went to gather red
ochre. There is very strong circumstantial
evidence for the very great antiquity of the
color red as a symbolic category, says
anthropologist Sally McBrearty of the
University of Connecticut, Storrs.
These finds of colorful ochre, fancy
tools, and beads have convinced many
researchers that the building blocks of
symbolism had emerged by at least
100,000 years ago and possibly
much earlier. But why? What
selective advantages did using
symbols confer on our ancestors?
To some scientists, the question is a no-brainer, especially
when it is focused on the most
sophisticated form of symbolic
communication: language. The
ability to communicate detailed,
concrete information as well as
abstract concepts allowed early
humans to cooperate and plan for the
future in ways unique to our species,
thus enhancing their survival during
rough times and boosting their reproductive success in good times. What
aspects of human social organization and
adaptation wouldnt benefit from the evolution of language? asked Terrence Deacon, a
biological anthropologist at the University
of California, Berkeley, in his influential
book The Symbolic Species: The Coevolution of Language and the Brain. Deacon
went on to list just some of the advantages:
organizing hunts, sharing food, teaching
toolmaking, sharing past experiences, and
raising children. Indeed, many researchers
have argued that symbolic communication is
what held groups of early humans together
as they explored new environments and
endured climatic shifts.
As for art and other nonlinguistic forms
of symbolic behavior, they may also have
been key to cementing these bonds, by
expressing meanings that are difficult or
impossible to put into words. In that way,
artistic expression, including music, may
have helped ensure the survival of the
fittest. This may also explain why great art
has such emotional force, because the most
effective symbols are those that convey
their messages the most powerfully
something the artists at Chauvet Cave seem
to have understood very well.

6 FEBRUARY 2009

MICHAEL BALTER

711

ORIGINS

On the Origin of
of

Photosynthesis

8
1286

To catch a photon
Over more than 200 years, researchers have
ironed out most of the molecular details of
how organisms turn carbon dioxide and
water into food. Chlorophyll pigment and
about 100 other proteins team up to put light
to work. Plants, some protists, and cyanobacteria embed their chlorophyll in two
large protein clusters, photosystem I and
photosystem II. And they need both systems
to use water as an electron source. Light
jump-starts an electrical circuit in which The electron thief
electrons flow from the photosystems Either way, it took some fancy fiddling to
through protein chains that
convert the primitive reaction
make the energy-rich molecules THE YEAR OF centers to oxygen-generating
Given its
ATP and NADPH. These molephotosystems. Oxygenic photocules then power the synthesis
synthesis was a huge upgrade,
importance in
of the sugars that organisms
leading to a land of plenty, says
making and
depend on to grow and multiply.
biochemist John Allen of Queen
keeping earth
Photosystem IIthe strongest
Mary, University of London.
naturally occurring oxidant
Water is everywhere, so the
lush, photoregains its lost electrons by
organisms never ran out of elecsynthesis ranks
swiping them from water, genertrons. They were unstoppable.
ating oxygen as a waste product.
But water clings to its elechigh on the
However, some bacteria
trons. With its oxidizing power,
top- 10 list of
dont rely on water as an elec- This essay is the third
photosystem II can wrench them
monthly series. More
tron source, using hydrogen sul- in aevolutionary
away, but the reaction centers in
on evolution online at
fide or other alternatives. These blogs.sciencemag.org/
nonoxygenic photosynthesizers
milestones.
nonconformists, which today origins.
cannot. Biochemists James

6 MARCH 2009

Allen (no relation to John Allen)

and JoAnn Williams of Arizona
State University, Tempe, and colleagues are working out how a
bacterial reaction center could
have evolved photosystem IIs
appetite for electrons.
Taking a hands-on approach,
they have been tinkering with the
reaction center of the purple bacterium Rhodobacter sphaeroides
to determine if they can make
it more like photosystem II.
First they targeted bacteriochlorophyll, the bacterial version
of chlorophyll thats at the core
of the reaction center, and
altered the number of hydrogen
bonds. Adding hydrogen bonds
hiked the molecules greed for
electrons, they found.
The water-cleaving portion
of photosystem II sports four
manganese atoms that become
oxidized, or lose electrons. So
the team equipped the bacterial
reaction center with one atom
of the metal. In this modif ied
version, the added manganese
also underwent oxidation, the
researchers reported in 2005.
James Allen says that their creations arent powerful enough to
split water. But eventually, they
hope to engineer a reaction center
that can oxidize less possessive
molecules, such as hydrogen
peroxide, that would have been
present on the early Earth. Even
if the researchers never replicate
photosystem II, if we def ine
the intermediate stages, weve
accomplished a lot, he says.

VOL 323

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www.sciencemag.org

CREDIT: NEALE CLARK/GETTY IMAGES

DARWIN

CREDIT: K. SUTLIFF/SCIENCE

Try to picture the world without photosynthesis. Obviously, youd have to strip
away the greenerynot just the redwoods
and sunflowers, but also the humble algae
and the light-capturing bacteria that nourish
many of the worlds ecosystems. Gone, too,
would be everything that depends on photosynthetic organisms, directly or indirectly,
for sustenancefrom leaf-munching beetles to meat-eating lions. Even corals, which
play host to algal partners, would lose their
main food source.
Photosynthesis makes Earth congenial for
life in other ways, too. Early photosynthesizers
pumped up atmospheric oxygen concentrations, making way for complex multicellular
life, including us. And water-dwellers were
able to colonize the land only because the
oxygen helped create the ozone layer that
shields against the suns ultraviolet radiation.
Oxygen-producing, or oxygenic, photosynthesis was the last of the great inventions
of microbial metabolism, and it changed the
planetary environment forever, says geobiologist Paul Falkowski of Rutgers University in New Brunswick, New Jersey.
Given its importance in making and keeping Earth lush, photosynthesis ranks high on
the top-10 list of evolutionary milestones. By
delving into ancient rocks and poring over
DNA sequences, researchers are now trying to

piece together how and when organisms first

began to harness lights energy. Although
most modern photosynthesizers make oxygen
from water, the earliest solar-powered bacteria
relied on different ingredients, perhaps hydrogen sulfide. Over time, the photosynthetic
machinery became more sophisticated, eventually leading to the green, well-oxygenated
world that surrounds us today. In the lab, some
biochemists are recapitulating the chemical
steps that led to this increased complexity.
Other researchers are locked in debates over
just when this transition happened, 2.4 billion
years ago or much earlier.
Looking so far into the past is difficult.
The geological record for that time is
skimpy and tricky to interpret. Eons of evolution have blurred the molecular vestiges
of the early events that remain in living
organisms. But its a terribly important
problem, says biochemist Carl Bauer of
Indiana University, Bloomington, one well
worth the travails.

live in habitats such as scalding hot springs,

dont generate oxygen. Their photosynthetic
proteins huddle in relatively simple reaction
centers that may have been the predecessors
of the two photosystems.
Envisioning the steps that led to this
complex biochemistry is mind-boggling.
Similarities between proteins in photosynthetic and nonphotosynthetic bacteria
suggest that early microbes co-opted some
photosynthesis genes from other metabolic
pathways. But protophotosynthesizers
might also have helped each other piece
these pathways together by swapping
genes. Biochemist Robert Blankenship of
Washington University in St. Louis, Missouri, and colleagues say theyve uncovered
traces of these lateral gene transfers by
comparing complete bacterial genomes.
For example, their 2002 study of more than
60 photosynthetic and nonphotosynthetic
bacteria (Science, 22 November 2002,
p. 1616) suggested that bugs had passed
around several photosynthesis genes,
including some involved in synthesizing the
bacterial version of chlorophyll.
Gene-sharing might also explain the puzzling distribution of the photosystems,
Blankenship says. A cell needs both photosystems to carry out oxygenic photosynthesis.
Yet modern nonoxygenic bacteria have the
presumptive predecessor either of photosystem I or of photosystem II, never both. To
explain how the two protein complexes
wound up together, Blankenship favors a
large-scale lateral [gene] transfer or even a
fusion of organisms carrying each photosystem. However, other researchers remain
skeptical, arguing that one photosystem
evolved from the other, possibly through the
duplication of genes, creating an ancient cell
with both. No one knows for sure.

Catching rays. Long before plants got

in on the act, photosynthetic cyanobacteria living in pools like this one in
Yellowstone National Park were changing the composition of the atmosphere.

says astrobiologist Roger Buick

of the University of Washington,
Seattle. These hints could push
the origin back 600 million
years or more.
One line of evidence is oil
biomarkers that researchers
think are the remains of cyanobacteria. Theyve turned up in
rocks that are up to 2.7 billion
years old. And in western Australia, thick shale deposits that
are 3.2 billion years old hold
rich bacterial remains but no
traces of sulfur or other possible
electron sources, suggesting that
the microbes were using water
to make energy.
Geologist Euan Nisbet of
Royal Holloway, University of
London, and colleagues found
additional support for an early
origin when they went searching for traces of RuBisCO, a
key photosynthetic enzyme.
RuBisCO feeds carbon dioxide
into the reactions that yield sugars. The enzyme version found
in oxygenic photosynthesizers
Oxygenic photosynthesis was the
plays favorites: It prefers carbon
dioxide that contains the carbonlast of the great inventions of micro12 isotope over the bulkier carbon-13. In 2007, Nisbet and
bial metabolism, and it changed the
his colleagues found disproportionately low carbon-13 values
planetary environment forever.
indicative of RuBisCO activity
Paul Falkowski, Rutgers University when they analyzed organic
matter in rocks from three sites
Something in the air
about 2.4 billion years ago, geologists see in Zimbabwe and Canada that are between
How the photosystems got their start is cru- the first unmistakable signs of significant, 2.7 billion and 2.9 billion years old. Nisbet
cial for understanding the origin of photo- sustained levels of atmospheric oxygen. concludes that oxygen-making photosynthesis. But the question thats drawn the These signs include red beds, or layers synthesis began at least 2.9 billion years ago.
most attentionand provoked the most tinged by oxidized iron, i.e., rust. Further
The early-origin case isnt ironclad. For
wranglingis when photosynthesis began. support that the GOE marks an atmospheric example, a 2008 paper that has some
Most researchers accept that nonoxygenic revolution comes from a technique that researchers fuming claims that the oil biophotosynthesis arose first, probably shortly detects skewed abundances of sulfur iso- markers are contaminants that seeped in
after life originated more than 3.8 billion topes that occur if the air lacks oxygen. from younger rocks. Advocates also have to
years ago. Life needs an energy source, and These imbalances persisted until the GOE, explain why it took hundreds of millions of
the sun is the only ubiquitous and reliable when they vanished.
years for oxygen to build up in the air.
energy source, says Blankenship.
Hard-liners construe these data to mean
Although the last word on the origins of
The sharpest disputes revolve around that oxygenic photosynthesis could not have oxygen-making photosynthesis isnt in,
when organisms shifted to oxygenic photo- emerged until shortly before the GOE. But researchers say they are making progress. One
synthesis. At issue is how to interpret a other scientists disagree. We are finding thing is for certain, however: Without this
watershed in the fossil record known as the more and more hints that oxygenic photo- innovation, Earth would look a lot like Mars.
MITCH LESLIE
great oxidation event (GOE). In rocks from synthesis goes deeper into the fossil record,
www.sciencemag.org

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NEWSFOCUS

ORIGINS
embryo that serves as its food supply.
Darwin was perplexed by the diversity of
flowering plants; they were too numerous
and too varied, and there were too few fossils to sort out which were more primitive.
Throughout much of the 20th century, magnolia relatives with relatively large flowers
were leading candidates for the most primihow flowers got startedand from which tive living flowers, although a few
ancestor. Today, researchers have analytical researchers looked to small herbs instead.
tools, fossils, genomic data, and insights that
In the late 1990s, molecular systematics
Darwin could never have imagined, all of came to the rescue, with several reports prewhich make these mysteries less abom- senting a fairly consistent picture of the
inable. Over the past 40 years, techniques lower branches of the angiosperm tree. An
for assessing the relationships between obscure shrub found only in New Caledonia
organisms have greatly improved, and gene emerged as a crucial window to the past.
sequences, as well as morphology, now help Amborella trichopoda, with its 6-millimeter
researchers sort out which angiosperms greenish-yellow flowers, lives deep in the
arose early and which arose late. New fossil cloud forests there. In multiple gene-based
finds and new ways to study themwith assessments, including an analysis in 2007
synchrotron radiation, for examplepro- of 81 genes from chloroplast genomes
vide a clearer view of the detailed anatomy belonging to 64 species, Amborella sits
of ancient plants. And researchers from var- at the base of the angiosperm family tree,
ious fields are figuring out genomic changes the sister group of all the rest of the
that might explain the amazing success of angiosperms.
this fast-evolving group.
Given that placement, Amborellas tiny
These approaches have given researchers flowers may hint at what early blossoms
a much better sense of what early flowers were like. Its one of the most similar living
were like and the relationships among them. flower[s] to the worlds first flower, says
But one of Darwins mysteries remains: the James Doyle of the University of Californature and identity of the angiosperm ances- nia, Davis. The petals and sepals of its sintor itself. When flowering plants show up in gle-sex flowers are indistinguishable and
the fossil record, they appear with a bang, vary in number; so too do the numbers of
with no obvious series of intermediates, as seed-producing carpels on female flowers
Darwin noted. Researchers still dont know and pollen-generating stamens on male
which seed- and pollen-bearing
flowers. The organs are spirally
organs eventually evolved into THE YEAR OF arranged, and carpels, rather
the comparable flower parts.
than being closed by fused tisFor more on
Were a bit mystif ied, says
sue as in roses and almost all
botanist Michael Donoghue of
familiar flowers, are sealed by a
flower origins,
Yale University. It doesnt
secretion.
listen to a
appear that we can locate a close
Most genetic analyses showed
relative of the flowering plants.
that
water lilies were the next
podcast by
branch up the angiosperm tree,
author Elizabeth
Seeking the first flower
followed by a group represented
One of two major living groups
by star anise, which also has a
Pennisi at
of seed plants, angiosperms have
primitive look about it, says
covered seeds that develop This essay
is the fourth
Doyle, though each of these
www.
encased in a protective tissue in a monthly series.
has deviations from the ancesFor more
on evolutionary
sciencemag.
called a carpel (picture a bean topics
tral type.
online, see the
at
pod). Thats in contrast to the Origins blog
org/
nonflowering gymnosperms, blogs.sciencemag.org/
Fossil records
origins.
For more on
multimedia/
such as conifers, which bear flower
Although some fossil pollen
origins, listen
by author
naked seeds on scales. An to a podcast
dates back 135 million years, no
podcast.
Elizabeth Pennisi at
angiosperms carpel sits at the www.sciencemag.org/
credible earlier fossil evidence
center of the flower, typically multimedia/podcast.
exists. In Darwins day, and for
surrounded by pollen-laden stamany decades afterward, palemens. In most flowers, the carpel and stamens obotanists primarily found leaves or pollen
are surrounded by petals and an outer row of but almost no fossil flowers. They had the
leaflike sepals. Seeds have a double coating wrong search image, says Else Marie Friis of
as well as endosperm, tissue surrounding the the Swedish Museum of Natural History in

On the Origin of
of

to British botanist Joseph Dalton Hooker,

lamenting an abominable mystery that
threw a wrench into his theory of evolution:
How did flowering plants diversify and
spread so rapidly across the globe? From
rice paddies to orange groves, alpine meadows to formal gardens, prairies to oakhickory forests, the 300,000 species of
angiosperms alive today shape most terrestrial landscapes and much of human life
and culture. Their blooms color and scent
our world; their fruits, roots, and seeds feed
us; and their biomass provides clothing,
building materials, and fuel. And yet this
takeover, which took place about 100 million years ago, apparently happened in a
blink of geological time, just a few tens of
millions of years.
The father of evolution couldnt quite
fathom it. Darwin had an abhorrence that
evolution could be both rapid and potentially even saltational, writes William
Friedman in the January American Journal
of Botany, which is devoted to this
abominable mystery. Throughout his life,
Darwin pestered botanists for their
thoughts on the matter, but they couldnt
give him much help.
Now, 130 years later, evolutionary biologists are still pestering botanists for clues
about what has made this plant group so
successful, as well as when, where, and

28

10

3 APRIL 2009

DARWIN

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CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE, UC SANTA CRUZ; PHOTO BY JENNIFER SVITKO, COURTESY OF WILLIAM L. CREPET, CORNELL UNIVERSITY

IN 1879, CHARLES DARWIN PENNED A LETTER

CREDIT:
WITH THE
KIND PERMISSION
OF
THEPERMISSION
DIRECTOR AND
THE DIRECTOR
BOARD OFAND
TRUSTEES,
ROYAL
BOTANIC
GARDENS,
KEW
CREDITSREPRODUCED
(TOP TO BOTTOM):
REPRODUCED
WITH THE
KIND
OF THE
THE BOARD
OF
TRUSTEES,
ROYAL BOTANIC
GARDENS, KEW; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)

Flowering Plants

Stockholm. When we started,

the search profile was bigger,
a magnolia [flower], she
recalls. But 30 years ago, she
and others discovered tiny
ancient flowers by sieving
through sand and clay sediments. With this technique,
they have now collected hundreds of millimeter-size
flowers, some preserved in
three dimensions, from Portugal and other locations with
Cretaceous deposits 70 million to 120 million years old.
This fossil diversity
shows that angiosperms were
thriving, with several groups
well-established, by 100 million years ago. In some, the
flower parts are whorled like
those of modern flowers; in
others they are spiraled, considered by some researchers
as the more primitive arrangement. Some
flower fossils have prescribed numbers of
petals, another modern feature, whereas in
others the petal count varies.
In 1998, Chinese geologist Ge Sun of
Jilin University in Changchun, China, came
across what seemed to be a much older
flower. The fossil, called Archaefructus, was
an aquatic plant that looked to be 144 million years old. By 2002, Sun and David
Dilcher of the Florida Museum of Natural
History (FLMNH) in Gainesville had
described an entire plant, from roots to flowers, entombed on a slab of rock unearthed in
Liaoning in northeastern China.
In one sense, Archaefructus wasnt much
to look at. Its a flowering plant before
there were flowers, Dilcher notes. It lacked
petals and sepals, but it did have an
enclosed carpel. When Kevin Nixon and
colleagues at Cornell University compared
its traits with those same traits in 173 living
plants, Archaefructus came out as a sister to
living angiosperms and closer to the common ancestor than even Amborella.
Archaefructuss distinction was shortlived, however. Within months, better dating of the sediments in which it was found
yielded younger dates, putting this f irst
flower squarely with other early fossil
flower parts, about 125 million years old.
Also, a 2009 phylogenetic analysis of
67 taxa by Doyle and Peter Endress of the
University of Zurich, Switzerland, placed
the fossil in with water lilies rather than at
the base of the angiosperms, although this
conclusion is contested.

Out of the past.

Tiny Amborella sits
at the bottom of the
angiosperm family tree.

from one of the nonflowering seed plants

or gymnosperms, whose heyday was 200
million years ago. Modern gymnosperms
include conifers, ginkgoes, and the cycads,
with their stout trunks and large fronds.
Before angiosperms came along, these
plants were much more diverse and
included cycadlike species, such as the
extinct Bennettitales, and many woody
plants called Gnetales, of which
Peter Crane, a few representatives, including the
University of Chicago joint firs, survive today (see family tree,
p. 31). Also common in the Jurassic were
These fossils often spark debate because seed ferns, a group now long gone; their
specimens tend to be imperfectly preserved most famous member is Caytonia, which
and leave room for interpretation. To help seems to have precarpel-like structures.
remedy that, Friis and her colleagues have These g roups perceived relevance to
begun to examine flowers using synchro- flower evolution and their relationships to
tron radiation to generate a 3D image of angiosperms have ping-ponged between
their inner structures, allowing the fossil to camps, depending on how the evolutionary
remain intact while Friis peers inside it trees were constructed.
from many angles (Science, 7 December
In the mid-1980s, Peter Crane, now at
2007, p. 1546). We can get fantastic reso- the University of Chicago in Illinois, prolution, says Friis. Its really exciting. But posed a solution, the anthophyte hypothesis.
so far, the flowers Friis finds are
Using several lines of evidence and noting
too diverse to trace back to a
that both Bennettitales and
particular ancestor. From
Gnetales organize their male
these fossils, we cannot
and female organs together
say what is the basic
in what could be conform, she says.
strued as a preflower,
he considered them,
Before flowers
along with angiosperms,
Although they have yet
as comprising a single
to find the oldest fossil
angiosperm entity called
Larger than life. Although merely
flowers, researchers
anthophytes. For the next
2.2 millimeters in diameter, this 3D
assume that the ancesdecade, most family trees
fossil flower shows that grasses date
tral angiosperm evolved
based on morphology supback to 94 million years ago.

We are realizing that this

huge diversity is probably
the result of one innovation piled on top of
another innovation.

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29

ORIGINS

ORIGINS

Angiosperms

such a causal relationship is not settled. Later, animals that ate fruit and
SEED PLANT
Paleozoic seed ferns
dispersed seeds likely helped evolvPHYLOGENY
ing species expand quickly into new
Asterids
territory. Some think the answer lies
Eudicots
in genes: duplications that gave the
angiosperm genome opportunities to
Rosids
try out new floral shapes, new chemical attractants, and so forth. This
Monocots
flexibility enabled angiosperms to
exploit new niches and set them up
for long-term evolutionary success.
Magnolias
My own view is that in the past, we
have looked for one feature, says
Crane. Now, we are realizing that
Water lilies
this huge diversity is probably the
result of one innovation piled on top
?
of another innovation.
Archaefructus
The latest insights into diversification come from gene studies. From
Amborella
2001 to 2006, Pamela Soltis of the
FLMNH and Claude dePamphilis
?
of Pennsylvania State University,
Caytonia
University Park, participated in
the Floral Genome Project, which
?
Bennettitales
searched for genes in 15 angiosperms.
Now as a follow-up, the Ancestral
Angiosperm Genome Project looks
at gene activity in five early angioCycads
sperms and a cycad, a gymnosperm.
DePamphilis and his colleagues
Ginkgoes
matched all the genes in each
species against one another to deter? Gnetales
mine the number of duplicates. They
then looked at the number of differences in the sequences of each gene
Conifers
pair to get a sense of how long ago
Extinct taxa
the duplication occurred. In most
early angiosperms, including water
lilies and magnolias, they saw many Shifting branches. As this simplified family tree shows, gene studies have helped clarify the relationships of many
simultaneous duplicationsbut not living angiosperms, but fitting in extinct species is still a challenge, and some nodes are hotly debated.
in Amborella, they reported in the
January 2009 American Journal of Botany,
The Floral Genome Project also looked are not as well-defined as they are in Araconfirming earlier reports. The data suggest to see whether the genetic programs guiding bidopsis. This sloppiness may have made
that a key genome duplication happened flower development were consistent development flexible enough to undergo
after the lineage leading to Amborella split throughout the angiosperms. We found that many small changes in expression patterns
off but before water lilies evolved. Were there are fundamental aspects that are con- and functions that helped yield the great
beginning to get the idea that polyploidiza- served in the earliest lineages, says Soltis. diversity in floral forms.
tion may have been a driving force in creat- But there are differences in how the genes
In his letter to Hooker, Darwin wrote
ing many new genes that drive floral devel- are deployed.
that he would like to see this whole probopment, dePamphilis says.
Take the avocado, a species on the lower lem solved. A decade ago, Crepet thought
Others have noted that a duplication branches of the angiosperm tree. In most Darwin would have gotten his wish by now.
occurred in the evolution of grasses, and the angiosperms, the flower parts are arranged in That hasnt happened, but Crepet is optiFloral Genome Project confirms that yet concentric circles, or whorls, around the mistic that he and his colleagues are on the
another duplication paved the way for eudi- carpels, with stamens innermost, then petals, right track, as analyses of various kinds of
cots, the group that includes apples, roses, and finally sepals. Each tissue has its own data become more sophisticated. We are
beans, tomatoes, and sunflowers. There are distinct pattern of gene expression, but not less likely to go around in circles in the next
some real hot spots in angiosperm evolu- in the avocado. Genes that in Arabidopsis 10 years, he says. I believe a solution to
tionary history, says dePamphilis, who is are active only in, say, the developing petals the problem is within reach. The mystery
working to fully sequence the genome of spill over in avocado to the sepals. Thus in is solvable.
ELIZABETH PENNISI
Amborella with his colleagues.
the more primitive plants, petals and sepals

Flowers, food, fuel.

at the
the diversity
diversityofofangiosperms.
angiosperms.Given
Given that
they represent
nine
in 10and
landsense
plants,
its no surprise
as
fuel. Darwin
Darwin marveled
marveled at
mainstays
of both our
welfare
of beauty.
Clockwisethat
fromthey
left:serve
aspens,
that they represent
ninewelfare
in 10 land
no surprise
that they
as aspens,
orchids,orchids,
grasses,grasses,
sunflowers,
tulips, apples,
mainstays
of both our
and plants,
sense ofitsbeauty.
Clockwise
fromserve
top left:
sunflowers,
tulips,walnuts.
apples, walnuts.

12
30

Inside and out. Synchrotron radiation helped produce a 3D rendering (gold) of this fossil male flower
(right) and insights into its internal structure.

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CREDITS: (ARCHAEFRUCTUS IMAGE) DAVID DILCHER; (ALL OTHER IMAGES) PHOTOS.COM

Seeds of success
The angiosperms ancestor may be missing,
but what is very clearand was quite
annoying to Darwinis that the angiosperm prototype so readily proved a
winner. Seed ferns and
other gymnosperms
arose about 370
million years ago
and dominated the
planet for 250 million years. Then in a
few tens of millions
of years, angiosperms edged them

out. Today, almost nine in 10 land plants

are angiosperms.
The exact timing of the angiosperms
explosion and expansion is under debate, as is
the cause. At least one estimate based on the
rate at which gene sequences changethat
is, the ticking of the molecular clock
pushes angiosperm evolution back to 215
million years ago. There appears to be a
gap in the fossil record, says Donoghue,
who also notes that molecular dating methods are still in their infancy and, thus,
could be misleading. He and others think
that flowering plants lingered in obscurity
for tens of millions of years before radiating
toward their current diversity.
Whatever the timing, there was something special about the angiosperm radiation. During the 1980s and again in 1997,
Cornells Karl Niklas compiled a database
showing the first and last occurrences of
fossil plants. When he and Crepet used that
and more recent information to look at
species appearances and disappearances,
they found that new angiosperms appeared
in bursts through time, whereas other plants,
such as gymnosperms, radiated rapidly only
at first. Moreover, angiosperms proved less
likely to disappear, somehow resisting
extinction, says Crepet.
Once the angiosperms arrived, how did
they diversify and spread so quickly? Darwin
suspected that coevolution with insect pollinators helped drive diversification, though

CREDITS
CREDITS (TOP
(TOP TO
TO BOTTOM):
BOTTOM): PHOTOS.COM;
PHOTOS.COM; ELSE
ELSE MARIE
MARIE FRIIS
FRIIS

work points you in another direction,

Crane says.
And if the molecular work is correct,
then the field doesnt know in which direction to turn, because in most analyses the
genetic data dont place any living plant
close to angiosperms. The angiosperms
group together, the living gymnosperms
group together, and theres nothing in
between. The nonangiosperm ancestor just
isnt there, says paleobotanist William
Crepet of Cornell. Im starting to worry
that we will never know, that it transformed
without intermediates.

Living
gymnosperms

ported this idea. Crane and others carefully

dissected and described fossils of these
groups, looking for the precursors to
carpels, the seeds double coat, and other
distinctive angiosperm traits.
But they have run into problems. We do
not really know how to compare them
because the structures are very differentlooking; figuring out whats homologous is
quite a difficult thing, says Crane. He and
his colleagues argue, for example, that the
seeds in the Bennettitales have two coverings, which may be a link to angiosperms.
But in the January American Journal of
Botany, Gar Rothwell of Ohio University,
Athens, and two colleagues disagree, saying that what Crane calls the outer layer is
the only layer, and f ind
fault with the hypothesis
in general.
To make matters
worse for anthophyte
proponents, genebased evolutionary
trees break up this
grouping, pulling the
Gnetales off any
angiosperm branch
and placing them
among or next to the
other gymnosperms.
The molecular work
points in one direction; the paleobotanical

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31

TIVES
PERSPECTIVES

HISTORY
HISTORY OF
OF SCIENCE
SCIENCE
HISTORY
OF
SCIENCE

atmospheric, oceanic, geological, ecological,

and cultural phenomena across the globe. Humboldts obsession with geographically referenced measurements and collections was central
to his vision. He recognized that spatial arrays
of observations could be aggregated to reveal
patterns that would in turn reveal underlying
processessuch as the distribution of incident
radiation, the transport of heat and materials in
winds and ocean currents, the influence of temperature on plant form, and the effect of latitude
and continentality on mountain snowline.
He expanded this vision in the succeeding
years, establishing international cooperative
networks of meteorological and geomagnetic
measurement stations, inventing isotherms and
other graphical devices to portray spatial patterns, and noting that plant form is often better
predicted by local environment than by taxonomic affinity (a paradox resolved by Darwin).
Humboldts genius lay in his geographical vision, and in his intuition that Earths land surface, oceans, atmosphere, and inhabitants form
an integrated whole, with linkages among the
various components (4, 5). Humboldts general
physics of the Earth envisioned climate as a
major control of Earth-surface phenomena, with
vegetation serving as both an index of climate
and a proximal control of microclimate, animal
habitat, and cultural practices (68).
Humboldts dream of systematic observational arrays across the globe took hold in the
19th century. Throughout the century, countless
Humboldt-inspired explorations were launched,
each involving systematic measurement and
mapping of physical, biological, and often cultural features of landscapes and oceans (810).
These surveys were relentlessly inductive,

von
Humboldt and
vonAlexander
Humboldt
and
the General
Physics
l Physics
of the
Earthof the Earth

In
early
In the
the
early 19th
19th century,
century, Alexander
Alexander von
von
In the early 19th century,
Alexander
von
In
the
early
19th
century,
Alexander
von
Humboldt
laid
the
foundations
Humboldt
laid
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foundations
for todays
todays
Humboldt laid
the
foundations for
for
todays
Humboldt laid the foundations
for
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Earth
Earth system
system sciences.
sciences.
Earth
system
sciences.

Earth system sciences.

Stephen
Stephen T.
T. Jackson
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Stephen
T.
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with geographi14
596
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1
2009
VOL
www.sciencemag.org
MAY
2009 resolved
VOL 324
324 bySCIENCE
SCIENCE
www.sciencemag.org
11 MAY
MAY
2009
VOL
324
SCIENCE
www.sciencemag.org
taxonomic affinity (a
paradox
with little
integration within or among the com-

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FROM
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CREDIT:
REPRODUCED
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ININ
THE
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HISTORY
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sss scientists
scientists are
are celebrating
celebrating the
the 200th
200th
scientists
are
celebrating
the
200th
anniversary
of
Charles
Darwins
anniversary of
of Charles
Charles Darwins
Darwins birth
birth
anniversary
birth
rating the 200thand
and the
the 150th
150th anniversary
anniversary of
of the
the pubpuband
the
150th
anniversary
of
the
publication
s Darwins
birthof
lication
of his
his On
On the
the Origin
Origin of
of Species,
Species,
lication
of
his
On
the
Origin
of
Species,
Darwins
rsary of the
pub- ideas
Darwins
ideas continue
continue to
to shape
shape and
and enrich
enrich
Darwins
ideas
continue
to
shape
and
enrich
the
sciences
(1).
6
May
2009
marks
the sciences
sciences (1).
(1). 66 May
May 2009
2009 marks
marks the
the 150th
150th
the
the
150th
gin of Species,
anniversary
of
the
death
of
another
19th-cenanniversary
of
the
death
of
another
19th-cenanniversary
of
the
death
of
another
19th-cenhape andtury
enrich
tury figureAlexander
figureAlexander von
von Humboldt
Humboldt
tury
figureAlexander
von
Humboldt
marks the
150th
whose
scientific
whose
scientific legacy
legacy also
also flourishes
flourishes in
in the
the
whose
scientific
legacy
also
flourishes
in
the
21st
century.
Humboldt
helped
create
nother 19th-cen21st century.
century. Humboldt
Humboldt helped
helped create
create the
the
21st
the
intellectual
n Humboldt
intellectual world
world Darwin
Darwin inhabited,
inhabited, and
and his
his
intellectual
world
Darwin
inhabited,
and
his
writings
inspired
Darwin
to
embark
writings
inspired
Darwin
to
embark
on
on
flourisheswritings
in the inspired Darwin to embark on
H.M.S.
Beagle.
More
pertinent
to
our
time,
H.M.S.
Beagle.
More
pertinent
to
our
time,
H.M.S.
Beagle.
More
pertinent
to
our
time,
lped create
the
Humboldt
Humboldt established
established the
the foundation
foundation for
for the
the
Humboldt
established
the
foundation
for
the
habited, Earth
and
his
system
sciences:
the
integrated
system
Earth system
system sciences:
sciences: the
the integrated
integrated system
system
Earth
of
on
to embark
on
of knowledge
knowledge
on which
which human
human society
society may
may
of
knowledge
on
which
human
society
may
depend
depend
in the
the face
face of
of global
global climate
climate change.
change.
ent to our
time,in
depend
in
the
face
of
global
climate
change.
Darwin,
Like
Darwin, Humboldt
Humboldt undertook
undertook aaa
Like
Darwin,
Humboldt
undertook
undationmajor
forLike
the
voyage
that
would
shape
major voyage
voyage that
that would
would shape
shape his
his ideas
ideas
his
ideas
tegrated major
system
and
thinking.
Humboldt
spent
5
years
and
thinking.
Humboldt
spent
5
years
(1799
and thinking. Humboldt spent 5 years (1799
(1799
man society
maywith
to
to 1804)
1804)
with botanist
botanistAim
Aim Bonpland
Bonpland explorexplorto
1804)
with
botanist
Aim
Bonpland
exploring
Venezuela,
the
northern
limate change.
ing Venezuela,
Venezuela, the
the northern
northern Andes,
Andes, and
and cencening
Andes,
and
central
tral Mexico,
Mexico,
with visits
visits to
to Tenerife,
Tenerife, Cuba,
Cuba, and
and
dt undertook
a with
tral
Mexico,
with
visits
to
Tenerife,
Cuba,
and
the
United
theideas
United States.
States. They
They collected
collected botanical,
botanical,
United
States.
They
collected
botanical,
hape histhe
zoological,
zoological, geological,
geological, and
and ethnological
ethnological specspecgeological,
and
ethnological
specnt 5 yearszoological,
(1799
imens,
made
extensive
atmospheric
imens, made
made extensive
extensive atmospheric
atmospheric and
and geogeo- Intellectual
imens,
and
geoIntellectual riches.
riches. The
The central
central portion
portion of
of Humboldts
Humboldts Physical
Physical Tableau
Tableau of
of the
the Andes
Andes and
and Neighboring
Neighboring
Intellectual
riches.
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central
portion
of
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Physical
Tableau
of
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Andes
and
Neighboring
Bonplandphysical
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and recorded
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the Countries,
published
as
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(2,
3),
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in
profile,
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Countries,
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(2,
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Countries,
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3),
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plant
species,
and
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erife, Cuba,
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ments.
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and
other
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ments.
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ments.
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ected botanical,
most
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his inherited
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in Paris,
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specparing
and
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45
volumes
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paring
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finished
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curimal
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curimal
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Intellectual
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of the Andes
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entitled
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e in Paris,
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atmospheric,
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the Origin
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system of(68).
22
the Earth on
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ically
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raphy ofcally
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6 May
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the 150th anniversary
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tions
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ally
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ander
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entitled
on
umboldt also
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northern
Andes,
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Mexico, with
In the text
and accompanying
color
the
g less than a syn- measurement stations, inventing
isotherms
mapping
of
physical,
biological,
and
often
cul5).
Humboldts
general
physics
of
the
Earth
ence
that
spurred
the
development
of
biogeog5).
Humboldts
general
physics
of
the
Earth
ence
that
spurred
the
development
of
biogeogCuba,
and
the
United
States.
plate
(see
the
figure),
Humboldt
lays
out
a vivisits
to
Tenerife,
5).
Humboldts
general
physics
of
the
Earth
ence
that
spurred
the
development
of
biogeogBotany
Department
and
Program
in
Ecology,
University
of
Botany Department
Department and
and Program
Program in
in Ecology,
Ecology, University
University of
of
Botany
envisioned
climate
as
aaa major
control
of
raphy,
oceanography,
and
other
envinic, geological,
and
other
graphical
devices
toThey
portray
spatial
features
of landscapes
oceans
(810).
Wyoming,
envisioned
climate
astural
major
control
of sion
raphy,
ecology,
oceanography,
and
otherof
envigeological,
general
physics
the
collected
botanical,
zoological,
of ecology,
aand
comprehensive
envisioned
climate
as
major
control
of
raphy,
ecology,
oceanography,
and
other
enviWyoming, Laramie,
Laramie, WY
WY 82071,
82071, USA.
USA. E-mail:
E-mail: jackson@
jackson@
Wyoming,
Laramie,
WY
82071,
USA.
E-mail:
jackson@
uwyo.edu
Earth-surface
phenomena,
vegetation
ronmental
sciences
(11).
uwyo.edu
Earth-surface
phenomena,
with
vegetation
ronmental
sciences
(11).less
omena across
the patterns, and noting that plant
and
ethnological
specimens,
made
extensive
Earth
aimed
at nothing
than a synthesis of
form
is often
Thesewith
surveys
were relentlessly
inductive,
typuwyo.edu
Earth-surface
phenomena,
with
vegetation
ronmental
sciences
(11).

typically producing detailed descriptive reports

with little integration within or among the component entities. However, for a few intellectually nimble participantsincluding Charles
Darwin, T. H. Huxley, Matthew Maury, Asa
Gray, C. Hart Merriam, and Peter Kropotkin
these explorations provided data and experience
that spurred the development of biogeography,
ecology, oceanography, and other environmental sciences (11).
Unfortunately, the conceptual unification
among the sciences of the Earth that Humboldt
sought never developed in the century following his death. Disciplinary specialization played
a large role in eclipsing Humboldts integration,
as did 20th-century trends toward reductionism,
experimentalism, and fine-scale processes in
many disciplines.
A new incarnation of Humboldts general
physics of the Earth began to emerge with the
plate tectonics revolution in the 1960s. Drawing on Humboldtian spatial arrays of observations, this theory provided a unified explanatory
framework for disparate geophysical, geological, paleontological, and biogeographic phenomena.
Today, a second, even broader manifestation
of Humboldts vision aspires to understand the
interactions and feedbacks among the components of the Earth system, encompassing the
lithosphere, atmosphere, hydrosphere, cryosphere, and biosphere as well as human societies
and economies. This effort is often referred to as
Earth system science, but it could just as well be
designated general physics of the Earth, using
the early-19th century definition of physics as
the study of the material world and its phenomena (which we now call science).

Global environmental change may be the

greatest challenge faced by human societies
since the advent of agriculture. Humboldt advocated for science that spoke to human needs
and concerns (5). It is fitting that on the 150th
anniversary of his death, we recognize his role
in fostering the sciences that speak to the most
profound human concernssustainability of
human societies and the ecosystems on which
they depend.
References and Notes

1. P. J. Bowler, Science 323, 223 (2009).[Abstract/

FreeFullText]
2. A. de Humboldt, Essai sur la gographie des
plantes (Levrault, Schell & Co., Paris, 1807).
3. An English translation of (2) is currently in
press at the University of Chicago Press, Chicago.
4. A. de Humboldt, Personal Narrative of Travels to the Equinoctial Regions of the New
Continent, During the Years 17991804, by
Alexander de Humboldt and Aime Bonpland;
with Maps, Plans, &c. (Longman, Hurst, Rees,
Orme, & Brown, London, 1814 to 1829), vols.
1 to 7.
5. A. von Humboldt, Cosmos: A Sketch of the
Physical Description of the Universe (Johns
Hopkins Univ. Press, Baltimore, 1997), vol. 1.
6. M. Nicolson, Hist. Sci. 25, 167 (1987). [ISI]
7. M. Nicolson, in Romanticism and the Sciences,
A. Cunningham, N. Jardine, Eds. (Cambridge
Univ. Press, Cambridge, 1990), p. 169.
8. M. Dettelbach, in Cultures of Natural History,
N. Jardine, et al., Eds. (Cambridge Univ. Press,
Cambridge, 1996), p. 287.
9. S. F. Cannon, Science in Culture: The Early
Victorian Period (Dawson, New York, 1978).
10. W. H. Goetzmann, New Lands, New Men:
America and the Second Great Age of Discovery (Viking, New York, 1986).
11. P. J. Bowler, The Norton History of the Environmental Sciences (Norton, New York, 1993).

In the early 19th century, Alexander von

Humboldt laid the foundations for todays
Earth system sciences.

15

BOOKS ET AL.
mer students who challenged
his ideas as they gained intellectual independence, and
debated the pro-evolution
(but anti-Haeckel) Jesuit priest
and entomologist Erich Wasby Robert J. Richards
mannthe list could go on
University of Chicago
and on. These were not isoPress, Chicago, 2008.
duced important books. Robert
lated episodes but rather
579 pp. $39, 27.
J. Richards, the director of the
moments in a lifelong camISBN 9780226712147.
University of Chicagos Fishpaign to advance his philosobein Center for the History of
phy, which was accompanied
H. G. Bronn,
Science and Medicine and a
by a bitter hostility to orgaErnst Haeckel, and
much-published author on Darwin
nized religion.
the Origins of
and German Romantic biology,
Richards does not negGerman Darwinism
has written a biography of Haeclect Haeckels science proA Study in Translation
kel. Sander Gliboff, a professor
per, treating us to fascinatand Transformation
in Indiana Universitys Departing and original discussions
ment of History and Philosophy
of his pathbreaking systemby Sander Gliboff
of Science, places Haeckel at the
atic and phylogenetic work
MIT Press, Cambridge, MA,
end of a study that examines the
on radiolaria and other marine
2008. 271 pp. $35, 22.95.
larger process through which
organisms, the importance
ISBN 9780262072939.
Darwins words were translated,
of linguistic analysis to his
and his ideas modified, in the
phylogenetic trees of the
context of German biology. Both illuminate races of humans, and his remarkable experithe twists and turns that evolutionary thought mental work with siphonophores. These contook in Germany, but they do so in dramati- stitute important contributions to our undercally different ways.
standing of the technical development of
Richardss book, though over twice as long evolutionary biology.
as Gliboffs, is the more entertaining read of
The big picture here, however, is an arguthe two. In his characteristically rich and ment about the power of personalityat least
rolling prose, Richards weaves a compelling one personalityto shape the course of scistory of a life marked by tragedy and of an ence. In Richardss presentation, German evointense, larger-than-life figure whose passions lutionism was profoundly shaped by both
drove his scientific research and philosophy. In Haeckels charisma and his combativeness.
Richardss rendering, the scientific Haeckel Perhaps the late-19th-century opposition of
cannot be understood separately from the evolutionary science to Christianity would not
mans personality and private circumstances. have been so fiery, he suggests, had Haeckel
His love of nature was surpassed only by his not continually fanned its flames. And
love for his first wife, Anna Sethe, who died in although Richards absolves Haeckel of perabdominal agony on his 30th birthday. Over sonal responsibility for fascism and Nazism,
the next year, he wrote his way through the in part by situating him firmly in his time and
despair that enveloped him, producing his place, he does show how the scientists ardent
foundational work, Generelle Morphologie temperament led him to the occasional intem(1). Although he remarried, the union was not perate statement that could be taken up by
happy, and passionate love would elude him extreme thinkers. One cannot leave this book
until his sixties, when he had a secret affair that without a deep appreciation for Haeckel as a
ended tragically with the death of his lover. tragic figure and for the force of personality in
Science remained his salvation and refuge.
shaping the direction science may take.
His professional life was also filled with
Gliboffs account is of a completely differdrama, much of which centered on his philos- ent order. His is not a story of personalities or
ophy of evolutionary monisma science- private lives (although he mentions salient
centered faith that became one of the most details), but of German academics seeking to
successful alternatives to the Judeo-Christian live up to the highest (if changing) ideals of
religion among those searching for a secular Wissenschaft and of the ways in which
spirituality. Haeckel could not turn down a Darwins theory was translated into this envifight: He battled the physician-statesman ronment. He thus situates Haeckel at the end
Rudolf Virchow over the role of evolution in of a revised intellectual history of 19ththe schools (Haeckel argued that it should century German evolutionism. Central to his
replace religious education), sparred with reli- account is the idea of translation, which he
giously conservative scientists and with for- uses both synchronically, especially in treatThe Tragic Sense of Life
Ernst Haeckel and
the Struggle over
Evolutionary Thought

Making German Evolution:

Translation and Tragedy
Lynn K. Nyhart

n this year of Darwin anniversaries (the

200th year of his birth and the 150th
anniversary of On the Origin of Species),
The Tragic Sense of Life and H. G. Bronn,
Ernst Haeckel, and the Origins of German
Darwinism remind us that the history of evolutionary thought in the 19th century extended
well beyond Darwin himself. Darwin did not
launch his theory onto an unprepared public
and scientific community, nor was the evolutionism that developed after 1859 a mere
extension of his viewsit was not even one
thing. How, then, should we think about the
history of evolution in the 19th century? What
sorts of accounts best help us understand the
reception of Darwins theory, its relations to
earlier ideas about nature, the directions that
evolutionary investigation subsequently took,
and the relations of all of these to the broader
social, cultural, and religious concerns scientists shared with their contemporaries?
These questions become especially pointed
when one considers German Darwinism, and
especially Germanys best-known follower of
Darwin, Ernst Haeckel. Most often remembered by biologists as the author of the biogenetic law (ontogeny recapitulates phylogeny), Haeckel has also been accused of
promoting European fascism via his monistic
philosophy and of presenting a eugenic, biologically determinist vision of humanity that
led to Hitlers final solution. Can one scientist be responsible for so much? Most historians would say no, arguing that it takes a community, rather than an individual, to make a
movement; that single-cause explanations are
insufficient to account for something as broad
as fascism; and that an individual cannot be
held responsible for the ways in which others
(such as Hitler) took up his ideas and molded
them to new agendas after his death. But that
still leaves open the questions of how to write
responsibly about what Haeckel actually
believed and how we should situate him in the
history of evolutionary thought.
The historians under consideration here
have chosen two radically different strategies
to understanding Haeckels place within
German evolutionism, and both have proThe reviewer is at the Department of the History of Science,
University of Wisconsin, Madison, WI 537061393, USA.
E-mail: lknyhart@wisc.edu

16

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27 FEBRUARY 2009

VOL 323

SCIENCE

www.sciencemag.org

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

HISTORY OF SCIENCE

BOOKS ETAL.
ing the translation of Origin of Species into translations involved an attempt to recast existGerman, and (more intriguingly) diachroni- ing German terms in a newer, more up-to-date
cally, as scientists reworked older words such mode that encompassed selection yet tamed
as perfection and type to lend them new Darwins emphasis on unpredictability to meet
meanings. Gliboffs own clear, crisp prose is the more rigorous requirements of a German
key to the success of this analysis, as he deftly academic scientists understanding of a law
leads his reader through dense philosophical of organic nature. Simultaneously, Bronn
and terminological thickets with nary a thorn sought to translate Darwins ideas about selecscratch. This is some of the best close reading tion into a language without an exact equivaI have seen. It also represents a profound chal- lent for the term, and for an academic audience
lenge to our standard picture of 19th-century lacking the gentlemanly traditions of breeding
German biology.
pigeons and dogs so central to Darwins expoThe old story, crudely put, is that Haeckels sition. The selection metaphor was further
version of evolution was a Darwinism in name fraught with an anthropomorphism foreign to
only, best understood as an update on early- Germans, who were not brought up on British
19th-century idealistic morphologists such natural-theological assumptions about a peras Carl F. Kielmeyer and J. F. Meckel that sonified God who had created a perfectly
retained their teleology, their typological adapted nature. Bronns translation, though it
emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehentionism. This story, emphasizing the long per- sible to a German academic audience, was not
sistence of a German transcendental approach a conservative throwback. It represented the
to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolohistory of biology.
gist who had also long been working on many
Gliboff challenges this history right from of the questions Darwin claimed as his own
the beginning. The ascription of simple linear a critical yet generous equal, who saw himself
recapitulationism to the views of Romantic as moving science forward through the modiembryologists, he notes, owes much to a carica- fications he made to Darwins flawed theory.
ture developed by Karl Ernst von Baer in a Bronns death in 1862 afforded him little
polemical context, then adopted uncritically by chance to steer the conversation further.
influential historians such as E. S.
Russell and Stephen Jay Gould.
Gliboffs fresh reading of the original sources interprets Kielmeyer
and Meckel as far less rigidly
typological in their orientation and
much more attentive to natures
variability than has been seen
before. Both for these early-19thcentury naturalists and for their
intellectual heirs, Gliboff argues,
the critical issue was to understand
natures manifold variety while
seeking out underlying strict natural laws to account for it.
This provides a new starting
point for analyzing Darwins first
translator, the prominent paleontologist H. G. Bronna figure little attended to in the standard
story but the lynchpin of Gliboffs. Intriguingly and plausibly,
Gliboff argues that Bronns use
of terms like vervollkommnet
(perfect) as translations for Darwins improved or favored
were not about dragging Darwin
backward into a German teleological view of nature (as has
been claimed by those who have
paid attention to Bronn at all). A painter, too. Haeckels oil landscape of highlands in Java, from
Instead, Gliboff asserts, Bronns Wanderbilder (1905).
www.sciencemag.org

SCIENCE

VOL 323

And so, finally, we come to Haeckel.

Gliboff s key insight here is that Haeckel
originally read Bronns translation of Darwin,
not Darwin in the original. Gliboff shows
Haeckel as both echoing and responding to
Bronns concerns, rather than either reflecting directly on Darwins original writing or
reaching directly back to the Romantic
embryologists. (Although Gliboff acknowledges the centrality of monism to Haeckels
thought, he focuses on the working evolutionary theorist, not the popular ideologue.) Like
Bronn himself, Haeckel made further amendments both terminological and intellectual,
and Gliboff rereads Haeckels research program as one not dominated by a typological
and linear-recapitulationist mindset but
rather as continuing to wrestle with the need
to account for variability and unpredictable
change in terms of mechanistic laws of
natureamong which Haeckel included, at
the top of his list, natural selection. Haeckels
Darwinism thus shows continuity with early19th-century concerns, mediated through
Bronn. But those concerns were always more
flexible than has been acknowledged, and
their articulation changed over time. Of
course Haeckels Darwinism was not
Darwins own, but it was not an aberration or
a distortion of some true theory, any more
than any other post-Darwinian additions or
adjustments were. It was science moving on.
Gliboff s overall picture of scientific
advance, in contrast to Richardss emphasis on
charisma and passion, is one of scientists
building and innovating incrementally, working with what their predecessors have handed
them and sculpting it into something new yet
understandable to those around them. His sensitive reading allows us to see post-1859
German evolutionists as rational actors rather
than irrationally stuck in some early-19thcentury moment with unmodern commitments. By challenging the very foundations of
the standard narrative of German morphology, this careful, compelling account does at
least as much as Richardss to undermine the
association of 19th-century German Darwinism with a dangerously exceptional view of
nature. But the two books offer very different
reads. Is scientific progress a matter of personal anguish and triumph, or of intellectual
chugging along? Our concept of it should be
capacious enough to include both.
References and Notes
1. E. Haeckel, Generelle Morphologie der Organismen
(Georg Reimer, Berlin, 1866).
2. The reviewer previously served as a press reader for both
books at the manuscript stage.

27 FEBRUARY 2009

10.1126/science.1169621

17

1171

REVIEW
REVIEW

up, in explaining
this case bypresent
in- distribuby something
(later identified
as genetic(the
mutascience,
shaped
by the organisms
own activities
so- vancing through a predetermined sequence of ulation became divided
oceanicofislands.
tions),
but it was effect),
not aimed
anytoo
onepermitted
direction stages within each family, driven by force derived dependent acts of migration
opments that would push other naturalists toward
tions into terms
past migrations,
called
Lamarckian
butinthis
Here, Darwin followed
Lyell in seeing
that Darwin
bioand, thus,
left adaptive
evolution
essentially
an evolutionary vision during the years he worked
extinctions
and (for
but not
multiple
vectors
of change.
Evolution
hadopento be from individual development.
REVIEW
opments that would push other naturalists toward
geography must become a historical
ended. He allowed a limited role for variation
in isolation. By the late 1850s, the idea of profor
Lyell)
evolutionary
adaptations.
depicted
as
a
branching
tree
in
which
each
act
of
an evolutionary vision during the years he worked
science, explaining present distribushaped by the organisms own activities (the sogressive
evolutionhiswastheory
widelytorecognized,
andorderly
the
by geographical
branching
was thevariants
result
ofin
a amore
less was
unpredict
an
pattern of
proposals
of the individual variants in a population was the relations among species. Several
in
Byevolution
the late 1850s,
the
idea
of
protions
in Populations
terms
pastdivided
migrations,
called
Lamarckian
effect),
but
this
tooorpermitted
was widely
recognized,
It has
been ofargued
that Darwins
move
of isolation.
progressive
of the
individual
population
positive
role
of
individual
competition
was
being
opments
that
would
push
other
naturalists
toward
barriers
will
develop
independently
predictable
migration
of
organisms
to
a
new
locarelations.
away
essentially undirected ruled out any possibility available in the 1830s deflected attention
opments
that
would
push
other
naturalists
toward
extinctions
and
(for
Darwin
but
multiple
vectors
of
change.
Evolution
had
to
be
gressive
evolution
was
widely
recognized,
and
the
was inspired
and the positive role of individual competition
essentially undirected ruled out any possibilto a more historical viewpointnot
articulated
by thinkers
such
as argued
Herbert
Peter J. Bowler that evolution could be shaped by a predeter- from the model of the branching
an
evolutionary
vision
during
the
years was
he Spencer
worked
asevolutionary
each
adapts
to its new environtion.depicted
At the same
time, Darwins
undermined
Itby
has
been
Darwins move to a
tree
(11).
for
Lyell)the
adaptations.
as a branching
treeshaped
intheory
whichby
each
act of
an evolutionary visionby
during
years
he worked
positive
role
of individual
competition
being
was
being
articulated
thinkers
such asthat
Herbert
could be
a predeGerman
romanticism
[e.g. (12)], but a
ity that evolution
(Fig.
1). But
keymore
aspects
of the viewpoint
Darwinian
vision
in
isolation.
By
the
late
1850s,
the
idea
of
proment
in
its
own
way, and the posthe
old
idea
that
species
were
idealized
types,
Populations
divided
by
geographical
branching
was
the
result
of
a
more
or
less
unhistorical
was
inspired
by
German
William
Sharp
Macleays
quinary
or
circular
mined
developmental
trend.
There
was
no
obin
isolation.
By
the
late
1850s,
the
idea
of
proarticulated
by
thinkers
such
as
Herbert
Spencer
Peter J. Bowler
But
key
aspects
of
the
Darwinwas
no
incentive
was
provided by
Spencer
(Fig.
1).
termined
developmental
trend.
There
more
practical
were
truly
original
andwidely
wouldrecognized,
not have
occurred
Charles Darwinsvious
theory
of natural
has been
hailed
of theofmost
innovative supposed(Fig.
barriers
will
develop
of organisms
a new order.
locagressive
evolution
was
and
thea more practical
sibility
thatindependently
barriers
be crossed
fixedpredictable
elementsmigration
in a clearly
defined to
natural
romanticism
[e.g.
(12)],
but
system
classification
that
goal
toward selection
which it was
aimed,
and as
it one
gressive evolution wasthe
widely
recognized,
and
the can
1).every
But
keytruly
aspects
of the
Darwinian
vision
and
would
not
have
on the
ian
vision
were
original
obvious
goal
toward
which
it
was
aimed,
and
biogeographical
insights
gained
as
each
adapts
to
its
new
environtion.
At
the
same
time,
Darwins
theory
undermined
to any be
other
naturalist
at the
time.
Here,
Wallace
contributions todid
modern
science. an
When
first pattern
proposed
in
1859, however,
it was widely
rejected
positive
role
of
individual
competition
was
being
occasionally
allows
for
the
branchSpecies
had
to
be
treated
as
populations
of
varyincentive
was
provided
by
the
biogeographical
genus
contained
five
species
that
could
arnot
produce
orderly
of
relations
positive
role
of
individual
competition
was
being
were
trulytooriginal
andnaturalist
would not
have
occurred
Charles Darwins theory of natural selection has been hailed as one of the most innovative
Here,
produce
anspecies
orderlywere
pattern
of relations
occurred
any comparison:
other
at the
time.
Beagle
voyage
(183136).
The
Galapagos
it did
not
ment
in
its
own
way,
and
the
posthe
old
idea
that
idealized
types,
provides
a
good
He
too
moved
toward
by
his
contemporaries,
even
by
those
who
accepted
the
general
idea
of
evolution.
This
article
articulated
by
thinkers
such
as
Herbert
Spencer
ingHerbert
process Spencer
of evolution that Darwin
individuals, with no fixed limit on the range
Peter J. Bowler
insights
gained
onHere,
the Beagle
voyagePeter
(183136).
rangeditinwas
a circle;
each
family five genera,
sonaturalist
species. When
The accusation
that the
theory however,
articulated by thinkers
such provided
as
J. Bowlering
to
any and
other
at the
time.
Wallace
contributions
to between
modern science.
first proposed
in 1859,
widely
rejected
accusation that the theomost
obvious example
Wallace
provides
a good
comparison:
He
too
between
species. inThe
species
sibility that
barriersthe
can
be crossed
fixed elements
the
idea
of branching
evolution
drivenprovided
by
local
identifies those depended
aspects ofonDarwins
work
that led
him to
develop
this
revolutionary
theory, hierarchy.provides
(Fig.
1). aBut
keycomparison:
aspects
of He
the too
Darwinian
vision
conceived
in vision
the
late 1830s. It was
of possible
variation.a clearly defined natural order.
The
Galapagos
species
the most obvious
on of
through
the taxonomic
Chamberss
variation
indicated
con- idea
(Fig.
1).
But
key
aspects
of
the
Darwinian
good
moved
toward
by his contemporaries,
even random
by those who
accepted
the the
general
evolution.
This article
occasionally
allows forwithin
the branchSpecies hadon
to be
treated as variation
populationsindicated
of varythe
idea
of
branching
evolution
group can
be
ry
depended
random
of
how
the
relations
moved
toward
adaptation,
but
even
he
did
not
share
Darwins
including
his
studies
of
biogeography
and
animal
breeding,
and
his
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olence as an explanation of adaptation. Unlike century were introduced with the aim of subvertweRussel
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environment.
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would
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related
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just
why
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theory
was
224
9 JANUARY
2009 his
VOL
SCIENCE
theory
selection
challenged
this
vision
which
he
developed
his
theory
(69).
Darwin
ferences
between
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These rigidly
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taxonomic it in full. Ernst Mayr argued that the theory of
the Darwin
related
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ferent
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9 JANUARY
2009
VOL 323
SCIENCE
hardDarwins
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ed
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paper
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cussed, although generally rejected (24). Robert combination of scientific interests that alerted off useless variations in a ruthless struggle for
generally
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species
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Creation
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cept
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ert
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and
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eclipse
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Darwinism
in
the
ever-changing
environment,
and
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did
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by
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plain
the
history
of
life
on
earth.
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had
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unique
theory,
published
in
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explain
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arrange
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of
Creation
of
1844
sparked
a
debate
over
time,
but
was
forced
by
his
scientific
interests
less
struggle
for
existence.
aptation.
Darwin
was
led
toward
his
alternative
were
introduced
with
the
aim
of
subverting
off
useless
in
a
ruthless
struggle
for
combination
of
scientific
interests
alerted
cussed,
although
generally
rejected
(24).
Robert
achievements,
in
addition
to
natural
selection
on
hazards
of
isolation,
and
local
lying
similarities.
Closely
related
species
have
dioff
useless
variations
in
a
ruthless
struggle
for
combination
of
scientific
interests
that
alerted
cussed,
although
generally
rejected
(24).
Robert
sibility that new species were produced from time, but was forced by his scientific interests to especially because its essentially selfish nature
natural
adaptive
response
in some
circumstances.
inaluse
way.
to
those
sources
ofbyinspiration
in a led
highly
groups,
because
he wasHe
more existence.
interested inThis implications
possibility
that
new
species
produced
from
the
process
that
would
instituted
species
principle
of common descent
model inbypart
existence.
did
not
seem
theitbe
kind
process
him
to
topics
ignored
other
He
Chamberss
Vestiges
ofrecently
thewere
Natural
ofancestor,
itself
(14).
was,
but
I by
think Mayr
over- Vestiges
adaptation.
Darwin
was
towardmeant
hiskind
alternaverged
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aHistory
common
whereas
did not seemof
thethe
kind
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him descent
to topics ignored
other
naturalists.
Chamberss
ofinto
the groups
Naturalwithin
History
of using
School of Philosophy
and Anthropological
Studies,
The Queen's
thatofaThis
parasitic
way
ofSo
life
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aofperfectly
use
those
sources
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innaturalists.
a highly
origMore
seriously
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idea
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teleTo some
Darwin
may
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ones
in
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progressive
sequence
explaincertainly
the underto thebe instituted
American
neo-Lamarckians
Edward
original
way.
a more
benevolent
especially
its
essena common
adaptation
than discussed
cosmic teleology,
pre-existing
(15). Theby
that
would
beGod,
instituted
by
abecause
benevolent
God,
certainly
drew extent,
on
ideas
widely
discussed
thewasnatural
Creation
1844
sparked
a debate
over
the
posUniversity ofof
Belfast,
University
Belfast,
Belfast,
Northern
estimated
the
rapidity
with
which other
naturaltive
model
in part
because
he
interthe
ancestry
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more
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related
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a benevolent
God,
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Creation
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response
in
some
circumstances.
inal
way.must
School
Philosophy
andspecies
Anthropological
The Queen's
ology,selfish
Darwins
supposition
thatselfish
the
production
merely
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develIreland,of BT7
1NN,
UK.
E-mail:
especially
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essentially
nature
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sibility
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meant
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leading
up
tonew
humans
(5).p.bowler@qub.ac.uk
But
lying
similarities.
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related
species
influence
of
William
Paleys
natural
theology.
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Cope
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tially
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ested
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sibility
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More seriously for the idea of cosmic teleTo some extent, Darwin may have been
University of Belfast, University Road Belfast, Belfast, Northern
meant
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aa parasitic
way
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life
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selection
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non-Darwinian
theories
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toof
the
influence
Paleysology,
thethep.bowler@qub.ac.uk
common point of origin. merely
meant that a parasitic
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perfectly
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E-mail:
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inal
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ology.push
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selection
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common
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adaptive series
response
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circumstances.
School of Philosophy and Anthropological
The
Queen's
www.sciencemag.org
SCIENCE
VOL
323have9 been
JANUARYMore
2009seriously for the idea of cosmic tele- 223School of Philosophy and Anthropological Studies, The Queen's inal way.
Toansome
extent,
Darwin
may
More
seriously
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idea
of cosmic
teledown
the
his
theory
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developmental
stages, an updated
ward
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the years
forms
must
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traced
further
back
and
Chambers,
Darwin
did
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expect
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century
were
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of subvertolencevision
as anduring
explanation
of he
adaptation.
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alternative
More
seriously
for
the
idea
of
cosmic
teleTo
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University of Belfast, University
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of Belfast, University Road Belfast, Belfast, Northern
ology,
Darwins ing
supposition
that the
the of
production
ahead
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hisBytime,
anticipating
develIreland, BT7 1NN, UK.
E-mail: p.bowler@qub.ac.uk
223of
www.sciencemag.org
SCIENCE
VOL
323 the
9Darwin
JANUARY
2009
the implications
the principle
common
Macleay
and
Chambers,
not
expect
models
could have been
proposed tomerely
account
isolation.
the
late
1850s,
idea did
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production
ology,
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supposition
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to find the common point
of origin.
to predict
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pattern
of relations.
of the
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worked
infor
ology, Darwinsversion
supposition
thatidea
the production
merely
ahead of
his time,
anticipating
develIreland,
BT7 1NN, UK.
E-mail:tree
p.bowler@qub.ac.uk

Darwins Originality
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Vestiges. The similarities linking the species in directed variation among individual organisms. tion thinking, and although he may have exa genus were due not to a recent common ances- Although convinced that the degree of variabil- aggerated the extent to which Darwin himself
try, but to parallel trends independently reaching ity was artificially enhanced under domestica- made the conceptual transition, the subsequent
the same stage of development. Like Chambers, tion, Darwin, nevertheless, accepted that there development of the selection theory brought this
they endorsed the recapitulation theory (ontog- must be some equivalent variability in every implication out more clearly.
In the debates that followed the publication
eny recapitulates phylogeny, in the terminology wild population. The analogy with artificial seintroduced by Ernst Haeckel) and saw evolution lection then allowed him to depict natural selec- of On the Origin of Species, the analogy with
role
as the addition of preordained stages to ontog- tion as a parallel process in which a few variant artificial selection continued to play a keyREVIEW
eny. Adaptation was not crucial once the basic individuals, in this case with characters useful to by forcing even Darwins critics to think about
descent (15). The American neo-Lamarckians scale and that could be investigated directly. interbreeding individuals. Traditionally, species
character of the group was established, and the species rather than the human breeder, sur- the problems of heredity and variation in a new
Edward Drinker Cope and Alpheus Hyatt pro- There was a well-developed network of breeders were treated as idealized types with a fixed esof the ofgroup
andbe
reproduce.
withalthough
harmfultheir
characthe linear, orthogenetic
vive
way (18).
sence,Opponents
any variationsuch
fromas
theFleeming
norm beingJenkin,
trivial
by this Those
time, and
ideas about
posedevolution
that the evolution
each group
should
byand
thevariation
strugglewere
for existence,
on large
might eventually generate
ters through
are eliminated
who saw
selection working
and impermanent.
The breeders
knewvariations
that they
heredity
distinctly pregenetseen as abizarre
series ofnonadaptive
parallel lines moved
could produce
huge changes
in structure by still
acical (likewill
Darwins
own), they
a very clear
the same
hierarchy of developmental
an the
up- breeder
to extinctionthe
the- stages,
any had
animal
just as
not permit
or sports
of nature,
were, nevertheless,
characters as a prelude
variations over
a number
of
appreciation
of have
how they
produced changes
in cumulating
datedDarwin
version of
the idea
suggested
could
make
no intoChamberss
he working
ory of racial senility.
reproduce if
it does not
the character
within normal
the framework
defined
by this
Vestiges. The similarities linking the species in a their artificially small populations. The insight generations. When Darwin linked this informasense of the theory proposed
by Cope and Hyatt, wants. It was the breeders who taught Darwin analogy. For supporters such as Francis Galton,
genus were due not to a recent common ancestry, that they worked by selection may have been tion with his conviction that species could change
is not directed
preor- among
to was
clarify
nature
because he could notbutimagine
evolutionary
artificial
selection
variation
indefinitely
overhelped
time, he
driventhe
toward
a
(this is toward
the pointsome
of contention
to parallelantrends
independently that
reaching
the important
trends. But Like
the Chambers,
build onnotebooks),
his exist- but of
the popway
dainedthey
goal, allowing
him toDarwins
heredity
selection,
process driven by predetermined
new
form of and
species
concept inpaving
which the
experts studying
theboth
same stage of development.
becomes paramount.
natural rangegeof
breeders
certainly evolution
taught himmust
one be
thing. for
He theulation
the in
recapitulation
theorying
(ontogeny
flourished
the late 19th
fact that such theoriesendorsed
conviction
that adaptive
revolutionary
impact The
of Mendelian
becomes
of theheredity
species character,
that in process.
a domesticated population there
phylogeny,
the terminology
intro- realized
the in
theory
The notion
of part
hard
was incentury demonstratesrecapitulates
just how radical
an open-ended,
branching
netics.variability
duced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental deviations from a
At the same time, the breeders attitude to- troduced in opposition to the soft form of
of open-ended, divergent
evolution was to the
the addition of preordained stages to ontogeny. undirected variation among individual organisms. fixed norm. This is what Mayr called the transiDarwin toward
the view
pushedconvinced
inheritance
implied
by the
Lamarckian
process.
naturalists of the time.
tion from
typological
thinking
to population
thinkthat the degree
of variabilAdaptation was not crucial once theward
basic variation
char- Although
of domestication,
inter- The undirected
natureheofmay
variation
was clarified
that
species
is artificially
just a population
ing, and although
have exaggerated
the
ity was
enhanced under
acter of the group was established, and
the the
linear,
extent to the
which
Darwin
himselfpopulations
made the conDarwin, nevertheless,
accepted that
there mustboth
be through
might even- individuals.
Artificial Selection orthogenetic evolution of the group breeding
study
of large
by
Traditionally,
species
transition, the
the subsequent
of
some
equivalent
variability
every wild
tually
generate
bizarre
nonadaptivewere
characters
These non-Darwinian
models
were
ultimately
idealized
types
with in
a fixed
es- popustudies of the
Galtonceptual
and through
breeding development
treated as
as a prelude to extinctionthe theory of racial lation. The analogy with artificial selection then the selection theory brought this implication out
synthesis
of the selection sence, any variation from the norm being trivial geneticists. Although it took some time for the
marginalized by thesenility.
Darwin could make no sense of the allowed him to depict natural selection as a par- more clearly.
century.
geneticists
to accept
studies
theory and genetics theory
in theproposed
early 20th
impermanent.
The breeders
that they
In the
debates the
that situation,
followed thetheir
publication
in which aknew
few variant
individuals,
by Cope
and Hyatt,and
because
he allel process
ultimately
Darwins
Genetic mutations seemed
toimagine
be essentially
plu- process
coulddriven
produceinhuge
changes
in structure
of mutation
of On the
Origin ofendorsed
Species, the
analogyclaim
with
this case
with characters
usefulby
to acthe species
could not
an evolutionary
artificial
selection
to play
a keyaffect
role
rather than
the human
survive
re- the
by providing
predetermined
But the fact
that such normal
justtrends.
the source
variations
overbreeder,
a number
of and that
could
only way
the continued
environment
ralistic and undirected,
cumulating
by forcing was
evenby
Darwins
criticsModern
to thinkevoluabout
Those withlinked
harmfulthis
characters
flourishedmechanism
in the late 19th century
dem- produce.
that Darwins
infor-are elimof random variationtheories
generations.
When Darwin
the population
selection.
onstrates just how radical the theory of open- inated by the struggle for existence, just as the the problems of heredity and variation in a new
required as its raw ended,
material.
This later devel- mation with his conviction that species could tionary developmental biology has reopened the
divergent evolution was to the naturalists breeder will not permit any animal to reproduce if way (18). Opponents such as Fleeming Jenkin,
over
he was
driven
evolution
can
opment highlights the
importance
of another change indefinitely
whether
variation
selection
working and
on large
variations
it does not
have time,
the character
he wants.
It wasquestion
the whoofsaw
of the
time.
species
in variation
which is be
form ofwho
as open-ended
Darwin
and his still
folinsight gained by Darwin in the late 1830s, his toward a newbreeders
or sports
of nature,aswere,
nevertheless,
taughtconcept
Darwin that
not quite
Artificial
Selection
within
framework
defined by
this
toward
some preordained
goal, allowing
of the animal the populationdirected
The natural
believed.
Butthethe
non-Darwinian
vision
decision to investigate
the work
becomes
paramount.
lowersworking
analogy.unfolding
For supporters
as Francis
Galton,
him to build
on hispart
existing
conviction
that adaptThese
non-Darwinian
models
ultimately
theirwererange
to ansuch
orderly,
predictable
breeders (Fig. 3) and his recognition that
of variability
becomes
of the
species
of evolution
marginalized by the synthesis of the selection ive evolution must be an open-ended, branching artificial selection helped to clarify the nature
method of artificial theory
selection
offered a useful character, not the result of accidental deviations plan has
been essentially marginalized by accepof both heredity and selection, paving the way
and genetics in the early 20th century. process.
how the
equivalent
natural
norm.
This
is
what
Mayr
called
the
from
a
fixed
tance
of
the
insights onimpact
which Darwin
based
way of understandingGenetic
for
thekey
revolutionary
of Mendelian
At
the
same
time,
the
breeders
attitude
mutations seemed to be essentially pluexactand
role
played by
Dar- justtransition
to populaof natural
selection.
process operated. Theralistic
typological
genetics.
The notion
of hard heredity was
toward
variationthinking
pushed Darwin
toward his
the theory
undirected,
providing
the sourcefrom
of random
variation that
Darwins mecha- view that the species is just a population of introduced in opposition to the soft form of
of his
wins study of breeding
in the formulation
nism by
required
as its raw
material.
theory is much debated
historians
(1617),
This later development highdoubt of how important
but there can be little
lights the importance of another
artificial
andby
natural
the analogy between insight
gained
Darwinselecin the
In thistocase,
tion became in his later
thinking.
late 1830s,
his decision
investigate because
the workeven
of the
animal
Darwin was truly unique,
Wallace
breeders
(Fig. 3) and his
recogdid not take this step
and dissociated
himself
nition that their method of artifiselection
expressed
from the link with artificial
cial selection offered a useful way
in Darwins later writings.
of understanding how the equivDarwin turned to alent
the breeders
in search
of a
natural process
operated.
The exactcould
role played
by Darwins
be changed
clue as to how a population
study ofwhere
breeding
in the formulamodifications
here at least was a situation
tion of his theory is much debated
were actually being produced
a human
by historianson(1617),
buttime
there
scale and that couldcanbebe investigated
directly.
little doubt of how
impornetwork
of breedThere was a well-developed
tant the analogy
between
artificial
natural selection
became
in his
their ideas
about
ers by this time, andand
although
thinking.
In this pregeneticase, Darwin
heredity and variationlater
were
distinctly
was truly unique, because even
they
a very
clear
cal (like Darwins own),
Wallace
did had
not take
this step
and
they produced
in
appreciation of how dissociated
himself changes
from the link
The expressed
insight
their artificially small
populations.
with
artificial selection
Darwins later
writings.
that they worked byinselection
may
have been
Darwin
turned to theamong
breeders
of contention
important (this is the point
in search of a clue as to how a
notebooks),
but
the
experts studying Darwins
population could be changed
He
realbreeders certainly taught
him
one
thing.
here at least was a situation where
ized that in a domesticated
population
there beis
modifications
were actually
ing produced
on a human
time Fig. 3. Pigeons (23).
purposeless
and unalways a fund of apparently

20

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VOL 323

9 JANUARY 2009

225

Traditionally,
species
scale and that for
could
investigated
directly.
descent (15). The
neo-Lamarckians
TheAmerican
Struggle for
Existence
thatbetransition
in the
late 19thinterbreeding
century. It individuals.
the Men
Who Discovered
It (Doubleday, New
were
treated
as
idealized
types
with
a
fixed
esThere
was
a
well-developed
network
of
breeders
Edward DrinkerOne
Cope
and
Alpheus
Hyatt
proYork,
1958).
of the most disturbing aspects of Darwins did, however, highlight the harsher aspects of
2. P.
Corsi,
Agebeing
of Lamarck:
sence,
any variation
from
theThe
norm
trivial Evolutionary
by for
this existime, and
their of
ideas
about The
posed that the evolution
of each
group should
to the be
struggle
struggle.
potential
theory was
its appeal
the although
consequences
Theories
in France,
17901830
and impermanent.
The
breeders
knew that
they (Univ. of
heredity
were distinctly
pregenetseen as a series tence
of parallel
moved
through
that equates
with and
the variation
clearly
as thelines
natural
process
implications
were drawn
out even more
California
Press,
Berkeley,
1988).
could
produce
huge
changes
in
structure
by
ical
(like
Darwins
own),
they
had
a
very
clear
the same hierarchy
of
developmental
stages,
an
upbreeders activity as a selecting agent. This very when Galton argued that it would be necessary 3. A. Desmond, The Politics acof Evolution: Morcumulating
normal
variations
over
a
number
of
appreciation
of
how
they
produced
changes
in
dated version of harsh
the idea
suggested
in
Chamberss
vision of nature certainly threatened the to apply artificial selection to the human race
phology, Medicine and Reform in Radical
generations.
When
Darwin
linked
this
informatheir
artificially
small
populations.
The
insight
Vestiges. The similarities
linking
the
species
in
a
London (Univ. of Chicago Press, Chicago,
traditional belief in a benevolent Creator. The in order to prevent unfit individuals from
that species could change
genus were due not
to a recent common ancestry, that they worked by selection may have been tion with his conviction
1989).
term struggle for existence occurs in Thomas reproducing and undermining the biological
P. J.heBowler,
Evolution:
The aHistory of an
was driven
toward
but to parallel trends independently reaching the important (this is the point of contention among indefinitely over4.time,
Robert Malthuss An Essay on the Principle health of the population. This was the eugenics
(Univ.inofwhich
California
Press, Berkeley, ed.
concept
the popsame stage of development. Like Chambers, they experts studying Darwins notebooks), but the new form of speciesIdea
of Population, although used in the context of program, and in its most extreme manifestation
3, 2003).The natural range of
endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing. He ulation becomes paramount.
tribal groups competing for limited resources. at the hands of the Nazis, it led not just to the 5. J. A. Secord, Victorian Sensation: The Exof the species character,
recapitulates phylogeny, in the terminology intro- realized that in a domesticated population there variability becomes part
traordinary Publication, Reception, and Secret
Darwin saw that population pressure would lead sterilization but also to the actual elimination of
deviations
duced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental
Authorship
of Vestigesfrom
of theaNatural History
to competition between individuals and was per- those unfortunates deemed unfit by the state. Did
Mayr called
theChicago
transi- Press, Chicago,
the addition of preordained stages to ontogeny. undirected variation among individual organisms. fixed norm. This is what
of Creation
(Univ. of
the first
to realize
that
it might
represent
Darwins
emphasis
the natural tion
elimination
from typological 2000).
thinking to population thinkAlthough
convinced
that the
degree on
of variabilAdaptation was haps
not crucial
once
the basic
charby
which
the
population
could
change
variants
help
to
create
a 6. heD.may
a
means
of
maladaptive
Kohn,
Ed.,exaggerated
The Darwinian
ing,
and although
have
the Heritage: A
acter of the group was established, and the linear, ity was artificially enhanced under domestication,
TheevenprocessDarwin,
workednevertheless,
by climate
throughoftime
(19, 20).
of opinion
in must
which
atrocities
Centennial
extent
to which Darwin
himselfRetrospect
made the(Princeton
con- Univ. Press,
accepted
that there
be such
orthogenetic evolution
the group
might
NJ, 1985).
theequivalent
popu- became
possible?
the least fitcharacters
variants within
subsequent
development of
some
variability
in every wild popu- ceptual transition, thePrinceton,
tually generate eliminating
bizarre nonadaptive
7. J. Browne, Charles Darwin: Voyaging (Jonahas to
be admitted
that,then
by making
death it- theory
lation and allowing
theof
better
adapted
to survive
the selection
brought
this
implication
lation.
The analogyItwith
artificial
selection
as a prelude to extinctionthe
theory
racial
than Cape, London,
1985).out
breed.make
Thisno
wassense
whatofthethe
philosopher
in nature,
Darwinmore
introduced
self a creative
andcould
clearly. 8. J. Browne, Charles Darwin: The Power of
allowedHerhim to depict
natural force
selection
as a parsenility. Darwin
refer he
to as the
Spencer
a new and
profoundly
disturbing insightIninto
thethe
debates that
followed
the Cape,
publication
allelsurvival
process in which
a few
variant individuals,
theory proposedbert
by Cope
andwould
Hyatt,later
because
Place
(Jonathan
London, 2002).
selection
of an
theevolutionary
fittest. Strictly
speaking,
an insight
seems
to have
9. ofM.
J. S. Hodge,
G. Radick,
Eds., The Camof resonated
On the Origin
Species,
the analogy
with
in this
case withworld,
characters
useful that
to the
species
could not imagine
process
drivennatural
bridge Companion
Darwin
with thebreeder,
thinkingsurvive
of many
not underrequires
differential
selection continued
to play atokey
role (Cambridge
than the human
andwho
re- didartificial
by predetermined
trends.only
But the
fact that reproduction
such ratheramong
Univ. Press, Cambridge, 2003).
variants,
thought
that theproduce.
pressureThose
of with
his theory.
Darwin-even Darwins
standharmful
or accept
the details
by forcing
critics to think about
characters
areofelimtheories flourished
in the but
lateDarwin
19th century
dem10. M. J. S. Hodge, Stud. Hist. Biol. 6, 1 (1982).
wastheory
necessary
to makeinated
it effective.
Darwinism
competition
ism wasfornotexistence,
responsible
socialthe
problems of 11.
heredity
and
variation
in a new Naturalists:
by the struggle
just asforthe
onstrates just how
radical the
of open P. F. Rehbock,
The Philosophical
input frombreeder
Malthus,
henot permit
seems that
without
or eugenics
in anytosimple
way.
some
wayall,(18).
OpponentsThemes
such as
Fleeming
Jenkin,
will
any animal
reproduce
if After
ended, divergentItevolution
was
to thethe
naturalists
in Early
Nineteenth-Century
British
geneticists
endorsed
eugenics
by analogy
would not have come up with the theory.
early
saw selection working
on large
variationsPress, Madison,
it does not have the
character
he wants.
It was
the who
of the time.
Biology (Univ.
of Wisconsin
1983).
The idea of struggle was pervasive
in thewho
lit- taught
even
whileordismissing
with Darwin
animal that
breeding
sports of nature,
were, nevertheless, still
breeders
variation
is not
J. Richards,
The Meaning
Artificial Selection
exploitedtoward
in some
evolution.
erature of the period, but could be directed
naturalpreordained
selection asgoal,
the mechanism
working
within 12.
the R.
framework
defined
by thisof Evolution: The
allowing of
Morphological
Construction
For supporters
such as Francis
Galton,and Ideological
to build
conviction
thattoadaptSpencer
had on his
many different
In the 1850s, him
Andexisting
the Nazis
wanted
purify a analogy.
fixed racial
These non-Darwinian
models ways.
were ultimately
Reconstruction of Darwins Theory (Univ. of
artificial
selection helped
clarify
the nature
ivebe
evolution
bewhich
an open-ended,
branching
marginalized byalready
the synthesis
of competition
the selectioncould
they certainly
did not want
to admit
seen how
turned must
type,
ChicagotoPress,
Chicago,
1992).
of both heredity
and
the way
process. less had evolved gradually from an ape ancestry.
theory and genetics
the different,
early 20thand
century.
into ainvery
in some respects
But 13.
A.selection,
Desmond,paving
J. R. Moore,
Darwins Sacred
for primarily
the revolutionary
impact
Mendelian
At the
the breeders
attitude
Genetic mutations
seemed to
be essentially
Cause:
Race, of
Slavery
and the Quest for Humechanism
of pluprogress (21).
Forsamebytime,
disturbing,
proposing
that evolution
worked
man
Lane,was
London, 2009).
genetics.DarThe notion
ofOrigins
hard(Allen
heredity
variation
pushed
toward
the variants,
ralistic and undirected,
providing
just the source
individuals
Spencer,
the interaction
betweentoward
through
the Darwin
elimination
of useless
14.

E.
Mayr,
One
Long
Argument:
introduced
in
opposition
to
the
soft
form
of Charles Darview
that
the
species
is
just
a
population
of
of random variation
that
Darwins
mechastimulated their efforts to adapt to the chang- win created an image that could all too easily be
win and the Genesis of Evolutionary Thought
nism required asing
its raw
material.
social
and physical environment. He then exploited by those who wanted the human race
(Harvard Univ. Press, Cambridge, MA, 1991).
This later development
high- concept of the inheritance to conform to their own pre-existing ideals. In 15. P. J. Bowler, The Eclipse of Darwinism: Antiinvoked Lamarcks
lights the importance
of another
of acquired
characteristics to explain how these the same way, his popularization of the struggle
Darwinian Evolution Theories in the Decades
insight gained by
Darwin in the accumulated over many gen- metaphor focused attention onto the individualAround 1900 (Johns Hopkins Univ. Press,
self-improvements
Baltimore, MD, 1983).
late 1830s, his decision
inves- to biological evolution and so- istic aspects of Spencers philosophy.
erations,toleading
16. R. J. Richards, Stud. Hist. Philos. Sci. 28, 75
tigate the workcial
ofprogress.
the animal
Modern science recognizes the importance
Spencers self-improvement mod(1997).
breeders (Fig. 3)el and
his recogof progress
became immensely popular in the of Darwins key insights when used as a way 17. M. Ruse, J. Hist. Ideas 36, 339 (1975).
nition that their later
method
of
artifi19th century, and because it too seemed to of explaining countless otherwise mysterious 18. J. Gayon, Darwinisms Struggle for Survival:
cial selection offered
a useful
wayas the motor of change, it was aspects of the natural world. But some of those
Heredity and the Hypothesis of Natural Sestruggle
rely on
of understandingoften
howconfused
the equiv-with the Darwinian mechanism. insights came from sources with profoundly dislection (Cambridge Univ. Press, New York,
1998).
alent natural process operated.
In fact, Spencer thought that all humans will turbing implications, and many historians now 19. P. J. Bowler, J. Hist. Ideas 37, 631 (1976).
The exact role played by Darwins
eventually acquire the faculties needed to inter- recognize that the theory, in turn, played into 20. A. Desmond, J. R. Moore, Darwin (Michael
study of breeding in the formulaact harmoniously with one another. But his occa- the way those implications were developed by
Joseph, London, 1991).
tion of his theory is much debated
sional use of highly individualistic language al- later generations. This is not a simple matter of 21. M. Francis, Herbert Spencer and the Invention
by historians (1617), but there
of Modern Life (Acumen, Stocksfield, UK,
lowed him to be perceived as the apostle of free science being misused by social commentacan be little doubt of how impor2007).
Much of what later became known tors, because Darwins theorizing would almost 22. C. Darwin, Transmutation Notebook B, from
tant the analogy enterprise.
between artificial
was, in fact, Spencerian certainly have been different had he not drawn
as social
Natural Selection portfolio p. 36 (Cambridge
and natural selection
becameDarwinism
in his
social
Lamarckism
expressed
in the terminology inspiration from social, as well as scientific, inUniv. Library, Cambridge, 1838); P. H. Barlater thinking. In this case, Darwin
rett, P. J. Gautrey, S. Herbert, D. Kohn, S.
with
of
struggle
popularized
by
Darwin.
fluences.
We
may
well
feel
uncomfortable
was truly unique, because even
Smith, transcribers and Eds., Charles DarThis
point
is
important
in
the
context
of
those
aspects
of
his
theory
today,
especially
in
Wallace did not take this step and
wins Notebooks p. 180 (British Museum of
by
modern
opponents
of
of
their
subsequent
applications
to
human
the
charge
raised
light
dissociated himself from the link
Natural History, Cornell Univ. Press, Ithaca,
Darwinism
that the theory is responsible for the affairs. But if we accept sciences power to upwith artificial selection
expressed
NY, 1987); available at the Darwin Digital
Library, http://darwinlibrary.amnh.org/.
in Darwins laterappearance
writings. of a whole range of unpleasant social set the traditional foundations of how we think
on struggle. Darwin exploited the about the world, we should also accept its po- 23. G. Neumeister, Das Ganze der Taubenzucht
policies
Darwin turned
to the based
breeders
(B. F. Voigt, Weimar, 1876).
idea as
of to
thehow
struggle
in search of a clue
a for existence in a way that tential to interact with moral values.
nearly
was
unique
until
paralleled
by
Wallace
population could be changed
years later.
here at least was 20
a situation
whereTheir theory certainly fed into
the movements
modifications were
actually be-that led toward various kinds of References and Notes
1. L. Eiseley, Darwins Century: Evolution and
not the only
Darwinism,
it was
Fig.
3. Pigeons
(23).vehicle
ing produced onsocial
a human
time but
www.sciencemag.org

SCIENCE

VOL 323

9 JANUARY 2009

225

21

Speciation

disentangle key aspects of clade histories. Clades

are monophyletic, including all descendants of an
ancestor, whereas taxa may be monophyletic or
vestigations,
provide an
outline
of how of
these
paraphyletic, excluding
some
descendants
the
and
other Comparative
studies correspond
to the predictions
ancestor.
macroecological
studies
disentangle
key
aspects
of
clade
histories.
Clades
of
the
RedtoQueen,
Court
Jester,that
andsister
multilevel
add
rigor
analyses
showing
clades
REVIEW
are monophyletic,
including
all descendants
of an
(Table
1),
and
outline
some
phymixed
models
may
vary whereas
in rate of taxa
evolution,
timing
of increases
ancestor,
may be
monophyletic
or
of spelogenetic
studies
ofand
themorphospace
macroevolution
in
species
richness
occupation,
paraphyletic, excluding some descendants of the
cies
diversity. of evolutionary novelties across
and
distributions
ancestor.
Comparative macroecological studies
lineages
Here, I that
will sister
explore
the
add rigorand
to subclades.
analyses showing
clades
The
Global global,
Patterntaxic
of Diversification
largest-scale
investigations,
provide
may vary in rate of evolution, timing of increases
Michael J. Benton
Through
an
outline Time
of
how these
and other studies
correin species
richness
and morphospace
occupation,
A
key
thetheorigin
of modern
spond
toquestion
the predictions
of
Red
Queen,
Court
and distributions
ofabout
evolutionary
novelties
across
Evolution may be dominated by biotic factors, as in the Red Queen model, or abiotic factors,
todays
10
million
species
biodiversity
is
how
Jester,
and
multilevel
mixed
models
(Table
1),
lineages and subclades. Here, I will exploreand
the
as in the Court Jester model, or a mixture of both. The two models appear to operate
microbial
arose
from
a single
ultimate
speciesofofthe
outline
some
phylogenetic
studies
macrolargest-scale
global,
taxic investigations,
provide
predominantly
over different geographic and temporal scales: Competition, predation, and other
Michael J. Benton
life
3500 of
million
ago
1).correTwo
evolution
diversity.
an outline
ofspecies
howyears
these
and (Ma)
other (Fig.
studies
biotic factors shape ecosystems locally and over short time spans, but extrinsic factors such as
models
for
global
diversification
are
termed
the
spond to the predictions of the Red Queen, Court
disentangle
key aspects
of clade histories.
Clades The
climate
and
oceanographic
events as
shape
larger-scale
patterns
regionally
and
Global Pattern ofmodel
Diversification
(57)(Table
and the
exEvolution
may
be dominatedand
by tectonic
biotic factors,
in the
RedareQueen
model,including
or abiotic
factors, of an saturation/equilibrium
monophyletic,
all descendants
Jester, and multilevel mixed
models
1), and
globally,
through
millions
years.
studies
that speciesor pansion
Through model
Time (811). The equilibrium model
as in the and
Court
Jester thousands
model, or and
a mixture
of of
both.
ThePaleobiological
two ancestor,
models whereas
appear
tosuggest
operate
taxa
may
be monophyletic
outline some phylogenetic
studies of the macrodiversity
is
driven
largely
by
abiotic
factors
such
as
climate,
landscape,
or
food
supply,
and
paraphyletic,
excluding
some
descendants
of
the
A
key
question
about
the
origin
of modern biopredominantly over different geographic and temporal scales: Competition, predation, and other
at
has
prevailed,
among
marine
paleobiologists
evolution
of species
diversity.
ancestor.
Comparative
macroecological
studies
comparative
approaches
intospans,
clade but
dynamics.
diversity
isa how
todays
10 million
species
arose
biotic factorsphylogenetic
shape ecosystems
locallyoffer
and new
over insights
short time
extrinsic factors such as
least,
for
long
time,
and
represents
a
classic
add rigor to analyses showing that sister clades
from
a singlePattern
ultimate
ofitmicrobial
life
climate and oceanographic and tectonic events shape larger-scale
regionally
andof increases Red
The Global
of species
Diversification
viewpoint
because
implies priQueen
may varypatterns
in rate of evolution,
timing
3500
million
years
ago (density
(Ma) (Fig.
1). Two modportant
not
export
organism-level
processes
to marily
here
are
two
ways
of
viewing
evolution,
globally,
andare
through
thousands
and millions
Paleobiological
studies
suggest
that
species
Through
Time
richness
morphospace
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here
two ways
of viewing
evolu-of years.
scales,
andinto
itspecies
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likely
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evolution
operates
in
dependence)
on
biotic
controls
distributions
evolutionary
els
fordiversity.
global diversification
termed biothe
global
andsupply,
it isnovelties
likely
that global
through
the largely
spectacles
of either
Red
diversity
is driven
abiotic
factors
such asregional
climate,orand
landscape,
oroffood
and across
oftheeither
way
(3).scales,
tion,
through
the by
spectacles
a pluralistic
A key
question
about the originare
of modern
lineages
and
Here,way
I will(3).
explore the saturation/equilibrium model (57) and the exevolution
operates
insubclades.
a pluralistic
Queen
or Queen
the Court
The Red
Queen
comparative
phylogenetic
approaches
offer
new insights
intoare
clade
dynamics.
There
two broad
methodologies
for provide
stud- diversity
There isare
two
versions
of the species
equilibrium
the Red
or Jester.
the
Court
Jester.
The
how
todays
10 million
arose
largest-scale
global,
taxic investigations,
pansion
(811).
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equilibrium
model
has
There
are
two
broad
methodologies
for
studies
model
(1)
stems
from
Darwin,
who
viewed
evoenton
taxic
and model,
time
when
the
global
diversity
differing
in the
Red Queen model (1) stems from Darwin, who ies of species
from a model
single
ultimate
species
of microbial
life
an outline
of howthrough
these and time,
other studies
correprevailed,
among
marine
paleobiologists
at
least,
of
species
diversity
through
time,
taxic
and
phylution
as
primarily
a
balance
of
biotic
pressures,
spond
to
the
predictions
of
the
Red
Queen,
Court
of bi- phylogenetic
involves
viewedhere
evolution
primarily
a balance
The
taxic approach
ecosystem
saturated.
3500 million
yearsbecame
ago (Ma)
(Fig. 1).Sepkoskis
Two modportant not to (4).
export
organism-level
processes
to marine
are twoasways
of viewing
evolution,
y be dominated
by biotic
factors,
as in the Red
Queen
model,
or abiotic factors,
Jester,The
and multilevel
mixed models
1), and for a long time, and represents a classic Red Queen
logenetic
(4).
taxic
approach
treatmost
notably
competition,
and
characterels for global
are termedthree
the
regional species,
or
global
scales,
itinvolves
is (Table
likely
that coupled
the
ofit was
either
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oticorpressures,
notably
competition,
it treating
genera,
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model (5) identified
urt Jester model,
a through
mixture ofmost
both.spectacles
The two models
appear the
toand
operate
outline
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phylogenetic
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of the macro- viewpoint because it implies primarily biotic coning
species,
genera,
families
as
independent
ized
by
the
Red
Queens
statement
to
Alice
in
saturation/equilibrium
model
(57)
and
the
exevolution
operates
in
a
pluralistic
way
(3).
Queenand
or temporal
the
Jester.
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Queen and
byCourt
thescales:
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Queens
statement
and
counting
their
occurrences
in
the
Cambrian,
most
of
the
wasgeographic
characterized
pendent
equilibria,
y over different
Competition,
predation,
other entities
evolution of species diversity.
trols
(density
dependence)
global
diversity.
entities
and
counting
their
occurrences
Through
the
Looking-Glass
thatwho
it
allevothe
shape ecosystems
locally
and
overfrom
short
time
spans,
buttakes
extrinsic
factors
asThere
pansion
model
(811).
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equilibrium
model has
areand
twoother
broadfactors.
methodologies
foragainst
studies Paleozoic,
model
(1)in
stems
Darwin,
viewed
that
it such
The phylogenetic
beginning
in
to
Alice
Through
the
Looking-Glass
against
time
and
perhaps
third,
oceanographicrunning
and
tectonic
events
shape
larger-scale
patterns
regionally
and
There
are
twocontinuing
versions
of
the present
equilibrium
time
and
other
factors.
The
phylogenetic
apyou
can
do,
to
keep
in
the
same
place.
The
Global
Pattern
oftime,
Diversification
prevailed,
among
marine
paleobiologists
at (Fig.
least,
of speciesuses
diversity
through
taxic and
phylution all
as primarily
a balance
of biotic
pressures,
trees
to
takes
the
running
you
can
do,
to
keep
in
approach
cladograms
or
molecular
the
Pliocene
and
to
the
through thousands
and
millions
of
years.
Paleobiological
studies
suggest
that
species
Through
Time
differing
the timea classic
when the
uses
cladograms
or molecular
trees
to model,
The
Court
Jester
model (2)
isit that
evolution, proach
for a long
time, andinrepresents
Red global
Queen
logenetic
(4).
The
taxicofapproach
involves
treatmost
notably
competition,
was
place.
Courtand
Jester
model
(2)supply,
is and
disentangle
aspects
clade
histories.
Clades
same
riven largely the
by
abiotic
factors
suchThe
as climate,
landscape,
orcharacterfood
A key
key question
about
the origin
of modern
bio- 2A). These three equilibrium levels correspond
speciation,
and
extinction
rarely
happen
except
in
viewpoint
because
it
implies
primarily
biotic coning
species,
genera,
or
families
as
independent
ized
by
the
Red
Queens
statement
to
Alice
in
phylogenetic that
approaches
offer new
insights into
dynamics.rarely
andclade
extinction
are monophyletic,
allmillion
descendants
of to three sets of phyla, the Cambrian, Paleozoic,
evolution,
speciation,
diversity is including
how todays 10
species arose
response
to
changesit
in the
physical
trols Modern,
(density dependence)
on global
diversity.
entities
counting
their
occurrences
against
Throughexcept
theunpredictable
Looking-Glass
takes
all the an
from
a singleof
ultimate
species
of microbial
life and
whereas
taxa
may
be monophyletic
happen
in responsethat
to unpredictable
ancestor,
that interacted
and successively
Fig.
1. and
Operation
Red
Queen
environment,
recalling
the
capricious
behavior
3500
million
years ago
(Fig.
1).A
Two modre two ways of
viewing
evolution,
portant
not
to
export
organism-level
to
There each
are two
versions
of the
timeparaphyletic,
and
other
factors.
The(Ma)
phylogenetic
ap- replaced
running you
canphysical
do, to keep
in the same
place. processes
changes
in the
environment,
recalling
some
descendants
other
through
the equilibrium
Cambrianor
excluding
(biotic
causation)
and
Court
Jester
els for
global diversification
are termed
the
h the spectacles
of Court
either
theJester
Red
regional
or global
scales,
and it is likely
that uses
of
licensed
foolmodel
of Medieval
times.
Neither
model, differing
in the
time when the
global
proach
cladograms
or
molecular
trees Genus
to Ordovician
Thethe
(2)
islicensed
that
evolution,
(abiotic
causation)
models
at
differbehavior
of
the
fool
of
intervals,
the
capricious
of
the
ancestor.
Comparative
macroecological
and
Permo-Triassic
saturation/equilibrium model (57) and the life
ex-span
or the Court Jester.
Thewas
Red Queen
evolution
operates in a and
pluralistic
way (3).
model
proposed
asrarely
exclusive,
both
speciation,
and
extinction
happen
except
in
ent
geographic
and
temporal
scales
(3-6
My)
was
proposed
as for
studies
rigormodel
to analyses
showing
that
sister
Medieval
times.
model
pansion
(811). The
equilibrium
model
has reaching higher equilibrium levels after each
ms from Darwin,
who viewed
evo-Neither
There
are two
broad
methodologies
studies add
Darwin
and
Van
Valenspecies
(1)
allowed
extrinsic
Court
response
unpredictable
changes
infor
theValen
physical
prevailed,
paleobiologists
at least,
marily a balance
of biotic to
pressures,
diversity
through
time,
and phy(A).
Themay
Red
Queen
maymarine
at timing
vary
inamong
rate
ofprevail
evolution,
of long-term replacementJester
event. The second model
exclusive,
and
both ofDarwin
andprimarily
Van
(1)taxic clades
Fig.
1.
Operation
of
Red
Queen
influences
on
evolution
in
their
biotic,
a long
time, and
represents
a classic Red
Queen
competition, environment,
and it was characterlogenetic
(4).
The taxic approach
involves
treat- for
recalling
the
capricious
behavior
organismic
and
species
level
on
short
Species
A
allowed
for
extrinsic
influences
on
evolution
in
and
morphospace
equilibrium level from
increases
in
species
richness
(6,
7)
identifies
a
single
(biotic causation)
and Court
Jester
Queen
views.
because
it implies
primarily biotic conRed Queens Red
statement
to Alice
in
species,
genera,
or families
as independent
life
span
of the
licensed
fooling
ofRed
Medieval
times.
Neither
time
scales,viewpoint
whereas
the Court
Jester
Genus
biotic,
Queen
views.
primarily
occupation,
and
distributions
of
evolutionary
the
early
Paleozoic,
perhaps
400 Ma, to the
trols
(density
dependence)
on
global
diversity.
Looking-Glasstheir
that
it
takes
all
the
entities
and
counting
their
occurrences
against
(abiotic
causation)
models
at
differ(1-2
My)
Species
in as
a Red
Queen world
de- holds his own on larger scales. The
life span
model
wasdiversity
proposed
and
both
There
aretemporal
two versions
of the equilibrium
can do, to keep
inSpecies
the same
place.
time
other factors.
The
phylogenetic
ap- across
diversity
in and
a exclusive,
Red
Queen
world
novelties
lineages
andscales
subclades.
Here,
present (Fig. 2B). In both models, the equilibria
ent geographic
and
(3-6 My)
pends
primarily
on
intrinsic
factors,
such
as
body
Red
stippled
green
shape shows
an time
areawhen the global
Darwin
Van Valen
(1)uses
allowed
for extrinsic
model,
the
ester model (2)
is that and
evolution,
proach
cladograms
or molecular
trees
toexplore
Court
Apparent
Milankovitch
intrinsic
factors,
as I(A).
thediffering
largest-scale
global,
to biodiversity
saturation in which
depends
primarily
on
willThe
correspondQueen?
Red
Queen
mayinprevail
at taxic insize,
breadth
physiological
tolerance,
orsuch
adaptRed Queen effects might be
d extinction rarely
happen
except
in
Jester
Red Queen
influences
onofevolution
in their
primarily
biotic, where
Scale
(100
ky)
organismic and species level on short
Species
tolerance,
body in
size,
breadth
of aphysiological
from
scale effect
ability
to
hard
times.
In
Court
Jester
world,
spenpredictable changes
the
physical
erroneously, but these are
Red Queen views. Fig. 1. Operation of Red Queen identified
life span
time
whereas the Court Jester
Fig. 1. Operation of Red Queen (biotic causation)
orcapricious
adaptability
to hardontimes.
In a Court
Jester likely
recalling thecies
behavior
A scales,
diversity
depends
fluctuations
in
climate,
the
result
of
spatial
averaging
of
Locality Average Biotic
Entire
(1-2 My)
and world
Court Jester
Species Neither
diversity(biotic
in a causation)
Red Queen
de- holds his own on larger scales. The
ed fool of Medieval
and Court Jester (abiotic
causation)
at difGenus
world,times.
species
depends
onmodels
fluctuations
species
region/ models
continent
landscape,
and diversity
food
supply.
In reality,
of as
course,
responses to climate change
(abiotic
causation)
at body
differ- regional
primarily
on intrinsic
factors,
such
life span
proposed as pends
exclusive,
and both
Red and
stippled
green
shape
shows
an
area
range
climate
ferent
geographic
temporal
scales
(A).
The Red
landscape,
food
supply.
Inand
realin climate,
entand
geographic
and temporal
scales
Apparent
(3-6 My)complex physical perturMilankovitch
both
aspects
might
prevail
in
different
ways
at
and
other
zoneand species level
Van Valen (1) size,
allowed
for extrinsic
Queen?
breadth
of physiological
tolerance,
orprevail
adapt-at where Red Queen effects might
Court be
Queen
Red Queen
(A). The Red
Queen
Scale (100
ky) may prevail at organismic
might
prevail
in difity,
course,
both
that may be in opposite
whataspects
could
perhaps
bemay
called
the bations
Jesterdievolution in different
theirof
primarily
biotic,
fromthe
scale
effect
ability
totimes,
hard
times.
In
a Court
organismic
andJester
speciesworld,
level onspeshort
Specieserroneously, but these are
on short time scales,
whereas
Court
Jester holds
identified
Geographical
scale
iews.
could
ferent ways
and at
different
times, the
what
and so cancel each other,
life span
multilevel
mixed
model.
Traditionally,
biologists
time
scales,
whereas
Court
Jester rections,
cies
diversity
depends
on
fluctuations
in
climate,
his
own
on
larger
scales.
The
stippled
green
shape
likely (1-2
theMy)
result of spatial averaging of
Locality Average Biotic
Entire
iversity in a Red
Queen
world
deholds
his own
onmixed
larger
scales.
The suggesting no controlling effect of the
perhaps
be called
multilevel
model.
have
tended
to think
in
a Red
Queen,
Darwinian,
species
region/
continent
shows
an
area
where
Red
Queen
effects
might
be
foodthe
supply.
In
reality,
of
course,
regional
responses
to
climate
change
ly on intrinsiclandscape,
factors, such and
as body
Red
stippled
green
shape
shows
aninarea
environment
on evolution.
range
climate
Apparent B
biologists
have
tended
to think
in
Traditionally,
Milankovitch
intrinsic,
biotic
factors
way,
and
geologists
a physical
identified erroneously,
but these
are likely the reof physiological
tolerance,
or adaptboth
aspects
might
prevail
in different
ways
and
at
and other
complexQueen?
physical perturwhere Red
Queen effects
might
be Physical-environmental
Red Queen
zone
Scale (100 ky)
disruptions
facadifferent
Red
Queen,
Darwinian,
intrinsic,
Court
Jester,
extrinsic,
physical
factors
way.
from scale
d times. In a Court
Jester
world,
speerroneously,
but
these
are
bations that may be in opposite
di- effect
times,
whatidentified
could
perhaps
bebiotic
called
the
Genus sult of spatial averaging of regional responses to
elicit biotic responses
along the
Geographical
depends on fluctuations
inand
climate,
likely theinresult
of spatial
averaging
of may
tors
way,
geologists
a
Court
Jester,
exclimate change and
other complexscale
physical perturlife span
Much
of
the
divergence
between
the
Red
Locality
Average
Biotic
Entire
rections,
and
so
cancel
each
other,
multilevel
mixed
model.
Traditionally,
biologists
species and
region/ continent(3-6 My)
red
line
separating
Red
Queen
d food supply.Queen
In
reality,
of
course,
regional
responses
to
climate
change
bations
that
may
be
in opposite directions, and so
and
Court
Jester
world
views
may
depend suggesting no controlling effect
physical
factors
way.
trinsic,
range ofclimate
the
have
tended
to
think
in
a
Red
Queen,
Darwinian,
might prevail in different ways and at and other complex physical pertur- Court Jester outcomes (B). The usage
zone
cancel each other, suggesting
Court no controlling effect
scale
(2)
(Fig.
1):
Biotic
interactions
Much
of the
divergence
between
the drive
Red
physical environment on evolution.
bations
thatand
may
be in opposite
s, what couldon
perhaps
be biotic
called
the
intrinsic,
factors
way,
geologists
in dia here
Speciesof the physical environment
is
the
microevolutionary
Red
Queen,
Geographical
scale B
Jester on evolution. Physicalmuch
of
the
local-scale
success
or
failure
of
inrections,
and
so
cancel
each
other,
Physical-environmental
disruptions
world
views
may
Queen
and
Court
Jester
xed model. Traditionally,
biologists
Court Jester, extrinsic, physical factors way.
life
span
opposed to the macroevolutionary
Genus
environmental disruptions may elicit biotic resuggesting
no
controlling
effect
of the as
o think in a Red
Queen,on
Darwinian,
dividuals,
populations,
and1):
species
(Red
Queen),
may elicit biotic responses along the
(1-2
My)
depend
scale
(2)
(Fig.
Biotic
interactions
life span
Much
of
the
divergence
between
Red Red
Queen
that
posits
constant
exphysical environment
onthe
evolution.
sponses along the red line separating Red Queen
ic factors way,
and
geologists
in
a
B line separating Red Queen and
(3-6 My)
red
but
perhaps
these
processes
areviews
overwhelmed
by
drive
much
of Jester
the
local-scale
success
or tinction
Queen
and
Court
world
may
depend
Physical-environmental
disruptions
risk, a view that has been largely
and Court Jester
extrinsic, physical
factors
way.
Red outcomes (B). The usage here is
Genus
Milankovitch
Court
Jester
outcomes
(B).
The
usage
substantial
tectonic
and
climatic
processes
atdrive
time
maypopulations,
elicit biotic
responses
along
the rejected
and species
failure
of (2)
individuals,
Court
on between
scale
(Fig.
1):
Biotic
interactions
life span
the divergence
the
Red
(31). Illustration based on (2).
the ky)
microevolutionary
Red Queen, as opposed to
Queen
Scale
(100
5
redperhaps
line
separating
Redprocesses
and
Species
here is(3-6
theMy)
microevolutionary Red Queen,
scales
above
10 but
years
(Court
Jester).
ItQueen
isofimJester
ourt Jester world
viewsof
may
(Red
Queen),
these
much
thedepend
local-scale
success
or
failure
inthe
macroevolutionary
Red Queen that posits conCourt
Jester
outcomes
(B).
The
usage
life
span
as
opposed
to
the
macroevolutionary
Court
(Fig. 1): Biotic
interactions
drive by substantial tectonic and
are
overwhelmed
stant extinction
risk, a view that has More
been largely
Less
dividuals,
populations,
and species (Red Queen),
Species
(1-2 My)
Jester
local-scale success or failure of in- here is the microevolutionary Red Queen,
Red Queen
5
life span that posits constant exDepartment
of these
Earth Sciences,
University
of
Bristol,
Bristol
as
opposed
to
the
macroevolutionary
rejected
(31).
Illustration
based
on
(2).
at
time
scales
above
10
climatic
processes
but
perhaps
processes
are
overwhelmed
by
pulations, and species (Red Queen),
Environmental scale
(1-2risk,
My) a view that has been largely
tinction
Red Queen that posits constant exBS8
1RJ,
UK. tectonic
E-mail:
mike.benton@bristol.ac.uk
Red
Milankovitch
not to export
(Court
Jester).
It isclimatic
important
substantial
processes
at time rejected (31). Illustration based on (2).
hese processesyears
are overwhelmed
by and
tinction risk, a view that has been largely
Queen
Scale
(100
ky)
Red
5
Milankovitch
ctonic and climatic
processes
organism-level
to regional
scales
aboveat time
10processes
years
(Court
Jester).or
It global
isonimrejected
(31).
Illustration
based
(2).
Queen
Scale (100 ky)
5

SPECIALSECTION

REVIEW

Red Queen and the Court Jester:

ies Diversity and the Role of Biotic
Abiotic Factors Through Time

Temporal scale

Temporal scale
Temporal scale

Temporal scale

Temporal scale
Temporal scale

T
T
T

10 years (Court Jester). It is im-

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Department
of Earth
Earth Sciences, University
of Bristol,
Bristol Sciences, University of Bristol,
BS8 1RJ, UK. E-mail: mike.benton@bristol.ac.uk
mail: mike.benton@bristol.ac.uk

22

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VOL 323

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Number of genera
(corrected; blue)

400
200
0

200

Number of genera
400
(corrected;600
blue)

600

3000
2000
1000

Number
genera
2000 of 3000
(empirical; red)

1000

tion

new taxa could

become
established
only by
on
diversity,
and
other correction
SPECIALSECTION
plants,
insects,
or
vertebrates,
because regimes
marine
ecosystem
became saturated.
these be
groups
seem to have
Sepkoskis
coupled logistic
model (5)
as toradiated
produce data in
driving others
to extinction.
Key evidence
may
so complex
explosively,
without
diversity
plateaus,signals
identified
threeand
equilibria,
in the Camorigination
extinction
rates
which
geologic
and
are
is that both
plants,
insects,
orbiologic
vertebrates,
because
marine
ecosystem
became
saturated.
particularly
the
past 100 million
brian,been
most density-dependent
of the Paleozoic, and pernot
obviously
separated.
appear to have
these ingroups
seem to have radiated
Sepkoskis
coupled
logistic
model (5) (5
years (My) (10).
haps a third, beginning in the Pliocene
Life
on land
today
be as much
as
7), limiting
risesequilibria,
in diversity
andCampromoting
explosively,
without
diversity
plateaus,
identified
three
in
Resolution
between
themay
equilibriand
continuing
to the
the
present
(Fig.
particularly
in as
thelife
past
100sea,
million
brian,
most 2A).
of the
Paleozoic,
andevents.
per- levels
after
extinction
inand
the
so it
25
asand
diverse
rapid recovery
um times
models,
between
these
These
three equilibrium
years
(My)
haps
a third,correspond
beginning
theglobal
Pliocene
expansionist
models,
might seem
tointhree
sets
of phyla,
the
Alternative
models
for
diversimay
be
wrong
to(10).
generalize
from marine
straightforward,
but
thebetween
solution
Paleozoic,
and (Fig.
Modern,
that
Resolution
the
and
continuing
to the
present
allowing
global
paleontological
studies
to all delife.equilibriPerhaps
fication
areCambrian,
expansionist,
pendsand
on adequate
assessment
of
the these
interacted
and successively
um
models,
and
between
2A).
These
threetoequilibrium
levelsreplaced
similar
patterns
of and
exspecies
diversity
rise,
with damping,
but
land
sea
show
quality of the fossil record. The longeach other through the Cambrianexpansionist
models,
might
seem
correspond
to three sets limit
of phyla,
the Denwithout a predictable
(811).
(8,
ponential
increase
in
species
numbers
term saturation model for global diverOrdovician and Permo-Triassic interCm
O
S
D
C
P
Tr
J
K
Pg Ng
butdiffer
the
solution
deCambrian,
Paleozoic,
and
Modern,
thatextincof origination
and
sity dependence
9,
11),straightforward,
or(Fig.
perhaps
in their key
sification
2, bluethey
curve)
arises
vals, reaching
higher
equilibrium
levels
500
400
300
200
100
0
pends
on
adequate
the
interacted
replaced
from extensive
attempts
to correct
data as aof
after successively
each
replacement
event.
with
the
seaassessment
acting
giant
tion rates and
does
notlong-term
preclude
expansionist
rules
(13,
14),
Time
(Ma)
of error
the
fossil
Thediverlongeach
other
through
the
Cambriansets forquality
sampling
(6,where
7),record.
whereThe
second
model
7) identifiesby
a
models
because
they may
be(6,dampened
Gaussian
petri
dish,
species
as theterm
multiple-equilibria
and
expansingle
equilibrium
level from
the food
early
saturationand
model
for global diverOrdovician
and Permo-Triassic
interof
limiting factors
such as shortage
density-dependent,
2. Patterns
animal
genus
the past sity is equilibrial
O of
S marine
D
C
P
Trdiversification
J
K through
Pg Ng
originally
used
raw
data,
Paleozoic,
perhaps 400levels
Ma, to the Fig.
Fig. 2. Cm
Patterns
of marine
animal
genus
diversification
through sion models
sification
(Fig.
2,
blue
curve) arises
vals,
reaching
higher
equilibrium
530
My,
the
Phanerozoic.
The
two
lines
compare
current
estimates
from
by
or space, orpresent
active(Fig.
predation,
as well
asthe
and
thecorrection
land witnessing
400Phanerozoic.
300 The200
100
0
without
(5, 811),continuing
although (damp2B). In both
models,
the empirical
past500
530(uncorrected)
My, the
two(red
linesline)
compare
current
from
extensive
attempts
to correct
data
after
each
long-term
replacement
event.
the
Sepkoski
database
and
samplingclimate andequilibria
other physical
factors.
Further,
ened)
exponential
rise
in
diversity
more recent analyses return a some- as ever
correspond to biodiversity estimates from the empirical
(uncorrected)
database
Time
(Ma)
standardized (corrected) analysis
of the
Paleobiology Sepkoski
Database (blue
line).
sets
for
sampling
error
(6,
7),
whereThe
second
model
(6,
7)
identifies
a
what dampened
butecospace
congruent signal
saturation
in whichlogistic
new taxamodel
could The
the coupled
sectors of
are conquered
it seems that
(redempirical
line) and
sampling-standardized
(corrected)
analysisreached
of the new
curve
(red line) suggests that global
marine diversity
as
the multiple-equilibria
expansingle
equilibrium
from the
when
corrections
are imposed.
Cor-and
become
established
onlyearly
by driving aPaleobiology
for global
diversificamay be
partly
anlevel
artifact
of
taxonomic
(9,
14).
Any
model
Database
(blue
line).
The
empirical
curve
(red
line)
possible
plateau
throughanimal
the Paleozoic
(450
to 250 Ma)
and
has risen,
Fig.
2.
Patterns
of
marine
genus
diversification
through
the
past
sion
models
used
Paleozoic,
perhaps
400 itMa,
toworked
the out
rection
for encompass
samplingoriginally
is the
clearly
es- raw data,
others
extinction.
Key
evidence
is apparently
exponentially,
ever
since.
The
sampling-standardized
curve
suggests
that
global
marine
diversity
reached
a
possible
plateau
scale (Fig. 2,
red to
curve);
was
tion
must
independent
evi530 My, the Phanerozoic. The two lines compare current estimates from
sentialwithout
(6, 7), and
future investigation
that
both
and the
extinction
correction
(5, 811),of
although
present
(Fig.
2B).
In origination
bothlevels
models,
(blue
line)the
suggests
that (450
globaltomarine
diversity
reached
near-modern
through
Paleozoic
250database
Ma)
and(red
has
risen,
apparently
familial
but
does
not
for
increasing
complexity
organat ordinal
and
dence
the
empirical
(uncorrected)
Sepkoski
line)
and
samplingappropriate
indepenrates appear to
to biodiversity
have been density- levels some 400 Ma and there has been only modest increase since then. must determine
more recent
analyses
return a someequilibria correspond
exponentially,
ever analysis
since. The
sampling-standardized
curve(blue
(blueline).
specific
work convincingly
at generic
isms,
increases
in the occupation
standardized
(corrected)
ofD,
the
Paleobiology
Database
dent proxies
for preservation
and hu- of novel
dependent (57),
limitingorrises
di- Cm, Cambrian;
C, Carboniferous;
Devonian;
J, Jurassic;
K, Cretaceous;
what
dampened
but
congruent
signal
saturation in
which new taxa
could in The
line)
suggests
that
global
marine
diversity
reached
near-modern
curveO,(red
line) suggests
that global
marineS,diversity
man error; some
current proxies
(suchwithin parand promoting
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levels (10, versity
11), there
are problems
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explosive
evolution
Ng, Neogene;
Ordovician;
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when
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only
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levels
some
400
Ma
and
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as number
of fossiliferous
localities)
after extinction
events.
a possible
plateau
through
Triassic.
Based on
(6). the Paleozoic (450 to 250 Ma) and has risen,
assumptions
(11, 12), and
and addition
of novel clades
key numerical
ticular
clades,
since then.
Cm, Cambrian;
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rection dependent
for sampling
is clearly esothers to extinction.
Keymodels
evidence
is apparently
are
themselves
on
diversity,
Alternative
for
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diexponentially,
ever
since.
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sampling-standardized
the background assumption of a global rassic; K, Cretaceous; Ng, Neogene; O, Ordovician; P, Permian; Pg, without the loss of precursors (9, 11, 15),
sential
(6, may
7), and
investigation
that both origination
extinction allowing
and other correction
regimes
be sofuture
complex
partly that
an artifact
taxonomic
scale (Fig.
2, red near-modern
versification and
are expansionist,
global
(blue line)
suggests
globalof marine
diversity
reached
carrying capacitydiversity
is doubtful
(8,
11).
all data
of which
have
happened
many times in
Paleogene;
S, Silurian;
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Triassic.out
Based
on (6).
as
to produce
in which
geologic
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it was
atonly
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to rise,
with10,
damping,
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must
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Ma
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there
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hard to
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loMy.
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out proved
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dent proxies
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(57),
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in(811).
di-theDensity
Cm,
Cambrian;
C,
Carboniferous;
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Devonian;
J,
Jurassic;
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Cretaceous;
or specific
(10,extensive
11), there are
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withcor- Life on land today may be as much as 25
of origination
andspeciose
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ariseslevels
from
attempts
gistic model
to the
much
more
error; some current proxies (such
versity
and dence
promoting
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recovery
Ng, Neogene;
O,keyOrdovician;
P, Permian; Pg,
Paleogene;
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timesLarge-Scale
as diverse
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12),(6,
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expansionist
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error
al realm,
whether
considers
plants,
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as Controls
number
ofonfossiliferous
localities)
after
extinction
events.
Triassic.
Based on
(6). assumption of a global carrying capacity is wrong to generalize
from
marine
paleontologground
be
dampened
by
limiting
factors
such
as
shortage
because
these
groups
seem
to
and
expansion
models
Taxic
paleobiological
studies
have
provided
the
multiple-equilibria
or vertebrates,
arelife.
themselves
on
diversity,a
Alternative
models
fororglobal
diPerhaps dependent
land and sea
of food
or space,
active predation,
as well as by doubtful (8, 10, 11). Further, it has proved hard to ical studies to all
without
diversity
pla(5,
evidence
about
controls,
mainly
have
radiated
explosively,
originally
used
raw
data,
without
correction
great
deal
of
otherpatterns
correction
regimes increase
may beinso complex
an artifact
of taxonomic
scale
(Fig.more
2, redshowand
versificationclimate
are expansionist,
allowing
similar
of exponential
export
the logistic
model to the
much
and other physical
factors.global
Further, itpartly
years
Bioticthey
factors,
such
teaus, particularly
in
thewith
pastdamping,
100
million
811),
although
more
recent
analyses
return
abiotic,
on species
diversity.
(8,data
9, in
11),
or perhaps
speciose
terrestrial
realm,
whether
oneand
considers
seems to
that
the
coupled
logistic
model
may becurve);
as tonumbers
produce
which
geologic
and biologic
it was
worked
out
at ordinal
familialaspecies
species
diversity
rise,
but
withdampened
but
congruent
signal
whenor Court
(My)a (10).
as
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size,
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ability
somewhat
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notdiet,
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levels
but does
not the
work
atintrinsic)
generic
out
predictable
(811). Density
depenTable 1.limit
Macroevolutionary
phenomena
and their
support
for
either
Redconvincingly
Queen (biotic,
Jesterare
(physical,
extrinsic)
models.
Manyor ecologiResolution
equilibrium
models,
Correction
for samcorrections
are (10,
imposed.
specialization,
appear
to have
effect
on
couldbetween
fit either
worldview,
and
are noted
multilevel
mixed.
on land today
may
be aslittle
much
as 25
specific levels
11), there
are problems
with cal Life
dence
of origination
andthe
extinction
ratessodoes
not asor
expansionist
models,
investhe
diversity
of asmodern
organisms,
although
and between
these and
plingnumerical
is clearlyassumptions
essential (6,(11,
7),12),
and and
future
times
as
diverse
life
in
the
sea,
so
it
may
be
key
the
backpreclude
expansionist
models
because
they
may
Red Queen
Court Jester
Multilevel mixed
solution ground
life-history
characmight
seem by
straightforward,
tigationassumption
must determine
appropriate
indepenand r-selected
wrong to generalize
from marine
paleontologof a global
carrying capacity
is abundance
be
dampened
limiting factorsbut
suchthe
as shortage
Interspecific
competition
Waxing
and waning
of cladesfor
in association
with and humanVicariance
and dispersal
in major
phylogenetic splitslarge
(17)
preservation
error;
depends
adequate
assessment
quality
(short
dent proxies
ical studies
to gestation
all life. period,
Perhaps landlitter
andsize,
sea
(8, 10, 11).
Further, it has
proved hard
to teristics
of
food oron
space,
or active
predation,ofasthe
well
as
by doubtful
tectonic and oceanographic events (2, 17)
record.displacement
The long-term
saturation
as
number
of
fossome
current
proxies
(such
and
short
interbirth
intervals)
sometimes
correof the fossil
show
similar
patterns
of
exponential
increase
in
export
the
logistic
model
to
the
much
more
climate
andCharacter
other
physical
factors. Further,
it
Mass extinctions and smaller extinction events
Latitudinal diversity gradient (2224)
(Fig. may
2, triggered
blue
withnumbers
high species
model that
for global
diversification
siliferous
localities)
themselves
species
(8, richness
9, 11), (16).
or perhaps they
speciose
whether onedependent
considers late
seems
the coupled
logistic model
be by
extrinsicterrestrial
causes
suchrealm,
asare
eruptions,
0

The Red Queen and the Court Jester:

Species Diversity and the Role of Biotic
The Abiotic
Red Queen
andThrough
the Court
Jester:
and
Factors
Time
Species Diversity and the Role of Biotic
and Abiotic Factors Through Time

Number of genera
(empirical; red)

Speciation

climate change, anoxia, impact (10, 11)

Table 1. Macroevolutionary
phenomena Coordinated
and their support
for either the Red Queen (biotic, intrinsic)
or Court Jester (physical, extrinsic) models. Many
Evolutionary arms races (1)
turnovers, originations, and extinctions
Occupation of new ecospace (25)
could fit either worldview, and so are noted
as
multilevel
mixed.
in response to physical perturbations termed
Red Queen

coordinated stasis or turnover pulse hypothesis

(2, 29, 30) Court Jester
Nonconstant
probability
of extinction
(3, 11)with
Waxing and waning
of clades
in association

of ecological
InterspecificConstancy
competition
guilds through time (25)
tectonic and oceanographic events (2, 17)
Incumbency advantage
Lack of evidence for a global carrying capacity and
Character displacement
Mass
extinctions
and smaller extinction events
(3, 24)
equilibrium levels (8, 10)
triggered
extrinsic causes
suchevolutionary
as eruptions,
Lack ofby
cohesiveness
of the great
climatefaunas
change,
(12)anoxia, impact (10, 11)
Species turnovers,
richnessenergy
relationshipand
(18,extinctions
19)
Evolutionary arms races (1)
Coordinated
originations,

Constancy of ecological
guilds through time (25)
Incumbency advantage
(3, 24)

in response to physical perturbations termed

Inverse relationship between global temperature and
coordinated
stasis or turnover pulse hypothesis
biodiversity (21)
(2, 29,
30)
Lack of clear correlation of species richness with
Nonconstant
extinction
(3, 11)
body probability
size or other of
biotic
factors (16)
Lack of evidence for a global carrying capacity and
www.sciencemag.org
SCIENCE VOL 323
equilibrium
levels (8, 10)
Lack of cohesiveness of the great evolutionary
faunas (12)
Species richnessenergy relationship (18, 19)

Multilevel mixed
Subdivision
of niches/specialization
(10, 25)phylogenetic splits (17)
Vicariance
and dispersal in major
Declining global extinction rates through time (1, 5)

Latitudinal diversity gradient (2224)

Onshore-offshore patterns and disturbance (3)

Resource
use: stenotopes
more speciose
Occupation
of new are
ecospace
(25) than
eurytopes (29, 30)

Subdivision of niches/specialization (10, 25)

Declining global extinction rates through time (1, 5)
729
Onshore-offshore patterns and disturbance (3)

6 FEBRUARY 2009

Resource use: stenotopes are more speciose than

eurytopes (29, 30)

Inverse relationship between global temperature and

biodiversity (21)
Lack of clear correlation of species richness with
body size or other biotic factors (16)

23
www.sciencemag.org

SCIENCE

VOL 323

6 FEBRUARY 2009

729

their continuing diversification in the Late Jurassic

and Cretaceous was mainly indistinguishable from
a random walk. In particular, dinosaurs did not
participate in the Cretaceous Terrestrial Revolution, some 130 to 100 Ma, when flowering plants,
leaf-eating insects, social insects, squamates, and
many other modern groups radiated substantially.

245.9

237

Anisian

shifts should mainly occur low in a clades history:

Clade shapes vary from bottom-heavy to topheavy, and diversification shifts may be concentrated low (dinosaurs and bats) or high (insects
and ants) in a clade (26).
In the future, the identification of diversification
shifts across numerous taxa may provide evidence

232.5 228

Lad

203.6 199.6

Crn

Norian

Rh. EJ

PTEROSAURIA

Dinosauromorphs
ORNITHISCHIA

Dinosauria

SAUROPODOMORPHA
THEROPODA
PHYTOSAURIA

Crurotarsi

AETOSAURIA
CROCODYLOMORPHA

Rauisuchids
POPOSAUROIDEA
ORNITHOSUCHIDAE

B
0.12

Principal coordinate 2

0.06
0

Dinosaur morphospace

-0.06
-0.12

Pterosaur morphospace

-0.18
-0.24
-0.3
Crurotarsan morphospace
-0.36
-0.24

-0.16

-0.08

0.08

0.16

0.24

0.32

Principal coordinate 1

Fig. 3. Phylogenetic relationships and morphospace occupation for Triassic archosaurs. (A) Framework
phylogeny for Triassic crurotarsans scaled to the Triassic time scale. Numbers at top refer to millions of years
before the present; gray bars represent the observed durations of major lineages; vertical dashed lines denote
two extinction events, at the Carnian-Norian and Triassic-Jurassic boundaries; arrowheads indicate lineages that
survived the latter event. Lad, Ladinian; Crn, Carnian; Rh, Rhaetian; EJ, Early Jurassic. (B) Empirical morphospace
for Late Triassic archosaurs, based on the first two principal coordinates. Large circles, dinosaurs; ovals,
pterosaurs; squares, poposauroids; hexagons, phytosaurs; stars, aetosaurs; crosses, crocodylomorphs; smaller
black dots, rauisuchids; larger black dots, nondinosaurian dinosauromorphs, Scleromochlus. Based on (28).

Geographic and tectonic history has generated patterns of species diversity through time.
The slow dance of the continents as Pangaea
broke up during the www.sciencemag.org
past 200 My has
affected
SCIENCE VOL 323
modern distribution patterns. Unique terrestrial
faunas and floras, notably those of Australia and
South America, arose because those continents
were islands for much of the past 100 My. Further, major geologic events such as the formation of the Isthmus of Panama have permitted
the dispersal of terrestrial organisms and have
split the distributions of marine organisms. A
classic example of vicariance is the fundamental
division of placental mammals into three clades,
Edentata in South America, Afrotheria in Africa,
and Boreoeutheria in the northern hemisphere,
presumably triggered by the split of those continents 100 Ma (17). Other splits in species trees
may relate to dispersal events, or there may be
no geographic component at all.
Species richness through time may correlate
with energy. The species richnessenergy relationship (18) posits correlations with evapotranspiration, temperature, or productivity, and
studies of terrestrial and marine ecosystems
have shown that these factors may explain as
much as 90% of current diversity, although relationships between species diversity and productivity change with spatial scale (19). Over long
time spans, there are strong correlations between
plankton morphology and diversity and water
temperature: Cooling sea temperatures through
the past 70 My, and consequent increasing ocean
stratification, drove a major radiation of Foraminifera, associated with increasing body size
(20). More widely, there is close tracking be-

24

Court Jester worldviews. If the majority of diversification shifts are coordinated, and associated
with particular climatic, tectonic, and geographic
drivers, then the Court Jester model of macroevolution would prevail. This would link most
increases in species diversity to particular largescale radiation events, such as the Cretaceous Terrestrial Revolution (26), or recoveries after mass
extinctions. If, on the other hand, the majority of
diversification shifts are unique to particular clades,
and not coordinated temporally with others, then
the Red Queen worldview might be considered.
Comparing Sister Taxa
A powerful element of the comparative phylogenetic approach
to species diversity relationships
through time
Fig.
3. Phylogenetic
and moris the opportunity to compare sister taxa. Sisters
phospace
occupation
fortheirTriassic
archosaurs.
arose from a single
ancestor, and so
trajectoriesFramework
occupy the same amount
of time, and
(A)
phylogeny
for Triassic cruthey started with the same genotype and pherotarsans
scaled
tosubsequent
the Triassic
time scale.
notype. Any similarities
in their
evolution probably reflect this phylogenetic signal of
Numbers
at top refer to millions of years
a common origin, but differences reflect independent aspects
separate histories.
before
theof their
present;
gray bars represent the
Comparisons of sister taxa have allowed tests
observed
durations
of the resource-use
hypothesis (29),of
thatmajor
general- lineages; verists are less speciose and have longer species
tical
dashed lines denote two extinction
durations than specialists. Specialists divide the
physical environment
small patches, each
events,
at theintoCarnian-Norian
and Triassicoccupied by a species, and each probably more
Jurassic
boundaries;
arrowheads
indicate
subject to environmental
crises than their
generalist relatives. Classic
examples
in support
of latter
the
lineages
that
survived
the
event.
Lad,
resource-use hypothesis come from studies of NeLadinian;
Carnian;
Rh,
Rhaetian; EJ, Early
ogene mammalsCrn,
(29). For
example, two
antelope
subgroups, the tribes Alcelaphini and Aepycerotini,
Jurassic.
morphospace
for Late
diverged 6 to (B)
8 Ma.Empirical
The former is now
highly
speciose, witharchosaurs,
some 7 living and 25
extinct speTriassic
based
on the first two
cies, and the latter is represented by two species,
principal
coordinates.
Large
only one, the impala
Aepyceros, surviving.
The circles, dinoslowly evolving Aepycerotini consists of few
saurs;
ovals,
pterosaurs;
squares,
poposauspecies at any time, and each of those is long
lived, whereas
the speciosephytosaurs;
Alcelaphini consistsstars, aetosaurs;
roids;
hexagons,
of many short-lived species. The ecological
crosses,
crocodylomorphs;
habits of both clades
differ: The impala has a smaller black
broad, generalist
diet, whereas the
specioseblack
aldots,
rauisuchids;
larger
dots, nondicelaphines show more dietary specialization. In
nosaurian
dinosauromorphs,
wider studies of many
clades of Neogene African Scleromochlus.
and South American mammals (30), the resourceBased
onwas
(28).
use hypothesis
supported, and some subsidiary
predictions confirmed: Specialists are more common than generalists, carnivores include more
generalists than herbivores, and there are more
specialists in habitats that underwent recent environmental change (tropical rain forests and
deserts). The resource-use model then stresses
the role of climate and tectonic movements in
determining species diversity rather than biological
controls such as competition and predation.

tween temperature and biodiversity on the global scaleOutlook

for both marine and terrestrial organisms
Paleontologists and evolutionary ecologists have
debated species
diversity and
largely familial
independently. richness were
(21), where
generic
relatively
low during warm greenhouse
phas6 FEBRUARY 2009
731
es of Earth history, coinciding with relatively
high origination and extinction rates.
A much-studied manifestation of energy and
temperature gradients is the latitudinal diversity
gradient (LDG), namely the greater diversity of
life in the tropics than in temperate or polar regions, both on land and in the sea. There are two
explanations (22): (i) the time and area hypothesis, that the tropical belt is older and larger than
temperate and polar zones, and so tropical clades
have had longer to speciate, or (ii) the diversification rate hypothesis, that there are higher rates
of speciation and lower rates of extinction in the
tropics than elsewhere. There is geological and
paleontological evidence for a mixture of both
hypotheses (23, 24).
Species diversity may increase by the occupation of new ecospace. The number of occupied guilds, that is, broad ecological groupings
of organisms with shared habits, has increased
in several steps through time, from 20 in the
early Paleozoic to 62 in post-Paleozoic marine faunas (25). Further, marine animals have
shown several step increases in tiering, the ability to occupy and exploit different levels in the
habitat: At times, burrowers have burrowed
deeper, and reef-builders have built taller and
more complex reefs. Analogous, if even more
dramatic, expansions of ecospace have occurred
on land, with numerous stepwise additions of
new habitats, from the water-margin plants and
arthropods of the early Paleozoic to the forests

and upland habitats of the later Paleozoic when

land animals first burrowed, climbed, and flew,
through the introduction of herbivory, giant size,
endothermy, and intelligence among vertebrates,
and the great blossoming of flowering plants
(with associated vast expansions in diversity of
plant-eating and social insects and modern vertebrates) during the Cretaceous Terrestrial Revolution 100 Ma (26).
The other mode of species increase globally
or regionally is by niche subdivision, or increasing specialization. This is hard to document because of the number of other factors that vary
between ecosystems through time. However,
mean species number in communities (alpha diversity) has increased through time in both marine (15, 25) and terrestrial (10) systems, even
though niche subdivision may be less important
than occupation of new ecospace in increasing
biodiversity. Further, morphological complexity
may be quantified, and a comparative study of
crustaceans shows, for example, that complexity
has increased many times in parallel in separate
lineages (27).

Phylogenetic Studies of Clade Histories

Species are not randomly distributed; they have
an evolutionary history, and so occur as twigs
on a great phylogenetic tree. Studying species
as members of clades is a fruitful approach to
understanding the drivers and controls on speciation. Key questions include (i) Do species
diversify early in a clades history? (ii) How do
diversity and disparity (variance in characters
or morphology) covary? (iii) Do major lineages
within a clade follow similar, or different, patterns, and if different, why? (iv) Do evolutionary
radiations follow the acquisition of new characters or emptying of ecospace? (v) How do major
clades of apparent competitors interact over long
spans of geologic time? and (vi) How do sister
clades vary in species diversity and why?
For such analyses, the ideal is a complete
species tree, a phylogenetic tree that contains
all species living and extinct, plotted accurately
against geologic time (4). Simple to say; hard
to achieve. More commonly, incomplete trees
have been used, with the risk of error in calculations of evolutionary rates or comparisons of
subclades. In paleontology, it has proven much
easier to work with higher taxa such as genera or
families because species fossil records are less
complete than those of higher taxa, and yet it
is not clear how higher-level patterns relate to
those at species level. Many key questions can
be tackled by comparing a real tree to a hypothetical tree that follows an equal-rate Markov
(ERM) model, equivalent to tree growth after a
random walk, where equal chances of speciation
and of extinction are shared by all species (4).
Major biotic replacements, where one clade
replaces another, have been a focus of debate
about the roles of competition and progress in

macroevolution, and dinosaurs provide a classic

example. The standard view was that dinosaurs
originated in the Late Triassic, some 230 Ma, by
a process of competition in which they prevailed
over their precursors, the crocodile-like crurotarsans and others, because of superior adaptations.
A comparative phylogenetic study (28) shows,
however (Fig. 3), that the Dinosauria expanded
in two steps, one after an extinction event 225
Ma that removed dominant herbivores, and the
second following the end-Triassic extinction 200
Ma that removed most of the crurotarsans. Dinosauria remained at moderate diversity and low
disparity, and at lower disparity than the crurotarsans they supposedly out competed, during
the 25 My between the events, suggesting that
there was no insistent competition driving other
groups to extinction but rather that the dinosaurs
occupied new ecospace opportunistically, after it
had been vacated.
A further study on Dinosauria explored the
subsequent evolution of the clade (26). Classic
views that the dinosaurs arose with a flourish,
and then finally gave way in the Cretaceous to
the superior mammals, or that they dwindled to
extinction because of racial senility, had long
been abandoned. The dinosaurs seemed to be
radiating actively in the Cretaceous, with many
new clades appearing through their last 55 My,
and especially in their final 15 My. The new
study (26) shows that most diversification shifts
(departures from ERM assumptions) fall in the
first one-third of the history of the clade and that
their continuing diversification in the Late Jurassic and Cretaceous was mainly indistinguishable
from a random walk. In particular, dinosaurs
did not participate in the Cretaceous Terrestrial
Revolution, some 130 to 100 Ma, when flowering plants, leaf-eating insects, social insects,
squamates, and many other modern groups radiated substantially. There is no geometric reason
that diversification shifts should mainly occur
low in a clades history: Clade shapes vary from
bottom-heavy to top-heavy, and diversification
shifts may be concentrated low (dinosaurs and
bats) or high (insects and ants) in a clade (26).
In the future, the identification of diversification shifts across numerous taxa may provide
evidence for the relative importance of the Red
Queen and Court Jester worldviews. If the majority of diversification shifts are coordinated,
and associated with particular climatic, tectonic,
and geographic drivers, then the Court Jester
model of macroevolution would prevail. This
would link most increases in species diversity
to particular large-scale radiation events, such
as the Cretaceous Terrestrial Revolution (26), or
recoveries after mass extinctions. If, on the other
hand, the majority of diversification shifts are
unique to particular clades, and not coordinated
temporally with others, then the Red Queen
worldview might be considered.

Comparing Sister Taxa

A powerful element of the comparative phylogenetic approach to species diversity through time
is the opportunity to compare sister taxa. Sisters
arose from a single ancestor, and so their trajectories occupy the same amount of time, and they
started with the same genotype and phenotype.
Any similarities in their subsequent evolution
probably reflect this phylogenetic signal of a
common origin, but differences reflect independent aspects of their separate histories.
Comparisons of sister taxa have allowed tests
of the resource-use hypothesis (29), that generalists are less speciose and have longer species
durations than specialists. Specialists divide the
physical environment into small patches, each
occupied by a species, and each probably more
subject to environmental crises than their generalist relatives. Classic examples in support of
the resource-use hypothesis come from studies
of Neogene mammals (29). For example, two
antelope subgroups, the tribes Alcelaphini and
Aepycerotini, diverged 6 to 8 Ma. The former
is now highly speciose, with some 7 living and
25 extinct species, and the latter is represented
by two species, only one, the impala Aepyceros,
surviving. The slowly evolving Aepycerotini
consists of few species at any time, and each
of those is long lived, whereas the speciose Alcelaphini consists of many short-lived species.
The ecological habits of both clades differ: The
impala has a broad, generalist diet, whereas the
speciose alcelaphines show more dietary specialization. In wider studies of many clades of
Neogene African and South American mammals
(30), the resource-use hypothesis was supported, and some subsidiary predictions confirmed:
Specialists are more common than generalists,
carnivores include more generalists than herbivores, and there are more specialists in habitats
that underwent recent environmental change
(tropical rain forests and deserts). The resourceuse model then stresses the role of climate and
tectonic movements in determining species diversity rather than biological controls such as
competition and predation.
Outlook
Paleontologists and evolutionary ecologists have
debated species diversity largely independently.
The realization that the Red Queen and Court
Jester models may be scale-dependent, and that
evolution may be pluralistic (3), opens opportunities for dialog. Taxic studies in paleontology continue to have great value in highlighting
correlations between species richness and other
factors, but comparative phylogenetic methods
will illuminate questions about clade dynamics, species richness, and the origin of novelties.
Further, methods are shared by paleontologists
and neontologists, and this allows direct communication on the patterns and processes of

macroevolution. Viewed close up, evolution is

all about biotic interactions in ecosystems (Red
Queen model), but from further away, the large
patterns of biodiversity are driven by the physical environment (Court Jester model).
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25

theories of the process (8, 11). I leave out discussion of sympatric

and allopatric speciation but
SPECIALSECTION
Under
this the
Darwinian
instead
identify
likelihoodperspective,
of ecologicallinkand
was
relatively
ing
speciation
with
adaptation
mutation-order
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when
there
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gene
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of
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for the
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has
evolved. I also
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(2007).
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126Schluter
(2003).
Dolph
Science
1939
[the
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evenspeciation
though
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Darwin,stages.
Voyage on
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46. C. E. Parent, B. J. Crespi, Evolution 60, 2311 (2006).
theC.early
symposium
speciation
before
major
Natural
drives
the origin
as Darwin
initially
Mechanisms of
1909),
p. 383.concept (7)], an extensive comRev. Ecol.
Syst. 33,claimed.
475 (2002).
47. J. A. selection
Coyne, T. D.commonly
Price, Evolution
54, 2166
(2000). of species, Annu.
logical
species
speciation
by D.
selection
fall into
mutation-order.
Under
66. We thankand
A. Birand,
R. Glor, A.from
Harrison, L. Harmon,
58. ecological
J. J. Wiens, C.and
H. Graham,
Annu. Rev. Ecol.
Syst. 36, 519 Speciation
48. J. B. Losos,
Schluter, Nature
408,two
847 broad
(2000). categories:
Adaptation
inparative
and biogeographic
studyand
showcased
D Jablonski,
L. Mahler, C. Marshall,
the anonymous
49. D. Lack,speciation,
Darwins Finches
(Cambridge is
Univ.
Press, by divergent(2005).
ecological
divergence
driven
natural selection between environments,
Darwin
to
Dobzhansky
stances
in
which
derived
morphological
and
life
reviewers
for useful
comments.
Supported by the
NSF
59. S. Skulason, T. B. Smith, Trends Ecol. Evol. 10, 366
Cambridge, 1947).
whereas under mutation-order speciation, divergence occurs when different mutations arise and
(grant
DEB-0519777)
and
thearisen
NIH between
(grant
(1995).
50. U. Dieckman, M. Doebeli, J. A. J. Metz, D. Tautz, Adaptive
Appreciation
of
connection
adaptaofthe
fishes
had
overGM56693).
and
over
history
forms
are fixed
in separate
adapting
to similar60.
selection
pressures.
of parallel
evolution
H. D. Bradshaw,
D. W.Tests
Schemske,
Nature 426,
176
Speciation
(Cambridgepopulations
Univ. Press, Cambridge,
2004).
tion
and
speciation
began
withtype
Darwin
when
a
(12).
The
reagain
from
the
same
ancestral
of51.reproductive
trait-based
assortative
and reproductive isolation by active
10.1126/science.1157966
(2003).
U. K. Schliewen,isolation,
D. Tautz, S. Pbo,
Nature 368,
629 (1994). mating,
morphological
concept
of nonparasitic
species largely
prepeated,
parallel
origin
of
lamprey
selection have demonstrated that ecological speciation is a common means by which new species
vailed.
In Onfrom
the Origin
of Species,
Darwin
wrote
in streams
the same
migratory,
parasitic
arise. Evidence for mutation-order speciation by natural selection is more limited and has been
that
I look
at thethat
termAgain
species,
asagain
one arbitrarily
and
the
paraancestor
showed
best documented by instances of reproductive isolation resulting from intragenomic conflict.
given
forofthe
sake
ofevolved
convenience
to aout
setdisof
nonparasitic
sitic
lampreys
have
into
theories
the
process
(8,
11).
I
leave
However,
we
still
have
not
identified
all
aspects
of
selection,
and
identifying
the
underlying
genes
REVIEW
individuals
closely
resembling
each
other...
and
forms...correlated
with
in small
streams,
cussion of sympatric
and life
allopatric
speciation
but
for reproductive isolation remains challenging.
The
amount
of difference
is one
very
important
where
a identify
suitable
foodlikelihood
supply
inofthe
way
of large
instead
the
ecological
and
criterion
in settling
whether(12).
two
forms
should
be
or seasonal
When
correlated
fish
is scarce
mutation-order
speciation
when
there
is gene
ries:
ecological
speciation
and
mutation-order
tttook
evolutionary
biologists
nearly
150
years,
ranked
as
species
or
varieties
(1).
Under
this
flow. environmental
I ignore reinforcement,
a special
type of
took evolutionary biologists nearly 150 would nevertheless be advantageous in both of with
repetition
is
factors, such
speciation
is thought
defined
as
accumulation
of
Ecological
refers to the
but
at last
can we
agree
Darwin
the speciation.
natural
selection
to the
favor
stronger precanwith
agree
with that
Darwin
of view,
years,
butwe
at last
their environments.
Thespeciation
relative importance
unlikely
to result
from chance;
environmental
origin
of species, that mystery of mysteries evolution of reproductive isolation between pop- sufficiently
many differences
between
populamating reproductive
isolation
oncebepostzygotic
pressures must
therefore
the cause
that the origin of species, that mystery of these two categories of mechanism for the ori- selection
(1), really does occur by means of natural selection ulations or subsets of a single population by ad- tions
to warrant
their Iclassification
as separate
isolation
has
evolved.
also
ignore
speciation
by
mysteries
(1), really does occur by means of gin of species in nature is unknown.
of speciation. As a result of our recent studies
Dolph Not
Schluter
(25).
all species appear to evolve by aptation to different environments or ecological taxonomic
species.
Darwin
understood
the
impolyploidy,
even though
selection
might be
crucial
In this review, I summarize progress in un- on
being
added
to
fishes...weight
is constantly
natural selection (25). Not all species appear to
selection, but the evidence suggests that most of niches (2, 8, 9). Natural selection is divergent, portance
of reproductive
barriers between species
in the
early
stages.
but
the
evidence
suggests
features
of
speciation
evolve
by
selection,
derstanding
the
general
the
theory
that
speciation
is...under
the
rigid
Natural
origin of species,
initially
claimed.
Mechanisms
of (1), but the study of speciation after the pubactingas
in Darwin
contrasting
directions
between
environthem
do.selection
The effortcommonly
leading updrives
to thisthe
conclusion
to by selection.
speciation control of the environment (12). However, this
that
most of
do. The
leading
Iand
do mutation-order.
not differentiateUnder
speciation
bythem
selection
fall effort
into
broadupcategories:
ecological
which drives
the fixation of different lication
involved
many
experimental
and two
conceptual
ad- ments,
of this work
focused mainly
on the evoSpeciation
Adaptation
from of
referring
to the origin
morphothis
conclusion
involved
many isexperimental
by sexual selection
herebetween
becauseenvironments,
natural selec- case
is onlyand
ecological
speciation,
divergence
selection
alleles,natural
each advantageous
in one environment lution
vances,
including
a revision
of the driven
notionbyofdivergent
oftospecies
differences, particularly of
Darwin
Dobzhansky
advances,
including
a
revision
drives
the
divergence
of
mate
preferences,
logical
species.
and
conceptual
tion
whereas under
speciation,ofdivergence
occurs
when
different
mutations
in the
other.
Following
G. S. arise
Maniand
and morphological
speciation
itself, mutation-order
80 years after publication
On but not
but also of between
behavioral
and
Appreciation
oftraits
the
connection
adapta80
years
orTests
mutation-order
mechaThe
turning
point
for speciation studies
of
notion
of Species,
speciation
byselection
either
ecological
arethe
fixed
in
populations
adapting
toon
similar
pressures.
of parallel evolution
B.
C.
Clarke
(10), I define
mutation-order
specia- other
the
Origin
of separate
the
to aitself,
definition
basedafter
phenotypic
traits.
tion and
speciation
beganconcept
with Darwin
when a
to mating,
(8, 11).byI came
of speciation
publication
ofisolation
On
the instead
Origin
of the
Species,
nisms,
in most
theories
of
the process
with
the Darwinian
modern
of reproductive
isolation,
trait-based
assortative
reproductive
isolation
byisolation
active
tion
as and
the
evolution
of reproductive
reproductive
of
morphological
Under
this
linking
morphological
concept
of perspective,
species
largely
of prethe
a
definition
based
on
reproductive
isolation
inleave
out
discussion
of
sympatric
and
allopatric
Species
separation
is
defined
as
a
stage
selection have
is a common
means
which of
newdifferent
species speciation with adaptation was relatively straightthe chance
occurrence
andbyfixation
differences
(6, 7).demonstrated that ecological speciation
vailed.
In
On
the
Origin
of
Species,
Darwin
wrote
differences
(6,
7).
speciation
but
instead
identify
the
likelihood
of
evolutionary
process
at
which
physiological
stead
of
morphological
arise.
Evidence
for
mutation-order
speciation
by
natural
selection
is
more
limited
and
has
been
The main question today is how does selec- alleles between populations adapting to similar forward,
requiring
test of whether
that I look
at theonly
termabecome
species,
as
one phenotyparbitrarily
main
question
todayare
is of
how
does selec-isolation
and mutation-order
speciation
when ic
mechanisms
developed
(6)
ecological
isolating
bestThe
documented
by instances
resulting
from
intragenomic
conflict.
selection
pressures.
Reproductive
isolation
evolves
tion
lead
to speciation?
What
thereproductive
mechanisms
differences
between
species
were
caused
by
given
for
the
sake
of
convenience
to
of
What
are
the
mechareinforcement,
a
spetoa set
mean
tion
lead
to
speciation?
there
is
gene
flow.
I
ignore
(here,
physiological
is
interpreted
However,
we
still
have
not
identified
all
aspects
of
selection,
and
identifying
the
underlying
genes
of natural selection, what genes are affected, and because populations fix distinct mutations that natural
selection.
For
example,
at
the
American
individuals
closely
resembling
each
other...
and
favor
nisms
naturalatisolation
selection,
what
genes
are af- would
cial type
of naturalbeselection
thought
evolved reproductive
isolation between
populafor reproductive
remains
challenging.
nevertheless
advantageous
in to
both
of Association
how
doofchanges
these genes
yield
the habitat,
forofthedifference
Advancement
Science
1939
The amount
is oneofvery
important
from[the
geographical
barriers to
fected, and mechanical,
how do changes
at these
genes yield their
stronger
premating reproductive
isolation once
tions, as distinct
environments.
The relative importance
of speciation
behavioral,
chemical,
physiological,
symposium
last
major
symposium
criterion in settling whether two forms should be
chemical, these
isolationofhas
evolved. for
I also
species
were
deinterbreeding).
Subsequently,
the other
habitat, behavioral, mechanical,
postzygotic
categories
mechanism
the ignore
origin on
and
that are
the reproducspeciation
before
the varieties
biological
species
concept
ecological
speciation
and mutation-order
t took incompatibilities
evolutionary biologists
nearly
150 years, ries: two
ranked
as species
or
(1).
Under
this
that
even though selection (7)],
physiological,
and other
incompatibilities
speciation
bynature
polyploidy,
finedanasextensive
groups of
interbreeding
natural popuof
species
in
is
unknown.
tive
barriers
between
new
species?
As
a
start,
the
comparative
and
biogeographic
but at last we can agree with Darwin that the speciation. Ecological speciation refers to the view, speciation is defined as the accumulation of
that are instances
reproductively
isolated
from
are theways
reproductive
between new
be crucial
in
the early stages.
lationsshowcased
In this
review,
I summarize
progress
in undermany
which barriers
new
arisespeby might
in which
derived
morevolution
of reproductive
isolation
between
pop- study
origin ofbyspecies,
thatspecies
mysterymight
of mysteries
sufficiently many
differences
between
populathe many
ways
by
which
new standing the general features of speciation by se- phological
this of
point
on,had
the
other such and
groups
(7). From
cies? As can
a start,
selection
be
grouped
into
two
broad
categolife
history
forms
fishes
(1), really does occur by means of natural selection ulations or subsets of a single population by ad- tions to warrant their classification as separate
Speciation
and
Adaptation
from
Darwin
can
be
grouped
the
evoluspecies
might
arise
by
selection
study
of
speciation
was
the
study
of
lection.
I
do
not
differentiate
speciation
by
sexual
arisen
over
and
over
again
from
the
same
ancestral
(25). Not all species appear to evolve by aptation to different environments or ecological taxonomic species. Darwin understood the imto
Dobzhansky
into
two broad
categories:
ecological
speciation
tion
of
reproductive
isolation
(3).between
Progress
up
to
here
natural
selection
the type
(12).
repeated,
parallel
origin
ofspecies
nonniches
(2,
8, because
9). Natural
selection
is drives
divergent,
selection,
but
the
evidence
suggests
most of selection
portance
ofThe
reproductive
barriers
Biodiversity
Research
Centre and
Zoologythat
Department,
divergence
of of
mate
by either
eco- parasitic
lamprey
in streams
frombetween
theafter
same
and
speciation.
Appreciation
the preferences,
connectionbetween
between
adapthen
in understanding
link
morphoUniversity
British
Columbia,
Vancouver,
V6T spe1Z4,
acting in contrasting
directions
environthemmutation-order
do.ofThe
effort
leading
up toEcological
thisBCconclusion
(1), but
the study
of the
speciation
themigrapuborwhich
mutation-order
most tory,
parasitic
showed
that was
Again
and
Canada.
E-mail:
schluter@zoology.ubc.ca
toexperimental
the evolution
reproductive
with Darwin
when
adaptation
largely
ciation
refers
tation
speciation
logical
speciation
ments,and
drives began
themechanisms,
fixation
of in
different
involved
many
andofconceptual
ad- logical
lication
of thisancestor
workand
focused
mainly
on the
evoor
subsets
of
a
under
isolation
between
populations
a
morphological
concept
of
species
largely
forgotten,
its
contributions
uncertain
vances, including a revision of the notion of alleles, each advantageous in one environment lution of species differences, particularly the
of
On
the Following
Origin of Species,
Darwin
single
population
adaptation
to different
concept. traits but also of behavioral and
but not in In
theSCIENCE
other.
S. Mani
and new
speciation
itself, 80byyears
after publication
of enOn prevailed.
morphological
www.sciencemag.org
VOL G.
323
6 FEBRUARY
2009
737
lookI at
the mutation-order
term species, as
one other
Thephenotypic
biologicaltraits.
species concept must surely
vironments
ecological
niches
(2, 8, 9).
Natuthat I(10),
B. C. Clarke
define
speciathe Origin oforthe
Species, to
a definition
based
on wrote
divergent,
acting
contrasting arbitrarily
difficultperspective,
to investigate
any
given forofthe
sake of convenience
made this
it more
ral
selection isisolation
tion as the evolution
reproductive
isolation by haveUnder
reproductive
instead
of in
morphological
Darwinian
linking
selection.
T.
directions
set of individuals
resembling
each link
between
speciation
natural
thea chance
occurrence closely
and fixation
of different
differencesbetween
(6, 7). environments, which drives to
speciation
with
adaptationand
was
relatively
straightand The
amount ofadapting
difference
is one Dobzhansky
the The
fixation
differenttoday
alleles,
eachdoes
advanta(13) only
suggested
the genes
unalleles between
populations
to similar
mainofquestion
is how
selec- other...
forward, requiring
a test ofthat
whether
phenotypin to
onespeciation?
environment
the other. very
criterion
in settling
whether
two derlying
differences
between
in orimportant
geous
selection
pressures.
Reproductive
isolation
evolves
tion lead
Whatbut
arenot
thein
mechanisms
ic differences
between
speciespopulations
were caused
by
andgenes
B. C.areClarke
(10),
speciesmutations
or varieties
were unlikely
to be the
Following
G. S. Mani
should
be ranked
traits
because
populations
fix as
distinct
that dinary
of natural selection,
what
affected,
andI forms
natural phenotypic
selection. For
example,
at the American
the habitat,
evolu- (1).
as the
changed
define
speciation
as the
Under
this view,be
speciation
is defined
of reproductive
isolation. He
would
nevertheless
advantageous
in both
of basis
how domutation-order
changes at these
genes yield
Association
for the Advancement
oflater
Science
1939
tion
of reproductive
the chance accumulation
of sufficiently
many
differences
mind, but
at the time
and the
their environments.
The relative
importance
of his
behavioral,
mechanical,isolation
chemical,byphysiological,
speciation
symposium
[thethis
lastviewpoint,
major symposium
and fixation of that
different
be- between
to mechanism
warrant their
greater
of studying
reprooccurrence
these twopopulations
categories of
forclassificathe origin generally
and other incompatibilities
are thealleles
reproducon speciation
beforedifficulty
the biological
species concept
of species
in nature
is unknown.
tive barriers
betweenadapting
new species?
As a start,
the tion
(7)], an extensive
comparative
and biogeographic
to similar
selecspecies. Darwin un- ductive
morphology,
must have
tween
populations
as separate
taxonomic
isolation than
In thisthe
review,
I summarize
progress inbarriers
under- discouraged
manypressures.
ways by which
new species
might evolves
arise by derstood
study showcased
instances
in which derived
mortion
Reproductive
isolation
importance
of reproductive
many
from pursuing
the connecstanding species
the general
of speciation
by se- tion.
selectionpopulations
can be grouped
into twomutations
broad categophological
and no
liferesearch
history effort
forms followed
of fishes that
had
because
fix distinct
that between
(1), features
but the study
of speciation
Virtually
lection.
do not differentiate
speciation
bymainly
sexual tested
arisen the
overrole
andofover
again from
the same ancestral
of this work
focused
adaptation
in speciation.
after
theIpublication
selection here because natural selection drives the type (12). The repeated, parallel origin of nonBiodiversity Research Centre and Zoology Department, on the evolution of species differences, particudivergence
of mate preferences,
by either
eco- Models
parasitic lamprey
in streams
from the same migraof Speciation
by Selection
of morphological
traits but also
of behavUniversity of British Columbia, Vancouver, BC V6T 1Z4, larly
logical
or
mutation-order
mechanisms,
in
most
tory,
parasitic
ancestor
showed
Again and
Canada. E-mail: schluter@zoology.ubc.ca
The topic of natural selection that
in speciation
is
ioral and other phenotypic traits.
REVIEW

Evidence for Ecological Speciation

and Its Alternative

Evidence for Ecological Speciation

and Its Alternative

II

26

www.sciencemag.org

SCIENCE

VOL 323

6 FEBRUARY 2009

737

Speciation

way becau
parasitic
lampreys
have evolved ecologiinto non- A Gambusia
models
of speciation,
once again receiving attention. The two most again theBoth
ulations d
forms...correlated
life in small
general hypotheses involving selection are parasitic
cal and
mutation-order,with
are theoretically
mutations
where a suitable food supply in the way
ecological and mutation-order speciation. Eco- streams,
plausible,
and only data can determine
order. Div
of large fish is scarce or seasonal (12). When corimportance
nature.
The
logical speciation is defined as the evolution related
their
relative
chastic bu
with
environmental
factors,insuch
repetition
of reproductive isolation between populations is unlikely
key is to
out bychance;
whichenvironmental
mechanism
from gene
to figure
result from
reproductive
isolation
firstbeevolved
by divergent natural selection arising from dif- selection
both smal
pressures must
therefore
the cause(3).
of
infinite) p
result ofgenetic
our recentdifferences
studies on
Once As
the aearliest
ferences between ecological environments (2, speciation.
can be ec
is constantly
being added
to the
8, 9, 14). It predicts that reproductive isolation fishes...weight
have accumulated
between
populations
mutationspeciation
is...under
the rigidmutations
control of
either
process,
subsequent
should evolve between populations adapting to theory
by that
ecology d
the environment (12). However, this case is only
contrasting environments but not between pop- referring
might
beorigin
favored
in one population
gence as s
to the
of morphological
species.
and turning
not the
other
because studies
of epistatic
ulations adapting to similar environments. The The
evolution
point
for speciation
came
with genetic
background
basic idea has been around for a while (7), al- withinteractions
ductive iso
the modern concept
of speciation
Species
tion of eco
is defined
as a stage
of the evoluthough it was tested only recently. The agents of separation
(10). Hence,
epistasis,
including
that
postzygot
process Dobzhansky-Muller
at which physiologicalincomisolat- B Mimulus
producing
divergent selection are extrinsic and can include tionary
Specia
ing
mechanisms
become
developed
(6)
(here,
abiotic and biotic factors such as food resources, patibilities in hybrids between species
tragenomi
physiological is interpreted to mean evolved
climate, habitat, and interspecies interactions reproductive
(3), can result
from
either
ecological
or
otic drive
isolation between populations, as
speciation.
such as disease, competition, and behavioral in- distinct
mutation-order
sterility (F
from geographical
barriers to interbreedSpeciation can
be rapid
terference. Ecological speciation can lead to the ing). Subsequently,
mutationspecies
were under
definedboth
as
cause, by c
of interbreeding
populations
alleles that
are
evolution of any type of reproductive isolation, groups
speciation
models,natural
because
tions cau
reproductively
isolated
from other
such
to fixation
by natural
selection
including premating isolation, hybrid sterility, are driven
countering
groups
(7).
From
this
point
on,
the
study
of
and intrinsic hybrid inviability as well as extrin- in both cases. However, under the muthe same i
speciation was the study of the evolution of
sic, ecologically based pre- and postzygotic iso- reproductive
tation-order
process,
the
same
alleles,
Speciation
isolation (3). Progress up to then in
if present,the
would
be favored
in every
lation. Speciation by sexual selection is ecologi- understanding
mutation-o
link between
morphological
thelargely
early forgotten,
stages of
population,
at least in
cal speciation if ecologically based divergent se- speciation
vergence
and adaptation
was
gamete re
under
the new
concept.
lection drives divergence of mating preferences, its contributions
divergence.uncertain
For this
reason,
mutationFig. 1. (A) Example of ecological speciation. Repeatedly and
fixation o
The
species
concept when
must surely
1.
(A)
Example
of
ecological
speciation.
Repeatedly
and
speciation
is difficult
there Fig.
for example by sensory drive (15).
orderbiological
independently, the mosquito fish, Gambusia hubbsi, inhabiting
more because
difficult togene
investigate
any link independently,
mosquito
fish, Gambusia
hubbsi,
inhabitIn accordance with (10), mutation-order spe- haveismade
flow increasgeneitflow,
blue holes in the the
Bahamas
has evolved
a larger caudal
region
and geous mu
between speciation and natural selection. T. ing
bluehead
holesin inthethepresence
Bahamas
evolved
a larger
of has
predators
(top)
than incaudal
their ulations,
ciation is defined as the evolution of reproduc- Dobzhansky
es the possibility
that favorable muta- smaller
(16). Div
(13) suggested that the genes under- region
and
smaller
head
in the presence
ofprobability
predatorsof(top)
absence
(bottom)
(29).
In
laboratory
trials,
the
in one
population
will than in their absence (bottom) (29). In laboratory trials, two
tive isolation by the fixation of different advan- lyingtions
occurring
differences
between
populations
in ordinary
the other learn
individuals mating was higher when they were from different
tageous mutations in separate populations ex- phenotypic
spread traits
to other
werepopulations,
unlikely to be preventing
the basis of probability
of twothe
individuals
matingenvironment
was higher (and
whensimilar
they havior und
populations having
same predation
isolation.
He later
hisresultmind, were
divergence
(17, 18).
Anychanged
process
periencing similar selection pressures. Whereas reproductive
from different
populations
the same
preda- tion, not m
body shape)
than when
they were having
from opposite
predation
at the
viewpoint,
theincluding
generally tion
environment
similar
shape)(29)].
than (B)
when
they efficient s
environments.
[Photo(and
credit:
Brianbody
Langerhans
Example
flow,
different alleles are favored between populations but ing
in time
low this
levels
of geneand
from opposite
predation
environments.
[Photo credit: is the cul
difficultyfacilitates
of studyingsubsequent
reproductivediverisola- were
of reproductive
isolation
evolving
under the mutation-order
under ecological speciation, the same alleles greater
selection,
Langerhans
(29)]. (left)
(B) Example
of reproductive
isolation
tion than morphology, must have discouraged Brian
mechanism.
Male-fertile
and male-sterile
(right) flowers
of mutation-o
would be favored in different populations under gence by the mutation-order process evolving
thean
mutation-order
mechanism.
between
Oregon population
of monkeyMale-fertile
flowers (M. al scenario
many from pursuing the connection. Virtually no F2 hybridsunder
speciation
mutation-order speciation. Divergence occurs research
(19).effort
In contrast,
andhaving
male-sterile
(right)male
flowers
of F2
hybrids
guttatus)
a cytoplasmic
sterility
element
andbetween
nuclear
Both
followed ecological
that tested the
role of (left)
anyway because, by chance, the populations do adaptation
can proceed
with or without gene flow, an
restorer
and population
a closely related
species flowers
(M. nasutus)
having neither
Oregon
of monkey
(M. guttatus)
hav- ecologica
in speciation.
(46,a47).
Both flowers
have
M. guttatus
cytoplasm.
The are theore
cytoplasmic
maleshown
sterility
element
and nuclear
restorer
not acquire the same mutations or fix them in the although it is easiest when gene flow ing
flower
on the left
also has
the nuclear
restorer,having
whereasneither
the one(46,
on only data
of Speciation by Selection
and
a closely
related
species
(M. nasutus)
same order. Divergence is therefore stochastic Models
is absent.
the right,
undeveloped
anthers,
lacks the cytoplasm.
restorer. [Photo
47).
Both with
flowers
shown have
M. guttatus
The ative imp
The
topic
of
natural
selection
in
speciation
is
once
Experiments with laboratory popu- credit: Andrea
but the process is distinct from genetic drift. It
on theCase
left (47)]
also has the nuclear restorer, whereas the key is to
again receiving attention. The two most general flower
can occur in both small and large (though not lations of Drosophila and yeast dem- one on the right, with undeveloped anthers, lacks the restormechanism
hypotheses involving selection are ecological and
infinite) populations. Selection can be ecologi- mutation-order
onstrate the
plausibility
of ecological
[Photoincluding
credit: Andrea
Case isolation,
(47)]
isolation,
premating
hybrid first evolved (3). Once the
speciation.
Ecological
speciation er.
cally based under mutation-order speciation, but is defined
speciation.
In thoseofinstances
as the evolution
reproductivewhen
iso- sterility, and intrinsic hybrid inviability as well as ences have accumulated b
between populations
divergent natural
ecology does not favor divergence as such. It lation
measurable
pre- andby postmating
re- extrinsic, ecologically based pre- and postzygotic either process, subsequen
isolation.
Speciation
by sexual
is favored
arising isolation
from differences
between
JYAlpha),
and selection
sexual isolation
(ds2)inbe-one populatio
evolved,
it wasecogreater
be- (Odsh,
can lead to the evolution of any type of repro- selection
productive
speciation
if ecologically
basedMost
diver- of because
of epistatic inte
environments
(2, 8, 9, to
14).different
It predictsenvironments
that ecological tween
Drosophila
species.
these genes
ductive isolation, with the exception of ecologi- logical
tween
lines subjected
reproductive isolation should evolve between gent selection drives divergence of mating background (10). Hence, e
than between lines raised under homogeneous show molecular signatures of positive selection,
cally based pre- and postzygotic isolation.
producing Dobzhansky-M
populations adapting to contrasting environments preferences, for example by sensory drive (15).
Speciation resulting from intragenomic con- but conditions
21). adapting
Laboratory
experiments
provingwith
natural
rolespe(3), provided
In accordance
(10), selections
mutation-order
in hybridsthat
between specie
not between (20,
populations
to similar
under
flict such as meiotic drive or cytoplasmic male environments.
on various
maintained
fixation
occurred
before
complete reproductive
ciation is defined
as the
evolution
of reproductive
either ecological or mutati
Themicrobes
basic idea has
been around
for homoisolation
rather
afterward.
sterility (Fig. 1B) is likely to be mutation-order a while
geneous
conditions
many
have by
the fixation
of than
different
advanta- The top-down
Speciation can be rapid
(7), although
it wasfor
tested
onlygenerations
recently. isolation
geous
in separate
expebecause alleles ar
agents of divergent
selection are extrinsic
and with
genetic divergence
consistent
the mutations
identifying
(i) themodels,
phenotypic
speciation because, by chance, the initial muta- Thedetected
approach
involvespopulations
riencing
selection
pressures.
Whereas(ii) natural
include abiotic andprocess
biotic factors
food on
(22),such
butaseffects
re- similar
those selection
traits in both
traits under
divergent
selection,
tions causing drive and those countering it are can mutation-order
resources, climate, habitat, and interspecies inter- different alleles are favored between populations the mutation-order proces
unlikely to be the same in separate populations. productive isolation have not been explored.
associated with reproductive isolation, and (iii)
actions such as disease, competition, and behav- under ecological speciation, the same alleles present, would be favored
Two approaches
investigate
Speciation by sexual selection is mutation-order ioral interference.
the genes
underlying
traits and
reproductive
isoin different
populations
under
least in the
early stages o
Ecological
speciation the
can mechanisms
lead would be favored
in nature.mutation-order
The lation.
Step (iii)
has beenoccurs
challenging
undermutation-order
both
speciation if divergence of mate preferences or to the
of speciation
natural
speciation.
Divergence
any- reason,
spe
evolution ofbyany
type selection
of reproductive
gamete recognition occurs by the fixation of bottom-up approach involves (i) genetic map- approaches but is needed to understand how sealternative advantageous mutations in different ping of reproductive isolation between closely lection has led to reproductive isolation.
6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
738
populations, as by sexual conflict (16). Diver- related species, (ii) testing whether discovered
gence in song and other learned components genes exhibit a genomic signature of positive Ecological Speciation
of behavior under purely social selection, not selection, and (iii) identifying the phenotype Evidence for ecological speciation has accumumolded by selection for efficient signal trans- and source of fitness effects of alternative alleles lated from top-down studies of adaptation and
mission (5), is the cultural equivalent of the at selected loci. The approach has been hugely reproductive isolation [reviewed in (2, 8, 9)].
mutation-order process. Additional scenarios successful in identifying major genes implicated We now know of many real species that have,
in hybrid inviability (Hmr, Lhr, Nup96), sterility at least in part, evolved by divergent natural seare elaborated in (5).

27

Number of studies

y to mate if they are of nents of reproductive isolation lacking identifiable

less of relatedness as causes (Fig. 2). The unidentified component of
speciation, if built by selection and not genetic
affinity.
is also
prematComponents divergent selection
plants (28), Littorina marine snail ecotypes
n which
rentially
inhabiting different zones of the intertidal
15
basis of
(24), and mosquito fish inhabiting blue
e under
10
holes with and without fish predators in the
nt selecBahamas (29) (Fig. 1A). In these studies, it
ortative
5
was shown that males and females are more
insects,
likely to mate if they are of the same ecoin fish,
0
or preftype, regardless of relatedness as indicated
notypic
by phylogenetic affinity.
Components unknown cause
flowerEcological speciation is also supported
15
be under
by
examples of premating reproductive
environ10
isolation in which individuals choose or
30, 31)].
preferentially encounter mates on the basis
vergent
5
directly
of phenotypic traits that are under ecologiuced fitcally based divergent selection. Examples
0
he enviinclude assortative mating by host choice
-0.6 -0.4 -0.2
0
0.2 0.4 0.6 0.8
1
migrant
in
insects, body size and coloration in fish,
31, 32)]
Cumulative reproductive isolation
beak size in birds, pollinator preferences for
ybrids in
of of
the the
magnitude
of reproductive
isolation
Fig. 2.2. Estimates
Estimates
magnitude
of reproductive
[extrin- Fig.
specific phenotypic floral traits, and variaresulting
from
divergent
selection
components
(top),
compared
isolation
resulting
from
divergent
selection
components
3)]. For
tion
in flowering timetraits inferred to be
with
othercompared
componentswith
lacking
identifiable
causes (bottom).
(top),
other
components
lacking
l perenDivergent
selection
components
includeDivergent
those attributable
to under divergent selection between environidentifiable
causes
(bottom).
selection
s of the active selection on traits (immigrant inviability and extrinsic
components include those attributable to active ments [see examples in (8, 30, 31)].
uttatus) postzygotic
and(immigrant
to trait-basedinviability
assortative and
mating
(habitat
selectionisolation)
on traits
extrinsic
Ecologically based divergent selection
North preference,
floralisolation)
isolation, and
breeding
time). The assortative
unattributed
postzygotic
and
to
trait-based
s when components include intrinsic hybrid inviability, sexual selection has also been directly measured, as shown
mating (habitat preference, floral isolation, and breeding
of the against
by reduced fitness of each ecotype in the enpollen competition,
and reduced
hybrid fecundity.
time).hybrids,
The unattributed
components
include
intrinsic
mple of Data
were taken from (32, 31) (table S1). A negative value vironment of the other [immigrant inviabilhybrid inviability, sexual selection against hybrids, pollen
ypic dif- indicates
that hybrids had higher fitness than the parental species
competition, and reduced hybrid fecundity. Data were ity; reviewed in (31, 32)] and by reduced fitutes di- for
at least one component of postzygotic isolation. One data value
taken
from
(32, 31) (table S1). A negative value indicates ness of hybrids in the parental environments
because of 2.66 was left out of the bottom panel.
that hybrids had higher fitness than the parental species [extrinsic postzygotic isolation (33)]. For
for at least one component of postzygotic isolation. One example, each of the coastal perennial and
value of 2.66
was left out of the bottom panel.
739
VOL 323 data
6 FEBRUARY
2009

lection between environments. The connections

between selection on ordinary phenotypic traits
and reproductive isolation are often strong and
straightforward. It follows that much of the genetic basis of reproductive isolation should involve ordinary genes that underlie differences in
phenotypic traits. But we still know little about
the genetics of ecological speciation.
One line of evidence comes from tests of
parallel speciation, whereby greater reproductive isolation repeatedly evolves between independent populations adapting to contrasting
environments than between independent populations adapting to similar environments (20,
23). A major challenge in applying the test to
natural populations is to eliminate the possibility that each ecotype has originated just once and
has spread to multiple locales. This is difficult
because gene flow of neutral markers between
closely related but nearby populations can result
in the false appearance of multiple independent
origins of these populations when evaluated by
phylogenies (3, 24). However, multiple origins
are supported in several examples of parallel
speciation, including the sympatric benthiclimnetic species pairs of threespine stickleback
in young lakes of British Columbia (25, 26), the
repeated origin of divergent marine and stream
populations of threespine stickleback around the
Northern Hemisphere (27), ecotypes of Timema
walking stick insects living on different host

28

inland annual races of the monkey flower

(Mimulus guttatus) along the west coast of
North America has low fitness when transplanted to the habitat of the other (31). This is an example of active selection on phenotypic differences, and it also constitutes direct reproductive
isolation because it is an evolved barrier to gene
flow between parental populations. Multiple
traits are probably involved, including flowering
time and tolerance of salt and drought. This type
of reproductive isolation is context-dependent
and is weakened in intermediate environments.
On the other hand, active selection favors the
evolution of ever-greater differences between
populations, which may strengthen the barrier
to gene flow (20).
It is unclear how much reproductive isolation typically evolves by ecologically based
divergent selection in nature. We can approximate an answer from estimates of the combined
contribution of active selection on traits and
trait-based assortative mating, as compared with
other forms of reproductive isolation (Fig. 2
and table S1). These estimates are incomplete
because individual studies may lack data on
components of reproductive isolation, separate
components may not be independent, and the
strength of barriers between species may not be
symmetric (34). Nevertheless, compilation of
the data shows that the amount of reproductive
isolation attributable to active selection and traitbased assortative mating is at least as strong,
on average, as the amount from components

of reproductive isolation lacking identifiable

causes (Fig. 2). The unidentified component of
speciation, if built by selection and not genetic
drift, could be the result of either ecological or
mutation-order mechanisms.
These examples indicate a growing knowledge of the mechanisms of selection and its
consequences for reproductive isolation. At
this point, the most glaring deficiency is our
knowledge of the impact of selection on genes.
Optimistically, progress is being made with genetic mapping to identify quantitative trait loci
(QTLs) and genes or regulatory control regions
that affect individual phenotypic traits on which
components of reproductive isolation depend.
Examples include the yup QTL, which affects
flower color differences between the monkey
flowers, Mimulus cardinalis and M. lewisii (35).
Swapping alleles of this QTL between the species with repeated backcrossing resulted in shifts
in pollinator preference and, hence, indirectly
affected premating isolation. Survival and salt
tolerance of second-generation hybrids between
the sunflowers Helianthus annuus and H. petiolaris transplanted to the salt marsh habitat of
their hybrid descendent species (H. paradoxus)
mapped strongly to a QTL identified as the salt
tolerance gene CDPK3 (36).
Another form of investigation involves the
analysis of genome scans of ecologically different populations and species. These scans compare allelic variation within and between populations at many marker loci spaced throughout
the genome (37). Markers that show excessive
differentiation between populations (outliers)
may indicate selection on nearby genes. The
method is particularly informative when applied
to populations with ongoing hybridization, because outlier markers may identify points in the
genome that resist the homogenizing influence
of gene flow, perhaps indicating genomic regions under divergent selection. However, sets
of genes that diverged under a mutation-order
process can produce the same pattern (17, 18),
which makes analysis of such studies more difficult. Clues to whether ecologically based divergent selection is involved are gained if outliers
at the same genomic locations turn up repeatedly in scans between populations that inhabit
contrasting environments (38) and by identifying phenotypic traits under divergent selection
that map to those locations in the genome (36,
39, 40). As genomic resources increase for more
species, it will be possible to measure natural
selection directly on genomic regions of interest by transplanting otherwise relatively homogenous experimental populations containing
alternative alleles into the environments of the
parent species (35).

Mutation-Order Speciation
Mounting evidence for divergent selection in
speciation does not diminish the potential role

of mutation-order divergence. It may be that the

mutation-order process is more difficult to detect, or perhaps we have not looked hard enough
at species with only small ecological differences
(5). We still do not know much about the selective factors causing mutation-order speciation.
Evidence for mutation-order speciation
comes from instances in which reproductive
isolation apparently evolved as a by-product
of conflict resolution between genetic elements
within individuals (intragenomic conflict), such
as cytoplasmic male sterility in hermaphroditic
plants (Fig. 1B), and genetic elements conferring meiotic drive. Under both mechanisms, a
mutation arises that can distort representation in
gametes and spreads in a selfish manner, even
though such an element reduces overall fitness of the organism that bears it. This, in turn,
places selection on mutations in other genes that
counter the selfish elements effects and restore
more equal genetic representation in gametes.
Distorter and restorer mutations are unlikely to
be the same in different populations regardless
of environment; thus the process leads to divergence. The mismatch between the distorter in
one population and the restorer in the other can
result in hybrid sterility or inviability and, thus,
reproductive isolation (3, 41). Numerous examples of selfish elements, such as those observed
in cytoplasmic male sterility of plants, support
these hypotheses (42, 43). In addition, partial reproductive isolation generated by meiotic drive
has been identified in Drosophila [reviewed
in (3, 41)]. Sexual conflict is also expected to
lead to mutation-order speciation, but there are
few compelling examples (3). The contribution by these mechanisms to speciation is still
uncertain, however. The alleles responsible for
meiotic drive and cytoplasmic male sterility
may be prevented from spreading to fixation because selection on such elements is frequencydependent (43) and because restorer alleles arise
and weaken selection on the distorter elements
(44). Second, if divergent populations come
into secondary contact, the alleles within each
population causing cytoplasmic male sterility
or meiotic drive (and the corresponding restorer
alleles) will spread between the populations by
gene flow, eliminating that component of reproductive isolation (43). Hence, for these mechanisms to contribute to speciation, the fitness of
hybrids must be reduced to very low levels, or
other incompatibilities must arise that interact
with these genes to prevent their spread after
secondary contact.

Conclusions
Our understanding of the role of natural selection in speciation has come a long way since
Darwins time. If he were here to witness, he
would most likely be staggered by the discoveries of genes and molecular evolution and astonished at the prospect that evolutionary conflict

between genes could generate reproductive isolation (45). Mostly, I expect that he would be
chuffed by mounting evidence for the role of
natural selection on phenotypic traits in the origin of species. This is really what On the Origin
of Species was all about. Between 1859 and the
present, the general acceptance of the biological species concept altered the focus of speciation studies. Yet, the discovery that reproductive
isolation can be brought about by ecological
adaptation in ordinary phenotypic traits bridges
Darwins science of speciation and our own.
The most obvious shortcoming of our current understanding of speciation is that the
threads connecting genes and selection are still
few. We have many cases of ecological selection generating reproductive isolation with little
knowledge of the genetic changes that allow
it. We have strong signatures of positive selection at genes for reproductive isolation without
enough knowledge of the mechanisms of selection behind them. But we hardly have time
to complain. So many new model systems for
speciation are being developed that the filling of
major gaps is imminent. By the time we reach
the bicentennial of the greatest book ever written, I expect that we will have that much more
to celebrate.
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S. Via, M. Whitlock, J. Willis, and a reviewer
for assistance and comments. This work was
supported by grants from the Natural Sciences
and Engineering Research Council of Canada
and the Canada Foundation for Innovation.

Supporting Online Material

www.sciencemag.org/content/full/323/5915/737/
DC1
Tables S1 to S3
References
10.1126/science.1160006

29

The Bacterial Species Challenge:

Making Sense of Genetic and
Ecological Diversity

T
T

30

www.sciencemag.org

SCIENCE

VOL 323

6 FEBRUARY 2009

741

lg
in
o

lyt
icu
s

V. ordalii

oi
en

si
s

S. pseudopneumoniae
S. pneumoniae
3% divergent
1.2% divergent

um

V.
r

The Bacterial Species Challenge:

Making Sense of Genetic and
Ecological Diversity

Speciation

V.
a

values that place two bacterial isolates into the

same or different species. The overall genetic
SPECIALSECTION
relatedness
mayhuman
be measured
by the
pneumoniaeof isisolates
a major
pathogen,
S.
extent
of
DNA
hybridization
between
them,
and
mitis is a commensal bacteria with a history
S. Rogers,
A. Schluter,
Via,more
M. Whitlock,
J. Willis,
and
40. S. Via, J. West, Mol. Ecol. 17, 4334 (2008).
32. P. Nosil, T. H. Vines, D. J. Funk, Evolution 59, 705 (2005).
those
that show
70%S. or
DNA
hybridpseudoof taxonomic
and
S. work
a reviewer foruncertainty
assistance and (11),
comments.
This
41. H. A. Orr, J. P. Masly, N. Phadnis, J. Hered. 98, 103
33. H. D. Rundle, M. C. Whitlock, Evolution 55, 198 (2001).
ization
are
defined
as
the
same
species
(2,
10).
pneumoniae
is abyrecently
described
of
was supported
grants from
the Naturalorganism
Sciences and
(2007).
34. N. H. Martin, J. H. Willis, Evolution 61, 68 (2007).
Such
cutoffs
imply
that
sequences
thatthecluster
Engineering
Research
Council
of Canada
and
Canada
42. D. A. Levin, Syst. Bot. 28, 5 (2003).
35. H. D. Bradshaw, D. W. Schemske, Nature 426, 176 (2003).
status
that nonetheless
corresponds
to
uncertain
Foundation
foraInnovation.
43. L. H. Rieseberg, J. H. Willis, Science 317, 910 (2007).
36. C. Lexer, Z. Lai, L. H. Rieseberg, New Phytol. 161, 225
together
with
certain
of There
similarity
data (12).
are
a distinct
cluster
in theseamount
44. D. C. Presgraves, Trends Genet. 24, 336 (2008).
(2004).
must
be differences
from
the Material
same
species,
and
Supporting
Online
of moreover
sequence
striking
in the
amount
45. D. C. Presgraves, Curr. Biol. 17, R125 (2007).
37. M. A. Beaumont, Trends Ecol. Evol. 20, 435 (2005).
that
this
cutoff
value
is
applicable
to
all groups
www.sciencemag.org/cgi/content/full/323/5915/737/DC1
diversity observed within homologous
house46.2L. Fishman, J. H. Willis,1 Evolution 60, 1372 (2006).
38. P. Nosil, D. J. Funk,1D. Ortiz-Barrientos,
Mol. Ecol. 18,
2,3,4
1
Tables
S1 to S3or archaea. Recent MLSA studies,
of
bacteria
Christophe
Fraser, * Eric J. Alm,
Martin F. Polz,
William
Hanage
47. A.Brian
L. Case,G.J. Spratt,
H. Willis, Evolution
62,P.
1026
(2008).
375 (2009).
keeping
References genes in these named species, ranging
which
use the concatenated sequences of mul48. We thank M. Arnegard, R. Barrett, A. Case, H. Hoekstra,
39. S. M. Rogers, L. Bernatchez, Mol. Biol. Evol. 24, 1423
from
1.2% for S. pneumoniae to 3.0% for S.
10.1126/science.1160006
M. Noor,
P. Nosil, S. Otto, of
T. Price,
Rieseberg,
housekeeping genes to discern clustering
The (2007).
Bacteria and Archaea are the most genetically diverse
superkingdoms
life, L.and
techniques tiple
pseudopneumoniae and up to 5.0% for S. mitis.
patterns among populations of closely related
for exploring that diversity are only just becoming widespread. Taxonomists classify these
The distance between two randomly selected
organisms into species in much the same way as they classify eukaryotes, but differences in their taxa, suggest that species defined by taxonois similar
to the
average
S.
mitisthat
genotypes
values
place
two
bacterial
isolates
into disthe
mists
in many
cases
correspond
to well-resolved
biologyincluding
horizontal gene transfer between distantly related taxa and variable rates of
REVIEW
S.
pseudotance
between
S.
pneumoniae
and
same or different
overall
genetic
clusters. species.
However,The
these
studies
also
homologous recombinationmean that we still do not understand what a bacterial species is. This sequence
pneumoniae
(5.1%)
(2). This implies
relatedness
ofgenotypes
isolates
may
be cutoff
measured
by the
show
that there
is no universal
or descripis not merely a semantic question; evolutionary theory should be able to explain why species
theclusters
of that
ahybridization
fixed
level of
sequence
diverthat
extent
ofuse
DNA
between
them,
and
tor
of
characterizes
a species.
Furexist at all levels of the tree of life, and we need to be able to define species for practical
species
would
gence
for
differentiating
those
that
show
70%
or
more
DNA
hybridthermore, inspection of the clusters does tend
not
applications in industry, agriculture, and medicine. Recent studies have emphasized the need to
to
either
S. pneumoniae
and
pseudoization
arerejoin
defined
aswhich
the same
(2, 10).
always
clearly
reveal
level species
in theS.hierarchy
combine genetic diversity and distinct ecology in an attempt to define species in a coherent and
or
breakthan
up sequences
S. mitis
that 1)
nearly
pneumoniae,
Such
imply
that
that
cluster
is
morecutoffs
fundamental
any
otherso(Fig.
(7).
convincing fashion. The resulting data may help to discriminate among the many theories of
of
its
own.
This
is
every
isolate
was
a
species
together
with
a
certain
amount
of
similarity
As an example, Fig. 1A shows the relationprokaryotic species that have been produced to date.
clearly
unsatisfactory.
must be
frommultiple
the sameisolates
species,of and
ships
among
threemoreover
closely
that this streptococcal
cutoff value is species.
applicableStreptococcus
to all groups
he species debate in microbiology is not reflect only a tiny subset of those characters that related
1
2
traordinary
variety
of 1different
microbial
life,
muchin1ofthe
it pneumoniae
he species
isbacnotF. Polz,
Habitats
Differentiation
of bacteriaand
or
archaea.
Recent
MLSA S.
studies,
Christophe
Fraser,
* Ericindesire
J.microbiology
Alm,to2,3,4
Martin
Brian
G.
Spratt,
Williamresources
P. Hanage
is aEcological
major human
pathogen,
mitis
allow
bacteria
to use
only
about
adebate
human
catalog
desiremanner,
to catalog
Beyond
this, taxa
too fraction
similar of
to is
A
natural
criterion
to identify
clusters
of
uncultured (1).
only diversity
about a inhuman
which
use
the concatenated
sequences
of taxomulaclear
commensal
bacteria with
a history
of
and
only capture
a small
terial
a consistent
but environment,
rRNA
se- nomic
importance,
we might
want
in
consistent
manbe
distinguished
and
evolutionary
tiple housekeeping
genes
topseudopneumoniae
discern
clustering
The
Bacteria
anddiversity
Archaea
areabecause
the
mostofgenetically
diverse
superkingdoms
life, andbytechniques
uncertainty
(11),
andwhich
S.
true diversity
in circumscribed
this ofsuperkingdom
of life.
is
also
abacterial
fundamental
argument
what
it the
patterns
among
of uncertain
closely
related
butabout
is alsoour
a fundamental
argument
ecological
features
that
quences
have Taxonomists
revealed
further
diversity
through is
to
species,
is populations
to find
ner,
for exploring
that
diversity of
are
onlyevolutionary
justbecause
becomingMore
widespread.
classify
these
acall
recently
described
organism
status
recently,
molecular
methods
[particularly
reveals
ignorance
how
taxa,nonetheless
suggestthem
that
species
defined
bycluster
taxonoabout
our
ignorance
of way
how
analysis
(MLSA)
and that
Among
of
whatform,
it into
reveals
distinguish
from
close
multilocus
organisms
species
much
thebacterial
same
classifysequence
eukaryotes,
butand
differences
inRNA
their
corresponds
to
arelatives.
distinct
in
DNA-DNA
hybridization
ribosomal(2)
forces
shape,
and in
extinguish
ge-as they
mists data
in many
correspond
biologyincluding
horizontal
gene
between
distantly
related
taxa(1),
andand
variable
of
andoftransfer
extinguish
diversity
evolutionary
forces
form,
shape,
metagenomic
studies
pathogens,
thecases
ability
causeto differences
awell-resolved
distinctive
these
(12).
There
aretostriking
in
(rRNA)
sequencing]
have
helped
to this
definerates
species,
netic
lineages,
of the
mechanisms
differensequence
clusters.
However,
studies
also
homologous
recombinationmean
thatcommon
we still
not these
understand
what
a by
bacterial
species
This
of dobut
has
beenthese
used
to within
define
bacterial
genetic
lineages, of thesharing
mechanisms
needs
to be
explained
theory.limitations
Thus, is.
practidisease
amount
ofhistorically
sequence
diversity
observed
methods
have
serious
and the
tiation
between
subpopulations
show thatbut
there
is no universal
ora descripis not merely
semantic
question;
evolutionary
should
beassign
able of
to
explain
whyobservations
species
lack
and
constitute
minute
differentiation
subpopulations
sharing
species,
pathogens
cal difficulties,
housekeeping
genescutoff
inonly
these
named
cannot
reliably
a theory,
large
collection
of similar homologous
descent,
and ofabetween
the
process
of adaptation
to new theory
tor
of
clusters
that
characterizes
a
species.
Furexist
at
all
levels
of
the
tree
of
life,
and
we
need
to
be
able
to
define
species
for
practical
species,
ranging
from
1.2%
for
S.
pneumoniae
to
andenvironments.
of the process
of adaptaas yet
unclassified
microbial
of
of vast to
amounts
common
speciesof(e.g.,
rRNA
sequences
are too fraction of overall bacterial diversity. Mapping
niches
anddescent,
changing
Animal
spe- strains
thermore,
inspection
the clusters
does
applications
in industry,
agriculture,
andand
medicine.
Recent studies
emphasized
therRNA
need
to
for S.
pseudopneumoniae
and up toresources
5.0% not
for
to resolve
similar
species).
se- 3.0%
cies
are
defined
by and
theirchanging
morphological
be- conserved
environments.
of how
tion
to new
niches
diversity
have
allhave
fueled
the controversy
bacterial
diversity
ontoofenvironmental
always
reveal which
level
in randomly
theofhierarchy
combine traits
genetic
diversity
ecology
to
define
species
a coherent
and S.
mitis.clearly
The
between
two
sequence
surveys
have, however,
the extrahavioral
andare
by defined
their and
ability
or inability
to in an
indicates
thatdistance
closely
related
groups
bacteria
Animal
species
bydistinct
their
morphooneattempt
defines
a bacterial
speciesinrevealed
(38).
is
more
fundamental
than
any
other
(Fig.
1)fine(7).
convincing
fashion.
The
resulting
data
may
help
to
discriminate
among
the
many
theories
of
lected
S.
mitis
genotypes
is
similar
to
the average
ordinary
variety
of
microbial
life,
much
of
it
interbreed,
but
such
categories
cannot
easily
be
can be ecologically divergent. For example,
logical and behavioral traits and by their abilAsresource
anbetween
example,
1A has
shows
relationprokaryotic
species
thatorhave
been
produced
to date.
S. Fig.
pneumoniae
andthe
S.observed
pseudouncultured
(1). Beyond this, taxa too similar to be distance
applied
to the
Bacteria
Archaea
(or
indeed to
Genetic Clustering
but
such
categories
been
ity
or inability
to interbreed,
scale
partitioning
ships among
multiple
of three
closely
genotypes
(5.1%)
(2).
This
implies
and circumscribed
rRNA se- pneumoniae
many
taxonomists
or Ar- distinguished
Darwin commented
that all trueby
classification
cannoteukaryotic
easily be microbes).
applied toInstead,
the Bacteria
among
coastal
Vibrio isolates
populations
coexisting
related
streptococcal
species.
Streptococcus
reflect
only
a
tiny
subset
of
those
characters
that
he
species
debate
in
microbiology
is
not
that
the
use
of
a
fixed
level
of
sequence
divergence
quences
have
revealed
further
diversity
through
have
been
forced
to
rely
on
biochemical
tests
and
chaea (or indeed to many eukaryotic microbes). is genealogical [(9), p. 404]. Taxonomists have in the water column (13). Partitioning was
pneumoniae
is a major
human
pathogen,
mitis
allowused
bacteria
to userelatedness
different(MLSA)
resources
in and
the for
about a human
desire
to catalog
bacdifferentiating
species
would
tend toS.either
sequence
analysis
limited
morphological
characteristics
for this
taxonomists
have
been forced
to purrely multilocus
to define(2)cutoff
were
collected
from
thus
sequence
discovered
because
strains
Instead,only
is
a
commensal
bacteria
with
a
history
of
taxoenvironment,
and
only
capture
a
small
fraction
of
terial
diversity
in
a
consistent
manner,
but
rejoin
S.
pneumoniae
and
S.
pseudopneumoniae,
metagenomic
studies
(1),
and
this
diversity
needs
pose.
Naturally,
biochemical
characters
have
been
on biochemical tests and limited morphological values that place two bacterial isolates into the distinct, ecologically informative samples, and
nomic
uncertainty
andnearly
S.ofpseudopneumoniae
thebetrue
diversity
this superkingdom
of life.
is also a fundamental
argument
of what
it to
break
up S. mitis(11),
so that
every
isolate was
explained
theory.
Thus,overall
practical
dif- or
selected
for the convenience
of because
taxonomists;
they
biocharacteristics
for this
purpose.
Naturally,
same
or
differentbyin
species.
The
genetic
the
phylogenetic
structure
the
ecologically
isspecies
a recently
described
organism
of uncertain
status
molecular
[particularly
reveals about our ignorance of how evolutionary More recently,
of its
own.
This
is clearly
unsatisfactory.
lack
theory,may
andmethods
observations
ofofisolates
be
measured of
byvast
the adifferentiated
populations
was superimposed
chemical characters have been selected for the ficulties,
relatedness
that
nonetheless
corresponds
to
a
distinct
cluster
in
1forces form, shape, and extinguish bacterial geDNA-DNA
hybridization
and
ribosomal
RNA
amounts
of
as
yet
unclassified
microbial
diversity
Department of of
Infectious
Disease Epidemiology,
taxonomists;
they
reflect Imperial
only a extent of DNA hybridization between them, and on their habitats. Habitats were defined using
convenience
2
Habitats
these dataand
(12).Ecological
There are Differentiation
striking differences in
(rRNA)
sequencing]
have helped to
define
species,
netic lineages,
of the
mechanisms
of differenCollege
London,
London
W2
1PG,
UK.
Department
of
Civil
have
all
fueled
the
controversy
of
how
one
detiny subset of those characters that allow bac- those that show 70% or more DNA hybridiza- an empirical modeling approach. This analysis
and
Environmental
Engineering, Massachusetts
Institute
of
theclear
amount
of sequence
diversity
observed
within
but these
methods
have(38).
serious limitations and A
tiation
between subpopulations
sharing
common
natural
criterion
to identify
clusters
of
fines
a bacterial
species
defined as
the same
species (2, 10). Such revealed
high levels
of specialization
for some
teria to use
differentMAresources
in 3the
environtion are
Department
of
Technology,
Cambridge,
02139,
USA.
homologous housekeeping
genes we
in these
named
cannot reliably assign a large collection of similar evolutionary
descent, and
of the process
of adaptation
to new
importance,
which
might
want
only capture
a smallInstitute
fraction
of the cutoffs imply that sequences that cluster together populations (e.g., V. ordalii is only found as
ment, and
Biological
Engineering,
Massachusetts
of TechnolGenetic
species,
rangingisfrom
1.2%
for S. pneumoniae
to
strains toClustering
species (e.g., rRNA sequences are too to
niches and changing
environments.
Animalofspecall species,
to find
ecological
features that
MIT
ogy,
MAthis
02139,
USA. 4Broad Institute
superkingdom
of life. More
true Cambridge,
diversity in
with a certain amount of similarity must be from single free-swimming cells), whereas others are
3.0% for S. pseudopneumoniae
and up to 5.0%
for
conserved
to resolve that
similar
rRNA se- distinguish
ciesHarvard
are defined
by their
morphological
and be- Darwin
them from close relatives.
Among
commented
allspecies).
true classification
and
University,
Cambridge,
MA 02139, USA.
DNAa wide
recently,
molecular
methods
[particularly
the
same
species,
and moreover
that this
more
generalist
(Fig. 1B) and can
colonize
S. mitis.
The
randomly
sequence
surveys
have,
revealed
thecutoff
extrahavioral
traits
and by
their
ability
or inability
to is
thedistance
ability between
to cause two
a distinctive
disgenealogical
[(9), however,
p. 404]. Taxonomists
have pathogens,
*To
whom
correspondence
should
be addressed.
E-mail:
DNA
hybridization
ribosomal
RNAeasily
(rRNA)
value
is applicable
tomicrobial
all groups
of much
bacteria
or
variety
ofmitis
surfaces,
including
organic
particles
lected
S.
genotypes
is
similar
to
the
average
ordinary
variety
of
life,
of
it
interbreed,
but suchand
categories
cannot
be thus
c.fraser@imperial.ac.uk
used sequence relatedness to define cutoff ease has historically been used to define species,
helped
define (or
species,
Recent
MLSAthis,
studies,
which
usetothe
zooplankton
water column
Most
sequencing]
distance
between inS.the
pneumoniae
and (13).
S. pseudouncultured
(1). Beyond
taxa too
similar
be and
applied to thehave
Bacteria
or to
Archaea
indeedbut
to archaea.
and can- concatenated
of multiple
Vibrio (5.1%)
populations
are implies
deeply
these
have
serious Instead,
limitations
the predicted
pneumoniae
genotypes
(2). This
distinguished sequences
and circumscribed
byhousekeeprRNA se- of
many methods
eukaryotic
microbes).
taxonomists
among
cases 741
not
assign
large
collection www.sciencemag.org
oftests
similar
geneshave
to SCIENCE
discern
patterns
divergent
eachlevel
other,
and in many
VOLdiversity
323 6through
FEBRUARY
2009
that the
usefrom
of a fixed
of sequence
divergence
quences
revealedclustering
further
havereliably
been forced
to arely
on biochemical
and ing
to
species
(e.g.,
rRNA
sequences
are
too
populations
of
closely
related
taxa,
suggest
that
are
congruent
with
named
species;
however,
V.
strains
limited morphological characteristics for this pur- multilocus sequence analysis (MLSA) (2) and for differentiating species would tend to either
similarcharacters
species). have
rRNAbeen
se- species
defined
by taxonomists
many needs
cases splendidus
is a notableand
exception
and splits into
conserved
to resolve
rejoin S. pneumoniae
S. pseudopneumoniae,
metagenomic
studies
(1), and this in
diversity
pose. Naturally,
biochemical
ex- correspond
sequence
clusters.
related
groups
with
distinct
quence
have, however,
revealed thethey
to well-resolved
or break up closely
S. mitis so
that nearly
every
isolate
was
to be explained
by theory. Thus,
practical
dif- numerous
selectedsurveys
for the convenience
of taxonomists;
is ecological
indicating
However,
these
studies and
alsoobservations
show that there
presumably
a species of preferences,
its own. This is
clearly unsatisfactory.
ficulties, lack
of theory,
of vast
no
universal
or descriptor
of clusters
that recent ecological radiation from a sympatric
1
amounts
of ascutoff
yet unclassified
microbial
diversity
Department of Infectious Disease Epidemiology, Imperial
Habitats population
and Ecological
a species.
Furthermore,
inspection
(13). Differentiation
Thus, genetic clusters
characterizes
College London, London W2 1PG, UK. 2Department of Civil
have all fueled
the controversy
of how
one de- ancestral
and Environmental Engineering, Massachusetts Institute of
always
clearly
reveal
ecology
can
be discerned.
of
the
clusters
does
not
that
correlate
with
A
clear
natural
criterion
to
identify
clusters of
fines
a
bacterial
species
(38).
Technology, Cambridge, MA 02139, USA. 3Department of
What do the
genetic data
tell us
about
mechwhich level in the hierarchy is more fundamen- evolutionary
importance,
which
we
might
want
Biological Engineering, Massachusetts Institute of TechnolGenetic
Clustering
than any
other (Fig. 1) (7).
and that
the
anisms
of population
tal
to call species,
is to finddifferentiation
ecological features
ogy, Cambridge, MA 02139, USA. 4Broad Institute of MIT
As ancommented
example, Fig.
the relation- evolutionary
queshistory
the microbes
distinguish them
fromof close
relatives. inAmong
Darwin
that1A
allshows
true classification
and Harvard University, Cambridge, MA 02139, USA.
pathogens,
abilityare
to organized
cause a distinctive
disis genealogical
[(9), p.isolates
404]. Taxonomists
have tion?
of three closely
ships
among multiple
That the
bacteria
into genetic
*To whom correspondence should be addressed. E-mail:
c.fraser@imperial.ac.uk
ease hasishistorically
been
usedinteresting
to define species,
thus usedstreptococcal
sequence relatedness
define cutoff clusters
not, per se,
a very
obserrelated
species. toStreptococcus
REVIEW

us

orvegic

vibrio n
Entero
nsis

V. calvie
S. mitis
5% divergent

r
ua

s
i
nu ge
i/lo
r
e
ch

ia

st
ae is
V. V. f
eri
ch
fis
.
V

teu

rs
pe

s
V.

a*

cid

e
an

p
V.

S. oralis
0.005

Vibrio splendidus

0.005

Fig. 1. Multilocus sequence analysis of closely related species. (A) Radial

minimum evolution tree constructed using MEGA4, showing clusters among 97
isolates of four Streptococcus species identified as indicated. The tree was built
using concatenates of six housekeeping loci, resulting in a total of 2751 positions
in the final data set (2). Distances were calculated as the percentage of variant
nucleotide sites. The mean distance within the clusters, calculated by MEGA4, is
shown. To the right, the pneumococcal cluster is shown at larger scale, and
putative subclusters are indicated in dark gray, purple, and green. (B) Ecological

associations of Vibrionaceae sequence clusters (13). Habitats (colored dots) were

estimated as differential distributions of groups of closely related strains among
samples (size fractions enriched in different environmental resources). Clusters
associated with named species are evident, and in most cases species show a clear
predilection for one of the habitats. The exception is V. splendidus, which breaks
up into many closely related ecological populations. Asterisk denotes that trees
based on additional loci indicate that the placement of V. panecida within V.
splendidus may be an artifact of horizontal gene transfer at the Hsp60 locus.

not, per se, The

a veryfirst
interesting
observation;
many
or makes
strict thereference
accumulation
of neutral
diversity.
The
but
pathogens
only a minute
fraction of diversity.
of a population
proposed
mechanism
was
unifying
biological
to the
vation;
many constitute
or most models
most models
of a population
first proposed
wasniche
basedpartitioning,
on artificial
overall
bacterial
of mutation
bacterial based
selection reproducing
experimentswith
witha principles
reproducing
withdiversity.
a small Mapping
amount of
on artificial
of mechanism
selection and
amount
of mutation
will eventually
selection
experiments
with
bacteria
grownasfora
diversity
onto environmental
resourcesconsisting
indicates small
will eventually
produce populations
under the
ecotype
has rightly
become
popular
bacteria
grown
for extended
periodsproduce
populations
consisting
of clusters of
related
orga- framework
extended periods
under
stable
in chethat
closely of
related
groups
of bacteria
can be ecorelated
organisms,
irrespective
of stable
which
to conditions
discuss bacterial
of clusters
conditions
in chemostats,
which
showed
within
nisms, irrespective
the details
of the the
evolutionmostats, which
showedand
repeated
selective sweeps
logically
For example,
fine-scale
re- repeated
forces
or ecologiselective of
sweeps
in which
whole evolution,
the detailsdivergent.
of the evolutionary
speciation,
ecology.
ary forceswas
or ecological
more in The
which
the whole
waspredicts
thoughtthat
to
source
partitioningAhas
been
observedobservaamong genome
fixation
ecotype
modelgenome
(4, 16, 24)
cal differentiation.
more
substantial
thought todifferentiation.
hitchhike to A
is thatmutation
there is very
little common
hitchhike ancestry
to fixation
along
with an advantageous
coastal
Vibrio
populations
coexisting
in the
water substantial
there
is very little
neutral
diversity
will
be preserved
among bacalong with observation
an advantageous
(periodic
tion is that
diversity
many populations
microbes,
mutation
(periodic selection)
(22). Selective
column
Partitioning
discovered
of was
microbes,
frombecause
which neutral
(22). inSelective
sweeps ofcan
purge terial
(which sweeps
should
in many(13).
populations
populations
within niches
selection)
from which
we maydiversity
infer some
features
of the be
canmonophyletic),
purge almost alland
genetic
the popstrains
were
collected
distinct,
ecologically
in the
population
we may
infer
some from
features
of the
selective almost
all genetic
thusdiversity
predictsinthat
ecolandscape.a candidate
Neutral diversity
is the
ulationare
andcoherent
thus constitute
a candidate
informative
samples,diversity
and the phylogenetic
struclandscape. Neutral
is the amount
of selective
for types
self-contained
genemechapools.
and thus constitute
mechanism
polymorphism
nisma result,
for reducing
variation that
(23).ecotypes
ture
of the ecologically
differentiated
populations
in noncoding
re- amount
been suggested
polymorphism
that is evident
reducingofneutral
variationthat
(23).is evident in non- As
it has neutral
was
their habitats. substitutions.
Habitats were coding regions or results in synonymous sub- should be considered as putative or actual spegionssuperimposed
or results inonsynonymous
Niches and Ecotypes
stitutions.
common measure of neutral cies,
defined
using measure
an empirical
modeling
approach.
andOne
Ecotypes
One common
of neutral
diversity
is the Niches
depending on the level of genetic differdiversity
is
the
effective
population
size
N
To extendfrom
this model,
one can population.
consider multiple
This
analysis
revealed
high
levels
of
specialization
,
dee
the ancestral
This
effective population size Ne, defined as the size To extend this model, one can consider multiple
entiation
ecological
niches
characterized
by of
theproviding
selective
for
some
populations
(e.g.,
V.
ordalii
is
only
found
fined
as
the
size
of
a
population
evolving
in
the
of a population evolving in the absence of se- ecological niches characterized by the selective model therefore has the advantage
theyunderstanding
confer to specific
genes.
This is
as
singlethat
free-swimming
cells),
others are
of selection
that would
generate
as much
genes.
This aadvantages
lection
would generate
aswhereas
much neutral
di- absence
advantages
they confer
to specific
mechanistic
of the
evolutionmore generalist (Fig. 1B) and can colonize a wide neutral diversity as is actually observed. Esti- the ecotype model, where genes adapted to
is the ecotype model, where genes adapted to ary processes, as well as an organizing principle
versity as is actually observed. Estimates of N
variety of surfaces, including5 organic9 particles ande mates of Ne for bacteria range from 105 to 109 specific niches cause selective sweeps within
for bacteria range from 10 to 10 (1418). To specific niches cause selective sweeps within for classifying species, that is based on experizooplankton in the water column (13). Most of the (1418). To put this into context, the numbers of those niches but not in other niches. In this way
put this into context, the numbers of Vibrio cells those niches but not in other niches. In this mental observations of bacterial populations.
predicted Vibrio populations are deeply divergent Vibrio cells per cubic meter of seawater in tem- the population will undergo adaptation and difHowever, these observations of repeated
per cubic meter of seawater in temperate coastal way the population will undergo8 adaptation
from each other, and in 8many cases
are congruent perate coastal regions range from 10 to 109 (19), ferentiation while maintaining relatively low levels
regions range from 10 to 109 (19), which sug- and differentiation while maintaining relatively selective sweeps were made in chemostats,
of
neutral
diversity, as selective sweeps confined
with named species; however, V. splendidus
is
a
which
suggests
vast
census
population
sizes
census and
population
sizes
(>1020closely
). This low
neutral diversity,
as selective
ungests vast
natural environments
arethe
markedly
to each ecotype
regularly purge
population
notable
exception
splits into
numerous
(>1020levels
). Thisofobservationa
mismatch
of many whereas
mismatch
of
many
orders
of
regularly
observationa
sweeps
confined
to
each
ecotype
stable
and
diverse.
How
would
one
detect
the
related groups with distinct ecological preferences, orders of magnitude between effective population of any diversity that might have accumulated
size purge
sweeps
in diversity
natural bactemagnitude indicating
between effective
population
the census
population
of any diversity
selective
(Fig. 2A). of
Crucially,
what
neutral
we do
presumably
recent ecological
radiation
size and
population
size (truethat
of might
most presence
accumulated
(Fig. 2A). originally
Crucially,used
what
examples
and census
population
size
(true of (13).
mostThus,
bac- have
populations?
Thetomost
conclusive
observe
is predicted
be associated
with
adaptfrom
a sympatric
ancestral
population
bacteria
studied to date)was
to rial
date)was
originally
to neutral
is argue
predicted
diversity
we do observe
not The
fromability
bacteria
but from
RNA
viruses,
teria studied
ive traits.
of such
selective
sweeps
to
genetic
clusterstothat
correlate with
ecologyused
can be
counter claims
of neutrality
and instead
that come
The which
mutate
at much
highersize
rateshas
than
DNAcounter claims of neutrality and instead argue to
associated
limit the
effective
population
been
recdiscerned.
all be
genetic
variationwith
wasadaptive
adaptive traits.
(20, 21).
21). ability
been
established
from
thatWhat
all genetic
wastell
adaptive
(20,
of there
such are
selective
limit the based
It has(17,
ognizedlife
forforms.
some time
23),
and this model
do thevariation
genetic data
us about
mechHowever,
several sweeps
different to
mechanisms
population
size has (Fig.
been2).recognized sequences
the
However,
are several
different and
mechacollected over
many by
years
that and
has been substantially
developed
Cohan
anisms
of there
population
differentiation
the effective
that can explain
this mismatch
explain
thismicrobes
mismatchin(Fig.
2).
anddriving
this model
has population
for Whatever
some time
(17, 23), are
structure
the human
influenza
nisms that can
colleagues (4,
16, 24).ofBecause
it links
patternsviof
evolutionary
history
of the
question?
mechanisms
the differWhatever
driving
driven
by repeated
selecsubstantially
Cohan
is predominantly
genetic
differentiation with
adaptation,
and makes
That
bacteria aremechanisms
organized intoare
genetic
clustersthe
is been
entiation
of bacteria developed
into clusters,bythey
mustand
re- rus
differentiation of bacteria into clusters, they colleagues (4, 16, 24). Because it links patterns tive sweeps (25) and that the resulting effective
must restrict the accumulation of neutral of genetic differentiation with adaptation, and population size Ne (<100) is very much smaller
742
6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org

31

iples of
ype has
within
ciation,

cts that
ng bacould be
cotypes
As a reshould
ies, dentiation
l therehanistic
sses, as
ssifying
bserva-

E2

E1

B
new and empty

*
*
*

*
*

colonization

*
*

old and void

stable ecotype
concept

del with
ot niche
bottlewhole
le indill other
induce
ks will
pulation
ded into
etween
e popupatches
acterial
eria are
ig. 2B)

Population size

20

ated sewhereas
ble and
ence of
lations?
ot from
utate at
orms. It
ollected
cture of
y driven
hat the
100) is
acteria.
genetic
models
karyotic
alogies,
iven by
ngitudions, as
shes in
changes
ological

colonization

Bacteria

Phage

15
10
5
0
0

20

40

60

80

100

Time

Fig. 2. Different models of microbial evolution that lead to low values of Ne. (A) The ecotype
model of bacterial population differentiation. The tree shows a single bacterial lineage that differentiates into two sublineages (E1 and E2) that differ in some aspect of their ecology. Periodic
selection (a selective sweep) occurs at the points marked by asterisks and eliminates almost all of
the diversity that has arisen since the last episode of periodic selection, which is shown by the
dashed branches (diversity purged by periodic selection) or solid branches (existing diversity) on
the tree. As the two populations are ecologically distinct (i.e., ecotypes), periodic selection in one
sublineage does not influence diversity in the other sublineage and vice versa. Each ecotype can
therefore diverge to become separate species. Reproduced from (24) with permission. (B) A metapopulation. Patches of varying size (gray circles) are vacant (empty) or may be colonized by a
single genotype randomly acquired from another patch. Strains may diversify within a patch (as
shown by different colors representing distinct genotypes), which may colonize empty patches as
described above. A characteristic of this sort of metapopulation is patch turnover, in which patches
occasionally become unable to support colonization and their inhabitants are removed (solid gray
circles). (C) A neutral model with small population size. Different genotypes (different colors) arise
by mutation or recombination and increase or decrease in the population by random drift. For
some purposes, this simple model is an adequate effective description of the more complex processes represented in (A), (B), and (D), and of other more complex evolutionary models not described in this review. (D) Predator-prey dynamics and population bottlenecks. Regular population
bottlenecks can drastically shrink the effective population size. In this case, bacteria-phage
predator-prey dynamics are simulated with a classical Lotka-Volterra model, which can generate
oscillations in population size of any amplitude. Population sizes and time axes are in arbitrary
units for illustrative purposes only.

Metapopulation structure, in which the population is divided into patches and where individuals disperse between patches, can generate
very low effective population sizes if patches
turn over (i.e., if patches are only intermittently
able to support bacterial growth, and if a small
number of bacteria are dispersed to colonize
empty patches) (Fig. 2B) (27). This structure
well describes the situation for parasites, which
can colonize a host but are then forced to move
on because the host develops immunity or dies
(17). It also describes any situation where bacteria use a limited resource intensively for short
bursts, followed by dispersal to new resource
patches (e.g., colonization of organic particles
in seawater by Vibrio populations). This metapopulation model is fundamentally different
from the ecotype model because it does not
predict an association between neutral diversity
and adaptive traits.
The relevance of the metapopulation model
to the species question is that, although highly
idealized and simplified, it may capture some of
the effects of complexity and instability of actual ecosystems on population structure. Selective
sweeps are predicted to be inevitable in simple,
stable environments but not in complex metapopulations [a point partly addressed in (28)]. A
metapopulation may evolve, differentiate, and
adapt without global selective sweeps. Diversity lost by a local selective sweep in one patch
may be rescued and reintroduced from other
patches. The ecotype model, with its predicted
monophyletic relationship between niche and
genotype, may therefore not be an appropriate
model of speciation in complex ecosystems.

Choosing Between Models

It has proven difficult to discriminate between
models of population differentiation that focus on ecotypes or metapopulations. For example, the ecotypic structure of a soil Bacillus has been modeled to predict a priori which
sequence clusters were ecotypes, and hence
which ones should be associated with specific
ecological properties (16). Some clusters are
associated with certain phenotypic traits, such
as a propensity to grow on shady north-facing
slopes or sunny south-facing slopes. However,
this model fitted no better (and in fact slightly
worse) than a version of the model with several
subpopulations and diversity generated only
by neutral drift. This version of the model was
dismissed because of its association with a very
low estimate of population size (14). However,
estimates of effective population size Ne are often grossly disconnected from census population sizes. It has proven very challenging to find
models that successfully explain low estimated
values of Ne while providing better predictions
than models based on simple neutral drift. The
analysis of Bacillus partly did this by predicting
more ecotypes in the model than were observed

(27). This structure well describes the situation does not predict an association between neutral
than observed for bacteria. The use of longitu- Bottlenecks, Metapopulations, and Local
for parasites, which can colonize a host but are diversity and adaptive traits.
dinal ecological and genetic data to distinguish Extinctions
then forced to move on because the host develops
The relevance of the metapopulation model to
between competing models of evolution has a The essential element of the ecotype model
immunity or dies (17). It also describes any the species question is that, although highly ideneutral
diversity
long
pedigree
eukaryotic
On with
to limiting
situation
whereinbacteria
use abiology
limited (26).
resource
alizedrespect
and simplified,
it may
capture
some is
of not
the
the
basis offor
these
any inference
of a niche
per se,
rather the
intensively
shortanalogies,
bursts, followed
by dispersal
effects adaptation
of complexity
andbut
instability
of effecactual
structure
driven(e.g.,
by selective
sweeps
population
bottleneck
caused by structure.
the replacement
of
to new resource
patches
colonization
of tive
ecosystems
on population
Selective
data
from
natupopulation
by
descendants
from
would
require
good
longitudinal
the
whole
organic particles in seawater by Vibrio popula- sweeps are predicted to be inevitable in simple,a
extinction
ral
bacterial
populations, as well
as is
observations
individual andbutthenotresulting
tions).
This metapopulation
model
fundamen- single
stable environments
in complex
metaof
episodic
crashes
in
diversity
causally
associof
all
other
lineages
(Fig.
2A).
Other
tally different from the ecotype model because it populations [a point partly addressed inmecha(28)].
ated with genetic changes and not associated nisms that induce or involve regular population
with changes in ecological covariates.
bottlenecks will also restrict neutral diversity.
743
ww.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009

32

Relative
r of of
change
distance
between
Relative
rate
r rate
change
in in
distance
between
-9)-9)
clusters
per
generation
(x10
clusters
per
generation
(x10

SPECIALSECTION

and diversity generated only by neutral drift. This ples shown in Fig. 3 differ only in the rate of to recombination will depend more on the accuto recombination
will depend
more on
accuples shown in
Fig. 3 differbetween
only inthe
theclusters,
rate of mulation
and diversity
by neutral
drift.of
This
of differences
at neutral
locithethan
at
recombination
version
of thegenerated
model wasonly
dismissed
because
its homologous
mulation loci.
of differences
neutral
lociathan
at
homologous
recombination
between
the clusters,
version of the
model
waslow
dismissed
because
of its all
The modelsatalso
assumed
homoother parameters
being held
constant.
As re- adaptive
association
with
a very
estimate
of populaadaptive
loci.
The
models
also
assumed
a
homoall
other
parameters
being
held
constant.
As
reassociation
with
a
very
low
estimate
of
population size (14). However, estimates of effective combination increases, we see a distinction be- geneous distribution of polymorphisms across
tion size (14).
However,
estimates of effective combination increases, we see a distinction be- geneous distribution of polymorphisms across
population
size N
e are often grossly disconnected
population
size
Ne ecological
are often
grossly
Recombination rate relative to mutation
using
established
criteria,
a hypothfrom
census
population
sizes.
It hasdisconnected
proven
very
Recombination rate relative to mutation
from
census
population
sizes.
has successfully
proven very
that can be
esis
challenging
to tested.
find models Itthat
0.10 clonal
3
challenging
to find
0.10 clonal
This problem
of lowmodels
power
selection
3
explain
low estimated
values tothat
ofdetect
Nesuccessfully
while
pro0.53 threshold
explain
low
estimated
Ne while
protovalues
reject
neutrality)
a
(or,
more
accurately,
viding
better
predictions
than of
models
basedis
on
0.53 threshold
viding
better
predictions
than
models
on
2.00 sexual
simple
neutral
drift. in
The
analysis
of based
Bacillus
genetics
that
very
general
problem
population
2
2.00 sexual
simple
neutral
drift.
The
analysis
of
Bacillus
2
partlynot
didnegate
this by
ecotypes in
in
does
thepredicting
importancemore
of adaptation
partly
did
this
by
predicting
more
ecotypes
in
the model than
were observed
established
evolution,
but rather
suggests using
that more
work
theneeded
model than
were aobserved
usingthat
established
1
ecological
criteria,
hypothesis
can be
model-based
methods
is
if
we want
1
ecological criteria, a hypothesis that can be
tested.
to
discriminate among different biologically
tested.
This problem
of low power
to detectdata.
selection
plausible
explanations
of genetic
In
0
problem
of low powerneutrality)
to detect selection
(or, This
more
accurately,
is a very
scheme for performing
Table
1 we
proposetoa reject
0
(or,
more
accurately,
to
reject
neutrality)
is
a
very
general problem
in population
that does
analyses
that could
be used genetics
to test, develop,
general
problemimportance
in population
genetics that
does
not
negate
of adaptation
evoand
validatethedifferent
competing
modelsinmore
-1
not negate
the
importance
ofthat
adaptation
in evolution,
but
rather
suggests
more
work
is
-1
systematically.
lution,
but
rather
suggests
that
more
work
is
"Speciation point" for
needed if we want model-based methods to dis"Speciation
point" for
sexual
species
needed if among
we wantdifferent
model-based
methods
to discriminate
biologically
plausible
-2
sexual species
Homologous
Recombination
criminate
among
different
biologically
plausible
-2
explanations
genetic data.
In Table
1 we
proOne
specific of
challenge
to models
that
invoke
explanations
of
genetic
data.
In
Table
1that
we
propose
a
scheme
for
performing
analyses
could
involves a feature
of bacterial
ecotypic
structure
poseused
a scheme
performing
analyses
could
-3
be
to test,fordevelop,
and
validatethat
different
evolutionhomologous
recombinationthat
-3
be
used
to
test,
develop,
and
validate
different
competing
models
more
systematically.
0%
10%
20%
30%
we
have notmodels
yet discussed.
Bacterial reproduccompeting
more systematically.
0%
10%
20%
30%
Mean
genetic
distance
between
clusters
the obligate reassortment
tion
does not involve
Homologous
Recombination
Mean genetic distance between clusters
of
genetic material
observed in most higher orHomologous
Recombination
3. The dynamics of cluster divergence. The figure summarizes some key results from (15) in a
One specific challenge to models that invoke Fig.
Fig. 3. The dynamics
of cluster
Thetwo
figure
summarizes
some
key results from
(15) in
ganisms.
However,
recombination
does occur
in phase-space
plot of the
geneticdivergence.
dynamics of
populations,
with
recombination
occurring
be-a
One
specific
challenge
to amodels
invoke
ecotypic structure involves
feature that
of bacterial
phase-space
plot
of
the
genetic
dynamics
of
two
populations,
with
recombination
occurring
bearchaea
(29) and
typically
bacteria
ecotypicand
structure
involves
a feature
of involves
bacterial tween them at a rate that is varied for the three different simulations. The y axis shows the rate of
evolutionhomologous
recombinationthat
tween them
at a rate
that isbetween
varied for
the
three as
different
simulations.
The y distance
axis shows
the(xrate
of
change
of
genetic
distance
the
clusters
a
function
of
the
genetic
itself
axis).
short
piece
of
DNA
with
the
replacement
of
a
evolutionhomologous
recombinationthat
we
have not yet discussed. Bacterial
reproduction When
changethe
of rate
genetic
distance
between
the
clusters
as
a
function
of
the
genetic
distance
itself
(x
axis).
of change is positive, the populations will diverge genetically; when negative, they
strain.
the
homologous
segment
from reassortment
another
we have
yet discussed.
Bacterial
reproduction
does
notnot
involve
the obligate
of converge.
When the rate
change of
is positive,
the each
populations
willisdiverge
when negative,
they
The of
direction
change for
scenario
shown genetically;
by arrows color-coded
to each
Recombination
becomes
less
probable
with
does
not
involve
the
obligate
reassortment
of
genetic material observed in most higher orga- scenario.
converge. For
Thelow
direction
of
change
for
each
scenario
is
shown
by
arrows
color-coded
to
each
recombination rates, the populations are effectively clonal and always diverge
sequence
divergence
between
the
increasing
genetic However,
material
observed
in mostdoes
higher
orgascenario.
For As
lowthe
recombination
populations
are effectively
clonal
and alwaysslow
diverge
nisms.
recombination
occur
in (green
line).
recombinationrates,
rate the
increases,
the cohesive
effects of
recombination
the
nisms.
However,
recombination
does
occur
in
31),
which
reduces
donor
and
the
recipient
(30,
(green
line).
As
the
recombination
rate
increases,
the
cohesive
effects
of
recombination
slow
the
bacteria and archaea (29) and typically involves rate
of divergence, until a threshold is passed (red line) and the populations become effectively
bacteria
and
and
typically
involves
but
does
not archaea
eliminate
recombination
between
rate of in
divergence,
is passed
(red line)
and For
the recombination
populations become
effectively
the
replacement
of a(29)
short
piece
of DNA
with sexual
the sense until
that athethreshold
populations
no longer
diverge.
rates above
this
the replacement
of
a short
pieceanother
of such
DNAstrain.
with sexual in the sense that the populations no longer diverge. For recombination rates above this
closely
related species.
Because
of
interthe
homologous
segment
from
level, the fate of the two populations will depend on how genetically distinct they are at the outset.
the
homologous
segment
from
another
strain.
any
given
isolate
within
species
recombination,
level,
of the
populations
will then
depend
on how genetically
distinct
are at the
outset.
Recombination becomes less probable with in- If
theythe
arefate
within
thetwo
speciation
point,
recombination
will cause
themthey
to merge.
If they
are
Recombination
becomes
lesstobetween
probable
with
in- farther
If they are
within
the
speciation
point,
then
recombination
will
cause
them
to
merge.
If
they
are
at donor
least
acreasing
speciessequence
is almost
certain
containthe
divergence
away than this speciation point, they will continue to diverge from each other. These
creasing
sequence
divergence
farther are
away
than using
this speciation
they
some
material
isbetween
characteristic
of curves
derived
the model point,
described
in will
(15).continue to diverge from each other. These
and
thegenetic
recipient
(30,
31),that
which
reducesthe
butdonor
does
and the
recipient
(30, species.
31), which
reduces
but does
closely
related
Hence,
whereas
it curves are derived using the model described in (15).
other
was once thought that bacteria do not form spe6 FEBRUARY
2009 VOL 323 SCIENCE www.sciencemag.org
744 cies in the eukaryotic sense because they
do not
6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
744
recombine at all (32), one current view is that process that reduces the rate of recombination Illegitimate Recombination and Gene
they do not form species because they recom- between themfor example, a period of allopa- Content Variation
bine too much (5).
try or ecological differentiation. The speciation Illegitimate recombination or gene acquisition
In asexual clonal organisms, even in the point is the amount of divergence between clus- is another unusual feature of bacteria. In this
absence of any selective pressure, clusters will ters that needs to accumulate to prevent them case, genes or clusters of genes are acquired
spontaneously split into multiple lineages or from returning to a single cluster if the barriers that typically have no homolog(s) in the recipidaughter clusters (15). However, under cer- to recombination are removed. A recent study ent strain. The importance of this phenomenon
tain circumstances recombination can prevent hypothesized that two related Campylobacter is evident in the clear and ubiquitous signature
this, and we can hence divide the bacteria into species are currently undergoing this process of such events in the growing body of genomic
sexual and nonsexual species. This effect, of merging into a single species as a result of data. These are identified by differences in the
described at greater length elsewhere (15), is changes in their environment (33).
characteristics of the acquired DNA and that of
The above insights were reached using mod- the host strain, for example, in base composition
summarized in Fig. 3, which shows the rate
at which two clusters diverge over timethat els based on the assumption that genetic varia- or codon usage; in most cases, the donor of the
is, the increase in the mean genetic distance tion is neutral. Although this is obviously not DNA in question is unknown. Gene acquisition
between them. If this becomes negative, then always an appropriate assumption, it is plau- leads to genomes being punctuated by stretches
the two clusters will stop diverging and instead sible that the number of loci explicitly involved of foreign DNA. The largest of these (which
converge. The three examples shown in Fig. 3 in adaptive ecological differentiation will be may be many kilobases in length) were initially
differ only in the rate of homologous recom- small, and thus that in an unstable landscape, termed pathogenicity islands, because the new
bination between the clusters, all other param- genomic barriers to recombination will depend functions encoded by the imports were often
eters being held constant. As recombination in- more on the accumulation of differences at neu- involved in virulence, but a better term is gecreases, we see a distinction between a clonal tral loci than at adaptive loci. The models also nomic islands as the phenomenon is far from
organism in which clusters are predicted to di- assumed a homogeneous distribution of poly- limited to pathogens (36, 37). Although it is
verge (the green line) and a sexual organism morphisms across the genome, and violation hard to quantify the selective impact of import(the blue line) in which they are predicted to be of this may alter the tempo and mode of these ing any given gene(s) into a new background,
held together by recombination. For sexual processes (34, 35).
the occasional ability to gain a new adaptation
species, the divergence of clusters requires a
in this fashionsuch as a new metabolic capa-

33

the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in
The importance of this phenomenon is evident in between them by mobile elements. The evolu- different genera on the basis of their specific charin the growing body of genomic data. These are loosely coupled with that of any particular gene content and recombination. In any case, no
the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in
identified
by differences in the characteristics of species or strain in which they are found, and biologist would deny the importance of ecology
in the growing body of genomic data. These are loosely coupled with that of any particular gene content and recombination. In any case, no
are maintained
selection
by and
the biologist
to what would
we observe,
it may not
be easy to
the acquired
DNA
that of inthethehost
strain, for of they
species
or strain in through
which they
are found,
deny thebut
importance
of ecology
identified
by and
differences
characteristics
incorporate
it
in
a
fashion
that
example,
in
base
composition
or
cobut it may
not beineasy
to is
the
acquired
DNA
andof
that
of the host strain, for they are maintained through selection by the to what we observe,
bility
ormost
a new
mode
transticular species
ortaxonomists.
strain
which
convenient
for
Nonedon usage;
in
cases,
the
donor
of
incorporate
it inand
a fashion
is
example,
in base
composition or cothey arethat
mainmission for
a pathogenmay
they are found,
theless,
population
geneticists
the DNA
in question
is unknown.
convenient
for taxonomists.
None-may
don
usage;
in most cases,
the donor of
be of enormous importance in
tained through selection by the
have little
choice geneticists
but to tackle
Gene the
acquisition
to genomes
theless,
population
may the
DNA inleads
question
is unknown.
terms of speciation.
habitat to which each host strain is
question
defining
being Gene
punctuated
by leads
stretches
of
have
little of
choice
but bacterial
to tackle species
the
acquisition
to genomes
Perhaps even more striking
adapted. In the case of very mobile
question
of
defining
bacterial
species
punctuated
by of
stretches
of
or,
at
the
very
least,
populations.
foreignbeing
DNA.
The
largest
these
elementsfor example, plasmids
is the amount of variation in
or,
at the veryareleast,
populations.
DNA.
Thekilobases
largest ofintheseEcological
Whether
estimating
effective
(whichforeign
maycontent
be
many
revealed
by mulencoding we
resistance
to antibiotics
gene
Ecological
factor
b
Whether
we size
are estimating
effective
may be termed
many kilobases
in
population
from
neutral
diversity
length)(which
were
initially
pathofactor
b
tiple genomes from the same
or heavy metalsthe ecological
population
size from
neutral diversity
length)
were because
initially termed
pathoor
choosing
an appropriate
set of
genicity
islands,
the that
new
which
implies
determined
by
these
species,
specificity
orstrains
choosing
anforappropriate
set of at
genicity
islands,
because
the new
to test
positive
selection
functions
encoded
by the occurs
importsatwere
gene
acquisition
a
accessory
loci
may
have
no
link
strains
to of
testinterest,
for positive
selection
at
functionsin
encoded
by the
imports
were
a locus
species
definitions
often involved
virulence,
but
a bethigh
frequency.
observe
using
surprisingly
the of
sequence
a to
locus
interest, we
species
definitions
often
involved
in virulence,
butIta betare
implicit ingenes
much(Fig.
of the
ter term
is genomic
islands
as the
is now
to speak
housekeeping
4).analytical
are
implicit in much
of the analytical
ter
termcommonplace
is genomic islands
as the
toolkit
of
population
genetics.
phenomenon
is
far
from
limited
to
genome,
which
of
the
core
toolkit of population genetics.
phenomenon is far from limited to
Distinguishing
among
mechapathogens
(36, 37).
Although
it is
hard
encodes
fundamental
funcIdentifying
Mechanisms
and
Distinguishing
among
mechapathogens
(36,
37). Although
it is hard
nisms
population
differentiation
to quantify
the
selective
impact
of imtions
shared
all
members
Delineating
Speciesdifferentiation
nisms
ofofpopulation
to
quantify
the by
selective
impact
of imbacteria
ultimately
comes
down
portingporting
given
gene(s)
ainto
new
What
do ultimately
we
want comes
from
bacterial
ofany
a species
(and, gene(s)
it into
should
goa new
inin
bacteria
down
to to
any given
Ecological
Ecologicalfactor
factoraa
species?
Do
weofneed
theoretical
withoutthesaying,
otherability
related
testing
ability
of
different
models
background,
occasional
to to
testing
thethe
ability
different
models
background,
the occasional
ability
4. Differences
between
schematic toto
4. Differences
betweencore
coreand
andauxiliary
auxiliary genes.
genes. This schematic
consistency
evenvariable
atvariable
the expense
species),
which
bolted
explainhighly
highly
patterns
gain a new
in thisinis
fashion
explain
patterns
gain
aadaptation
newonto
adaptation
this
fashionFig.Fig.
illustrates
the
relationships
between
three
species
in
ecotype
space, within
illustrates
the
relationships
between
three
species
in
ecotype
space,
of taxonomic
practicality,
incorpothe
auxiliary
or
accessory
within
and
between
genetic-ecological
such as
a
new
metabolic
capability
and
between
genetic-ecological
such as a new metabolic capability
shown
in two
dimensions,and
anda amobile
mobilegene
gene common
common to
herehere
in two
dimensions,
to all
all three.
three. clusters
clonal
sexual
genome,
composed
of genes
rating both
(Fig.
1).1).It It
isand
stillstill
unclear
or
amode
new mode
of transmission
clusters
(Fig.
is
unclear
or a new
of
transmission
for afor ashown
The
areas
occupied
by
the
species
are
shown
as
solid
in
red,
blue,
The
areas
occupied
by
the
species
are
shown
as
solid
lines
in
red,
blue, whether
populations
into
a single
theoand operons
may
or may
these
patterns
areare
mainpathogenmay
of enormous
whether
these
patterns
mainpathogenmay
bethat
ofbe
enormous
im- im- and green. The part of the ecological space where the shared mobile gene
and green. The part of the ecological space where the shared mobile gene tained
framework?
One
unifying
present
all
isolates. It
reticalby
notinbeterms
gene
flow
or or
selection,
portance
in terms
of speciation.
tained
by
gene
flow
selection,
portance
of in
speciation.
is selected
in each
species
shownbybyaadashed
dashedpurple
purple line
line and
is selected
in each
species
is isshown
and overlaps
overlaps theoretical
is
consider
seems
likelymore
that more
such striking
auxiliaof to
population
Perhaps
even
andwhat
whattheconcept
theeffect
effect
of
population
Perhaps
even
striking
is theis the all three species ranges. Examples of (circular) genomes from each species and
all
three
species
ranges.
Examples
of
(circular)
genomes
from
each
species structure
is.
The
joint
distribution
of of
ofhelp
variation
in gene
content with and without the purple mobile element are also illustrated. Note
as
the
arena
within
which
genes
toindetermine
the
species
ryof
structure
is.
The
joint
distribution
amountamount
variation
gene
content
that
with and without the purple mobile element are also illustrated. Note that genetic
and
ecological
data
cancan
be be
revealed
by multiple
genomes
individuals
are
similar
enough,
specific
ecological
properties
for each
species,
the
locus
is
not
selected
for
all
isolates,
and
its
evolugenetic
and
ecological
data
revealed
by multiple
genomes
fromfromfor each
the locus is not selected for all isolates, and its evolu- or interbreed
above that
for Vibrio
the
same
species, For
implies that tionaryspecies,
enough,
organism.
example,
of the
is uncoupled from that of each host species, because if one used,
used,asasdescribed
described
above
forindiVibrio
the same
species,
whichwhich
implies
that tionary fatefate
is
uncoupled
from that of each host species, because if one species
to genes
define compete
populations
gene
acquisition
at a sur- undergoes a selective sweep
vidual (13),
variant
dia group
of related occurs
Leptospirilor
goes
extinct,
the
mobile
gene
may
be
gene acquisition occurs at a sur- undergoes a selective sweep or goes extinct, the mobile gene may be species (13), to define populations
making
a strong success.
theoretprisingly
high frequency.
It is now reintroduced from one of the other species. Examples of such distributed without
reproductive
been hypothrectly for
lum has recently
without
makingto aeither
strong
theoretprisingly
high frequency.
It ofisthe
now
of the determinants
other species.inExamples
suchb-lactamase
distributed ical
commitment
of these
commonplace
to speak
corereintroduced
loci includefrom
drugone
resistance
pathogensof(e.g.,
Practical
advances building
on
esized to adapt
to different
ical
commitment
to
either
of
these
commonplace
to
speak
of thefundamental
core loci genes)
include
drug
resistance
determinants
in
pathogens
(e.g.,
b-lactamase
alternatives.
One
clear
result
from
genome,
which
encodes
and heavy metal resistance in environmental organisms. These
this or other theoretical concepts
areas of an acid mine drainage
alternatives.
One
clear
result
from
genome,
which
encodes
fundamental
and
metal resistance
in environmental
of the
hereare
is
functions
by allof
members
genes
mayheavy
be transferred
among strains
and species by organisms.
conjugative These
plas- allwill
onlystudies
come discussed
when these
system byshared
shuffling
chro- of agenes)
all
of
the
studies
discussed
here
functions
shared
by
all
members
of
a
genes
may
be
transferred
among
strains
and
species
by
conjugative
plasthat
the underlying
ques- is
species
it should
go without
mids or other mobile elements (including transducing phage).
developed
into theoretical
explicit models
enriched
in
mosome(and,
segments
that
the
underlying
theoretical
quesspeciessaying,
(and,
it
should
go
without
mids
or
other
mobile
elements
(including
transducing
phage).
tions
concerning
species
will
not
be
other
related
species),
onto
and model-based algorithms that
noncore genes (38, 39). We
tions
concerning
species
will
not
saying,which
other
related
species),
onto
answered
in
the
absence
of
more
detailed
genetichabitat
to
which
each
host
strain
is
adapted.
In
is
bolted
the
auxiliary
or
accessory
are tested and refined on a wide be
should, however, be aware
mapping.
some
guidethe
case
of very
mobile
elementsfor
examcomposed
genesormay
and
operons
answered
in the
absenceMoreover,
of more
genetictodifferent
which
each
host
strain is adapted.
In environmental
which genome,
is bolted
theinauxiliary
accessory
it maydetailed
be sensible
that
changes
coreof genes
also
leadthat
to habitat
tic of
levels
of ecological
specificity,
range
of data.
Alternatively,
lines
for
the
types
of
ecological
studies
that
will
ple,
plasmids
encoding
resistance
to
antibiotics
or
may
or
may
not
be
present
in
all
isolates.
It
seems
environmental
mapping.
Moreover,
some
guidethe
case
of
very
mobile
elementsfor
examgenome,
composed
of
genes
and
operons
that
ecological differentiation, a phenomenon well ranging from highly conserved core functions to suggest an ad hoc application of principles
be
most
informative
are
emerging.
Most
imporheavy
metalsthe
ecological
specificity
deterthat
such
auxiliary
genes
help
to
determine
lines
for
the
types
of
ecological
studies
that
ple,
plasmids
encoding
resistance
to
antibiotics
or
may orlikely
may
not
be
present
in
all
isolates.
It
seems
documented in experimental studies of bacteria that are essential for growth in all environments to different genera on the basis of their specificwill
the ecological
data
be imporrelmined
by
these
loci
may
have no
linka tant,
the
specific
ecological
properties
the(40).
organism. heavy
be most
informative
arecollected
emerging.
metalsthe
ecological
deterlikely that
suchinauxiliary
genes
help toofdetermine
including
the
extentmust
ofMost
variation
growing
structured
environments
to loci
that
are accessory
involved
withspecificity
adaptation
to
characteristics,
evant
to
the
niche
boundaries
of
the
populations
to
the
sequence
clusters
we
observe
using
houseFor
example,
a
group
of
related
Leptospirillum
tant,
thecontent
ecological
data collected
be relby these
accessory
mayniche-specific
have no link in
the specific
ecological
properties
of the
In must
any case,
Estimates
vary,
depending
on organism.
the genomes mined
Some loci
narrow
gene
and recombination.
specific
habitat.
if genetic
groups do
map exgenes (Fig. 4).we observe using house- studied.
has recently
been of
hypothesized
to adapt to dif- keeping
evant
toAnd
thewould
niche
boundaries
of not
the populations
sequence
For example,
a group
butrelated
as littleLeptospirillum
as 40% of genes to the
biologist
deny
the importance
of ecolthat are available,
genes
may beclusters
distributed across species, being no
onto sampling categories (as is likely
ferent areas of an acid mine drainage system by keeping genes (Fig. 4).
studied.
And
geneticbut
groups
notbemap
has recently
hypothesized
to adapt
to dif-of a transferred between them by mobile elements. clusively
to what
weifobserve,
it maydonot
easy exgenomes
may bebeen
present
in all sequenced
ogy
to be the case), more complex statistical models
shuffling of chromosome segments enriched in Identifying Mechanisms and
clusively
onto
sampling
categories
(as
is
likely
in
a
fashion
that
is
convenient
fate
of
such
genes
may
hence
to
incorporate
it
may consider
genes Delineating
The evolutionary
ferent named
areas ofspecies
an acid(41).
mineWe
drainage
system by
Species
will be needed to identify and describe the undernoncore genes (38, 39). We should, however, be Identifying Mechanisms
population
gea named species
as being
characteristaxonomists.
Nonetheless,
be only loosely coupledand
with that of any par- for
within
to
be
the
case),
more
complex
statistical
models
shuffling
of
chromosome
segments
enriched
in
aware that changes in core genes may also lead to What do we want from bacterial species? Do we lying niche structure. Longitudinal studies that
Species
neticists
may have
little choice
but to tackle
will be needed
to identify
and describe
the the
undernoncore
genes (38,
39). We should,
however, bewell Delineating
the dynamics
of ecological
associations
ecological
differentiation,
a phenomenon
need theoretical consistency even at the expense measure
question
of
defining
bacterial
species
or,
thethat
lying
niche
structure.
Longitudinal
studies
aware documented
that
changes
in
core
genes
may
also
lead
to
What
do
we
want
from
bacterial
species?
Do
we
18. H.time
Ochman,
C. Wilson,
in Escherichia
coli andathow
willA.also
be helpful
to determine
in experimental
studies
of bacteria andofvalidating
taxonomic
practicality,
incorporating
Table 1. A proposed
strategy
for developing
models
of bacterial
evolution both
that over
populations.
are
estimatvery
least,
Salmonella
typhimurium:
Cellular
andwe
Molecular
Biology,
measure
the
dynamics
of ecological
associations
ecological
a phenomenon
well diversity
need
theoretical
consistency
evenfoundation
at into
the expense
mightdifferentiation,
eventually
be used
to classify
genetic
dataand
andsexual
provide populations
a firm
for a transient
natural
habitatsWhether
are,
and
thus
how
likely
growing
in structured
environments
(40).
clonal
a single
F. C. Neidhart,
Ed. (ASM Press,
Washington,
DC, diver1987),
size
from
neutral
ing
population
overeffective
time
will
also
be
helpful
to
determine
how
documented
in species
experimental
studiesonofthe
bacteria
taxonomicframework?
practicality,
both bottlenecks
bacterial
are
to
result.
Finally,
whole-genome
Estimates
vary,concept.
depending
genomes of theoretical
Oneincorporating
unifying theoretical
pp. 16491654.
to
sity
or choosing
appropriate
set thus
of
transient
natural
habitats
are, and
how
likely
growing
structured
(40).
a within
single sequences
from etan
entire
populations
of strains
environthatinare
available,environments
but as little as
40% of genes clonal
conceptand
is tosexual
considerpopulations
species as theinto
arena
19. J. R. Thompson
al., Appl.
Environ.
Microbiol.
70, 4103
1. Collect
according
to systematic
stratification.
Focus onOne
longitudinal
for
positive
a locuswhole-genome
of interest,
(2004).
bottlenecks
are selection
to result.atFinally,
Estimates
vary, samples
depending
on the
genomesecological
theoretical
framework?
unifyingstudies,
theoretical test
geographical studies, and measurement of physical and chemical gradients affecting bacterial
20. M. Kimura,
Trends Biochem.
Sci. 1, N152
(1976).
definitions
are implicit
in much
the
sequences
from
entire
populations
of ofenvironthat are available,
but as little as 40% of genes concept is to consider species as the arena within species
21. R.
Milkman,
Trends
Sci. 1,genetics.
N152 (1976).
growth. Consider biotic factors www.sciencemag.org
such as the presence of other competing
parasitic6 phage.
745
SCIENCEbacteria
VOLor323
FEBRUARY
2009
of Biochem.
population
analytical
toolkit

Speciation

22. K. C. Atwood, L. K. Schneider, F. J. Ryan, Proc. Natl.

2. For each isolate, sequence as much as possible and affordable (16S rRNA, MLSA, auxiliary
Distinguishing
among mechanisms of popAcad. Sci. U.S.A. 37, 146 (1951).
genes, full genomes, etc.).
bacteria ultimately
ulation
www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY
23. B.2009
R. differentiation
Levin, Genetics 99, 1in(1981).
3. Use empirical classification algorithms that use genetic and ecological data to jointly map isolates.
24. F. M.down
Cohan, to
E. B.testing
Perry, Curr.
17, R373
differcomes
theBiol.
ability
of(2007).
25. models
A. Rambaut
al., Naturehighly
453, 615
(2008). patterns
4. To guide model formulation, use population genetic tests on observed clusters, focusing on
ent
toetexplain
variable
26. R. A. Fisher, E. B. Ford, Heredity 1, 143 (1947).
tests for selection, population structure, and gene flow.
and between
genetic-ecological
within
27. M. Slatkin,
Theor. Popul.
Biol. 12, 253 (1977).clusters
5. Generate evolutionary models and simulate populations.
whether
these
(Fig.
It is still
28. J.1).
Majewski,
F. M.unclear
Cohan, Genetics
152,
1459patterns
(1999).
6. Test, then reject or adapt, evolutionary models according to agreement between simulations
29. maintained
E. J. Feil, B. G. Spratt,
Annu. Rev.
Microbiol.
55, 561 (2001).
and
are
by gene
flow
or selection,
30. J. Majewski, F. M. Cohan, Genetics 153, 1525 (1999).
and real populations; if necessary, return to step 1.
what
the effect of population structure is. The
31. J. Majewski, P. Zawadzki, P. Pickerill, F. M. Cohan,
7. For successful models, develop model-based methods for interpreting pure genetic data
jointC.distribution
of genetic
ecological
data
G. Dowson, J. Bacteriol.
182,and
1016
(2000).
(without ecological covariates) and test on new data.
above for12th
Vibrio
specan
32. be
S. T.used,
Cowan,asin described
Microbial Classification,
Symposium
8. If one or more validated models emerge, use these to classify genetic data and to develop
the Society
for General
Microbiology,
G. C. Ainsworth,
without
making
cies of(13),
to define
populations
bacterial species concepts.
P. H. A. Sneath, Eds. (Cambridge Univ. Press, Cambridge,
a strong
theoretical commitment to either of
1962), pp. 433455.

34 mental bacteria will be useful in dissecting the

roles of the auxiliary and core genome in

References and Notes

1. J. Handelsman, Microbiol. Mol. Biol. Rev. 68, 669 (2004).

33. S. K. Sheppard, N. D. McCarthy, D. Falush, M. C. J.

Maiden, Science 320, 237 (2008).
34. A. C. Retchless, J. G. Lawrence, Science 317, 1093 (2007).

these alternatives. One clear result from all of

the studies discussed here is that the underlying
theoretical questions concerning species will
not be answered in the absence of more detailed
genetic-environmental mapping. Moreover,
some guidelines for the types of ecological
studies that will be most informative are emerging. Most important, the ecological data collected must be relevant to the niche boundaries of
the populations studied. And if genetic groups
do not map exclusively onto sampling categories (as is likely to be the case), more complex
statistical models will be needed to identify and
describe the underlying niche structure. Longitudinal studies that measure the dynamics of
ecological associations over time will also be
helpful to determine how transient natural habitats are, and thus how likely bottlenecks are to
result. Finally, whole-genome sequences from
entire populations of environmental bacteria
will be useful in dissecting the roles of the auxiliary and core genome in ecological differentiation. If after this process it emerges that some
model or models are consistently validated for
different study systems, these would inevitably
form a good basis for identifying fundamental
levels of clustering, or species.
In the foregoing we have emphasized ecotype and metapopulation models, but there are
others that deserve considerationnotably the
epidemic clonal model (42) and the impact of
phage epidemics causing classic Lotka-Volterra
boom-bust dynamics (43) illustrated in Fig.
2Dand it is possible, even likely, that more
than one of these mechanisms may be relevant
to any given problem in speciation and cluster
formation. Distinguishing among these mechanisms is the bacterial species challenge (Table
1), described in 1991 by John Maynard Smith
as follows: Ecotypic structure, hitch-hiking,
and localized recombination can explain the
observed patterns of variation. The difficulty, of
course, is that the model is sufficiently flexible
to explain almost anything. To test the hypothesis of ecotypic structure, we need to know the
distribution of electrophoretic types [i.e., genotypes] in different habitats (17).
Much research on bacterial species to date
has come from studies on pathogens, where the
correct identification of species is crucial for accurate clinical diagnoses. However, for pathogens the identification of the multiple ecological

niches within (for example) the nasopharynx or

gut is difficult, and studies of the relationships
between bacterial populations and ecology may
be more fruitful for some environmental species where the categorization of niches is a more
tractable enterprise. Hopefully, we will soon obtain richer data sets that map bacterial diversity
onto ecology and provide a way to distinguish
among various models of population differentiation and speciation, including those based on
ecotypes or metapopulations.

References and Notes

1. J. Handelsman, Microbiol. Mol. Biol. Rev. 68,

669 (2004).
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10. E. Stackebrandt et al., Int. J. Syst. Evol.
Microbiol. 52, 1043 (2002).
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12. J. C. Arbique et al., J. Clin. Microbiol. 42,
4686 (2004).
13. D. E. Hunt et al., Science 320, 1081 (2008).
14. See supplementary information in (16) for a
statistical comparison of the ecotype model
with an effective neutral model and an
implicit estimate of Ne.
15. C. Fraser, W. P. Hanage, B. G. Spratt, Science
315, 476 (2007).
16. A. Koeppel et al., Proc. Natl. Acad. Sci.
U.S.A. 105, 2504 (2008).
17. J. Maynard Smith, Proc. R. Soc. London Ser.
B 245, 37 (1991).
18. H. Ochman, A. C. Wilson, in Escherichia
coli and Salmonella typhimurium: Cellular
and Molecular Biology, F. C. Neidhart, Ed.
(ASM Press, Washington, DC, 1987), pp.
16491654.
19. J. R. Thompson et al., Appl. Environ.
Microbiol. 70, 4103 (2004).
20. M. Kimura, Trends Biochem. Sci. 1, N152
(1976).

21. R. Milkman, Trends Biochem. Sci. 1, N152

(1976).
22. K. C. Atwood, L. K. Schneider, F. J. Ryan,
Proc. Natl. Acad. Sci. U.S.A. 37, 146 (1951).
23. B. R. Levin, Genetics 99, 1 (1981).
24. F. M. Cohan, E. B. Perry, Curr. Biol. 17, R373
(2007).
25. A. Rambaut et al., Nature 453, 615 (2008).
26. R. A. Fisher, E. B. Ford, Heredity 1, 143
(1947).
27. M. Slatkin, Theor. Popul. Biol. 12, 253
(1977).
28. J. Majewski, F. M. Cohan, Genetics 152, 1459
(1999).
29. E. J. Feil, B. G. Spratt, Annu. Rev. Microbiol.
55, 561 (2001).
30. J. Majewski, F. M. Cohan, Genetics 153, 1525
(1999).
31. J. Majewski, P. Zawadzki, P. Pickerill, F. M.
Cohan, C. G. Dowson, J. Bacteriol. 182, 1016
(2000).
32. S. T. Cowan, in Microbial Classification,
12th Symposium of the Society for General
Microbiology, G. C. Ainsworth, P. H. A.
Sneath, Eds. (Cambridge Univ. Press,
Cambridge, 1962), pp. 433455.
33. S. K. Sheppard, N. D. McCarthy, D. Falush,
M. C. J. Maiden, Science 320, 237 (2008).
34. A. C. Retchless, J. G. Lawrence, Science 317,
1093 (2007).
35. K. Vetsigian, N. Goldenfeld, Proc. Natl. Acad.
Sci. U.S.A. 102, 7332 (2005).
36. A. Tuanyok et al., BMC Genomics 9, 566
(2008).
37. U. Dobrindt, B. Hochhut, U. Hentschel, J.
Hacker, Nat. Rev. Microbiol. 2, 414 (2004).
38. P. Wilmes, S. L. Simmons, V. J. Denef, J.
F. Banfield, FEMS Microbiol. Rev. 33, 109
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39. V. J. Denef et al., Environ. Microbiol. 11, 313
(2008).
40. E. Bantinaki et al., Genetics 176, 441 (2007).
41. R. A. Welch et al., Proc. Natl. Acad. Sci.
U.S.A. 99, 17020 (2002).
42. J. Maynard Smith, N. H. Smith, M. ORourke,
B. G. Spratt, Proc. Natl. Acad. Sci. U.S.A. 90,
4384 (1993).
43. K. H. Hoffmann et al., FEMS Microbiol. Lett.
273, 224 (2007).
44. We thank T. Connor and S. Deeny for
useful discussions. Supported by University
Research Fellowships from the Royal Society
(C.F. and W.P.H.), a program grant from the
Wellcome Trust (B.G.S.), grants from the
U.S. Department of Energy Genomes to Life
program (M.F.P. and E.J.A.), and the NSF/
National Institute of Environmental Health
Sciences Woods Hole Centre for Oceans
and Human Health, the NSF Biological
Oceanography Program, and the Moore
Foundation (M.F.P.).

745

35

Berlin,

nu. Rev.

9).
nndez,

4).
nsect
y, J. Rolff,
18.
004).
, Proc. R.

in
ot

hreat,
sparse
ators,
species

pot.
region,
his sets
ty

ause of
n idenal proions of
m sub-

36

L
L

processes
invoked to explain regions
Supporting must
OnlinebeMaterial
www.sciencemag.org/cgi/content/full/323/5915/782/DC1
of
high endemism (5, 6). Recent studies from
Materials and Methods
subtropical
biomes have usefully employed post
SOM Text
models of species and habihoc
palaeoclimate
Figs. S1
and S2
Table to
S1 provide insights about processes shaping
tats
References and species diversity (5, 7). Building
genetic
Audio S1 to S4
on them, we first map the palaeodistribution of
22 July 2008;species
accepted to
28 identify
November 2008
temporally stable
endemic
10.1126/science.1163583
(refugial) and unstable (recently colonized)
regions for species occurrence, which are then
validatedbiomes
with multispecies
tropical
have usefullymolecular
employeddata.
post Gohoc
ing
beyond
the
traditional
species-by-species
palaeoclimate models of species and habitats to
approach,
the molecular
analyses
contrast
the
provide
insights
about processes
shaping
genetic
data
to
the
spatially
exfit
of
assemblage-level
and species diversity (5, 7). Building on them, we
by the
plicit
demographic
scenarios suggested
first map
the palaeodistribution
of endemic
climate-based
models.
species to identify
temporally stable (refugial)
apply this
approach
to one of regions
the worlds
andWe
unstable
(recently
colonized)
for
yet notoriously
endangered
most
speciesspecies-rich,
occurrence, which
are then validated
with
Brazilian
and
understudied
ecosystems:
multispecies
molecular
data. Goingthebeyond
the
Atlantic
Originally
extending
for
traditionalrainforest.
species-by-species
approach,
the mokm2 along
thetheBrazilian
coast and
1,300,000
lecular analyses
contrast
fit of assemblagethis biome
reaching
and Argentina,
level datainto
to Paraguay
the spatially
explicit demographic
(8).
has
been reduced
to by
lessthe
than
8% of its range
scenarios
suggested
climate-based
models.
Todays
fragments
harbor one
of the
perWe apply
this approach
to one
of largest
the worlds
of endemic
species in the
world, with
centages
most species-rich,
yet notoriously
endangered
and
understudied
the of
Brazilian
Atlantic
vertebrates
still
many
species ecosystems:
and even genera
1
Museum of Vertebrate Zoology, University of California,
Berkeley, CA 947203160, USA. 2Biology Department,
Queens College, City University of New York, Flushing, NY
11367, USA. 3Departamento de Zoologia, Instituto de
Biocincias, UNESP, Rio Claro, SP 3526-4100, Brazil.
4
Departamento de Zoologia, Instituto de Biocincias,
Universidade de So Paulo, SP 055008-090, Brazil.

*To whom correspondence should be addressed. E-mail:

carnaval@berkeley.edu

6 FEBRUARY 2009

We use molecular genetic data from multiple,

largely codistributed species to test whether spatial modeling of species-specific Late Quaternary refugia sheds light on historical processes and
hence improves prediction of genetic endemism
and diversity in tropical Brazil (11). We focus
on three common species of tree frogs that are
widely distributed along the Brazilian Atlantic
forest: Hypsiboas albomarginatus, H. semilineatus, and H. faber. Given their life history
traits, amphibians are useful indicators of environmental changes through time (12). Whereas
H. albomarginatus and H. semilineatus occur in
low and mid altitudes and are mostly restricted
to the evergreen or semideciduous components
of the Atlantic Forest in eastern Brazil, H. faber
has a broader altitudinal range and also inhabits
mixed and deciduous areas, occupying interior
and coastal sites in the Atlantic Forest south to
Paraguay and Argentina (figs. S1 and S2) (13).
The comparative phylogeographic approach is
a powerful test of assemblage-scale responses
to former environmental change and thereby
provides a means for critical assessment of the
scenarios produced by modeling of species distributions under palaeoclimates (7).
The palaeomodeling method intersects
predicted species distributions under current
conditions and climatic extremes of the Late
Quaternary (6000 years before present, or 6
kybp, and 21 kybp) to predict areas of stability
(regions in which species are predicted to occupy irrespective of time period) and unstable
areas (7, 14). Because the stability maps raise
specific hypotheses about regional differences

785

(AUC) values (16) 0.968, 0.989, and 0.994;

maximum Kappa (17) 0.81, 0.925, and 0.94 in H.
albomarginatus, H. faber, and H. semilineatus,
respectively (fig. S2)]. Stability maps, depicting the intersection of distribution models for
each taxon under current, 6 kybp, and 21 kybp
climates, predict for all species a large central
refugium throughout the Late Quaternary (Bahia refugium) (Fig. 2). A second, much smaller
refugium is predicted in the northeasternmost
portion of the forest (Pernambuco refugium).
In H. faber, a third, southeastern refugium of intermediate size is also predicted (So Paulo refugium). This is not surprising, given that this
species occupies a broader environmental niche.
In contrast to the central and northern regions,
populations south of the Bahia or So Paulo
refugia appear much less stable, despite the
more extensive (preclearing) range of the forest in southern and southeastern Brazil. We hypothesize that these areas received a significant
influx of migrants from adjacent, large refugial
populations after the LGM. These palaeomodel
results are congruent with the fossil pollen record, which documents a replacement of forests
by grasslands in the southern Atlantic forest during the LGM (14, 18) and suggests the occurrence of small forest refugia in the southernmost
range of the putative Bahia refugium (19). The
results also agree generally with forest models
published previously (14), although the central
refugium extends farther south in the frog-based
models. Such differences are expected because
the forest and its associated species may differ
slightly in their climatic tolerances and realized

Distribution
Modeling

Stability Predicts Genetic Diversity in

the Brazilian Atlantic Forest Hotspot

Hypothesis
Formulation

9. J. A. Thomas, G. W. Elmes, J. C. Wardlaw, Proc. R. Soc.

in persistence
diversity,
theypost
leadhoc
to
tropical
biomesand
havehence
usefully
employed
London Ser. B 265, 1895 (1998).
10. G. W. Elmes, J. C. Wardlaw, K. Schnrogge, J. A. Thomas,
phylogeographic
predictions
for both
individual
palaeoclimate
models
of species
and habitats
to
Entomol. Exp. Appl. 110, 53 (2004).
(codistributed
taxa;
species insights
and assemblages
provide
about processes
shaping genetic
11. Materials and methods are available as supporting
driven
by
the
model
Fig.
1).
Field
sampling
is
and
species
diversity
(5,
7).
Building
on
them,
we
material on Science Online.
first
map the
palaeodistribution
endemic
and
predictions
to cover
both predictedofrefugia
12. P. J. DeVries, R. B. Cocroft, J. A. Thomas, Biol. J. Linn.
Soc. 49, 229 (1993).
species
identify colonized)
temporallyareas,
stableparticularly
(refugial)
unstableto(recently
1
2
Ana
Carnaval,
Michael
Hickerson,
Clio F. B. Haddad,3
13. F.Carolina
Roces, J. Tautz,
J. Acoust.*Soc.
Am. 109,J.3080
(2001).
and
unstable previously
(recently colonized)
regions
undersampled
areas.for
If
emphasizing
4
1
Miguel
T. Rodrigues,
14. R. Hickling,
R. L. Brown, Craig
J. Acoust.Moritz
Soc. Am. 108, 1920
species
occurrence,
which
are thencurrent
validated
with
patterns
the approach
correctly
predicts
(2000).
multispecies
molecular
Going
beyond
the
of biodiversity
at the data.
regional
scale,
species
15. H. Markl, B. Hlldobler, Behav. Ecol. Sociobiol. 4, 183
Biodiversity
hotspots, representing regions with high species endemism and conservation threat,
(1978).
traditional
species-by-species
the moshould consistently
show (i) approach,
higher genetic
dihave
globally.
Yet,
biodiversity distribution data from within hotspots are too sparse
16. H.been
Markl,mapped
Z. Vgl. Physiol.
60, 103
(1968).
lecular
analyses
contrast
the
fit of assemblageand
among
populations
in
refugia
versity
within
17. effective
H. Markl, Science
149, 1392in(1965).
for
conservation
the face of rapid environmental change. Using frogs as indicators,
level data to the spatially explicit demographic
18. D. A. Grasso,
Mori, F. Leunder
Moli, M.paleoclimates,
Giovannotti,
ecological
nicheA. models
and simultaneous Bayesian analyses of multispecies relative to unstable areas, because of long-term
scenarios
suggested
by the climate-based
A. Fanfani, Ital. J. Zool. 65, 167 (1998).
genetic
persistence
and population
structure; (ii)models.
molecular
data, we compare alternative hypotheses of assemblage-scale response to late
19. T. C. Scott-Phillips, J. Evol. Biol. 21, 387 (2008).
We apply
this
approachexpansion
to one of in
theunstable
worlds
signature
of
population
Quaternary
climate
change.
reveals
a Apollo
hotspot within the Brazilian Atlantic forest hotspot.
20. K. G. Schurian,
K. Fiedler,
Nachr.This
Entomol.
Vereins
most species-rich, yet notoriously endangered and
We show
that
the southern Atlantic forest was climatically unstable relative to the central region, areas, reflecting multispecies colonization from
14, 339
(1994).
understudied ecosystems: the Brazilian Atlantic
21.
C.
J.
Hill,
J.
Aust.
Entomol.
Soc.
32,
283
(1993).
which served as a large climatic refugium for neotropical species in the late Pleistocene. This sets adjacent refugial regions after the Last Glacial
22. D. R. Nash, T. D. Als, R. Maile, G. R. Jones, J. J. Boomsma,
Maximum (LGM, 21 kybp); (iii) absence of
new
priorities for conservation in Brazil and establishes a validated approach to biodiversity
1
Science 319, 88 (2008).
Museum patterns
of Vertebrate
Zoology, University of California,
genetic
of isolation-by-distance
in unprediction
in
other
understudied,
species-rich
regions.
2
23. P. J. DeVries, Am. Mus. Nov. 3025, 1 (1991).
Berkeley,
CA 947203160,
Biology Department,
areas,
given
that USA.
colonization
has been
stable
24. K. Fiedler, B. Hlldobler, P. Seufert, Experientia 52, 14
Queens College, City University of New York, Flushing, NY
too recent to3 permit restoration of equilibrium
(1996).
Quaternary
fluctuations
refugia models have been dismissed because of 11367, USA. Departamento de Zoologia, Instituto de
25. M. ate
A.ate
Travassos,
N. E. climate
Pierce,climate
Anim.
Behav.
60, helped
13
being described (8, 9). Our ultimate goal is to Biocincias,
Quaternary
fluctuations
and
between migration
genetic
drift (15);Brazil.
UNESP, Rioand
Claro,
SP 3526-4100,
to shape present-day diversity in temper- conflicting evidence (2, 3) or circularity in iden- 4Departamento de Zoologia, Instituto de Biocincias,
(2000).
diversity
in pinpoint regions for inventory work and habitat (iv) strong phylogeographic structure between
helpedettoal.,shape
present-day
26. N. ate
E. Pierce
Annu.
Rev.
Entomol.
47,
733
(2002).
and boreal systems (1), providing a tifying putative refugia (4), but historical pro- Universidade de So Paulo, SP 055008-090, Brazil.
boreal
systems
(1),
protection before we lose a substantial fraction refugia, reflecting assemblage-wide, long-term
27. J. C.temperate
Downey,
C.and
Allyn,
Bull. Mus.
Entomol.
14, progeneral
contextA.for
understanding
current
pat- cesses must be invoked to explain regions of
whom correspondence
be addressed.
1 (1973).
in isolated
areas. E-mail:
population
persistence should
viding
a general context for understanding cur- of described and undocumented diversity. The *To
terns
ofthank
endemism.
In
tropics,
high endemism (5, 6). Recent studies from sub- carnaval@berkeley.edu
28. We
N.ofElfferich
andthe
P. J.In
DeVries
forPleistocene
introducing
Pleis- approach differs from previous methods by diDistribution models developed under current
rent
patterns
endemism.
the tropics,
us to ant-butterfly acoustics; G. W. Elmes, J. C. Wardlaw,
tocene
refugia models have been dismissed be- rectly modeling historical processes, as opposed climatic conditions accurately predict distribuV. La Morgia, M. B. Bonsall, and referees for
of conflicting
evidence
(2, 3)for
ordesigning
circularity to observed biodiversity
(10), with
the tions2009
of each of the target species along the At- 785
cause
www.sciencemag.org
SCIENCE patterns
VOL 323
6 FEBRUARY
comments
and advice;
and M. Charles
the acousticalputative
equipment.
refugia (4), but historical aim of informing conservation.
in identifying
lantic rainforest domain [area-under-the-curve

is higherlarger
thaninthe
because of the
in the
southernmost
range by
of magnitude
critical assessment
of the scenarios
produced
by testsmall
the other
central species
(Bahia) refugium
which refugia
documents
a replacement
of forests
phylogeographic
approach
is a powerful
of forest
modeling of species
distributions
under
assemblage-scale
responses
to palaeoformer environ- grasslands in the southern Atlantic forest during relative to the less stable (southern) portion of the
climates (7). mental change and thereby provides a means for the LGM (14, 18) and suggests the occurrence of forest. Diversity of H. faber in this southern area
higher than the otherCurrent
species&because of the
the southernmost rangeMap
of ofispredicted
critical assessment
of the
scenarios preproduced by small forest refugia inSpecies
The palaeomodeling
method
intersects
of species
under palaeooccurrence
stable areas
historical climate
dicted speciesmodeling
distributions
underdistributions
current condiclimates (7).
data
Inclimatic
H. albomarginatus
andLate
H. Quaternary
faber, the
niches.
(putative refugia)
data
tions and
extremes
of the
palaeomodeling method intersects preSpecies
Map of predicted
Current &
So
Paulo
refugium
extension
the The
predicted
(6000 yearsofbefore
present,
or
6
kybp,
and
21
kybp)
occurrence
stable areas
historical climate
dicted species distributions under current condiwestward
theofand
neighboring
Cerrado
data
(putative refugia)
data
to predict into
areas
stability
(regions
which
tions
climatic extremes
of in
thebiome
Late Quaternary
reflects
overprediction
(fig.irrespective
S2)
(6000
years
present,
or 6(14).
kybp, and
species model
are predicted
tobefore
occupy
of21 kybp)
Spatially explicit hypotheses Re:
to
predict
areas
ofthrough
stability
(regions
Models
habitat
stability
time
period)ofand
unstable
areas
(7, 14). fluctuatBecausein which
species
predicted
to occupy
irrespective of
predict
patterns
of phyloing
climatesmaps
correctly
Spatially explicit hypotheses Re:
the stability
raiseare
specific
hypotheses
about
and unstable areas (7, 14). Because
rainforest
geography
in time
the period)
Brazilian
Atlantic
regional differences
in
persistence
and
hence
dithe stability maps raise specific hypotheses about
spatial-temporal patterns
(Fig.
2 and
S3
todifferences
S5). In all
species,
high
distribution of
congruence
versity,
theyfigs.
lead
to phylogeographic
predictions
regional
in persistence
and hence diof colonization
genetic diversity
across taxa
spatial-temporal patterns
levels
of individual
divergence
and
population
structure
are
for both
species
and
assemblages
(codistribution of
congruence
versity, they lead to phylogeographic predictions
and/or
vicariance
of colonization
genetic diversity
across taxa
forFig.
both1).
individual
species and
distributedacross
taxa;
Field
sampling
isassemblages
driven (corefugia
(Tamura-Nei
corrected
observed
and/or vicariance
distributed
taxa;
Fig.
1).
Field
sampling
is
driven
by the model
to coverBahia
both predicted
and Perdistances
(20):predictions
4 to 7% between
by the model
predictions
to coverareas,
both predicted
Sampling across predicted stable and unstable areas
refugia and
unstable
colonized)
nambuco
refugia,
1% (recently
between
the
nearby
Bahia
Sampling across predicted stable and unstable areas
refugia and unstable (recently colonized) areas,
particularly
emphasizing
previously
undersamSo Paulo
refugia
in
H.
faber).
Similarly,
in
and
particularly emphasizing previously undersampled
areas.
the
approach
correctly
predicts
curthereIfare
multiple,
divergent
withall
taxa
pled
areas. If the
approachclades
correctly
predicts current
patterns
of
biodiversity
at
the
regional
scale,
rent
patterns
of
biodiversity
at
the
regional
in the Bahia region, agreeing with model-based scale,
Genetic tests
of of
Assemblage-scale
Genetic
tests
Assemblage-scale
should
consistently
showarea.
(i) higher
species should
consistently
show
(i)inhigher
genetic
Descriptive
Descriptive
this
In genetic
predictions
of species
a large
refugium
stability/expansion,
hypothesis
testingtesting
stability/expansion,
hypothesis
phylogeography
diversity
within populations
and among populations
in refugia
phylogeography
diversity
within
and
among
in
refugia
divergence
times
(HABC)
H. faber, divergent clades are also represented
divergence times
(HABC)
relative
to
unstable
areas,
because
of
long-term
perrelative
to unstable
areas, because
of long-term perin
the So
Paulo
region,
of
sistence
andmatching
population predictions
structure; (ii) genetic
sigandrefugium
population
structure;
(ii)
sigin
this
area.
Allgenetic
taxain show
asistence
mid-sized
nature of population expansion
unstable areas, Fig. 1. Proposed method of biodiversity prediction. Three stages are involved: biodiversity disnaturegenetic
of population
incolonization
unstable
areas,
Fig. 1.tribution
Proposed
method
of model-based
biodiversityhypothesis
prediction.
Three stages
arehypothesis
involved:testing
biodiversity
disreflectingexpansion
multispecies
from adjacent
modeling
(top),
formulation
(middle),
and
southernmost
low
diversity
across the
reflecting
multispecies
colonization
from
adjacent
tribution
modeling
(top),
model-based
hypothesis
formulation
(middle),
hypothesis
testing
and
refugial
regions
after
the
Last
Glacial
Maximum
model
validation
(bottom).
range of the forest, an area predicted to be less
refugialbyregions
after the LastFurthermore,
Glacial Maximum
stable
the palaeomodels.
mito- model validation (bottom).
DNA (mtDNA) lineages found in this
chondrial786
6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org
refugia
(one
in
in and E). Using Bayes factor (25), we also detect
scale,
persistence
of populations
region
are
shared
with
adjacent
786
6 FEBRUARY
2009long-term
VOL 323
SCIENCE
www.sciencemag.org
H. albomarginatus and H. semilineatus, two in isolated refugial areas, as opposed to post-LGM evidence for stability in both areas under the noH. faber).
migration model [B(Z2 = 0, Z2 > 0) = 4.89], as
colonization of refugial regions.
Metrics of genetic diversity confirm the
To test for assemblage-wide colonization well as under a postisolation migration model
above patterns (Table 1). In H. albomarginatus of predicted unstable areas, we group mtDNA [B(Z2 = 0, Z2 > 0) = 4.84].
Relative to nuclear loci, mtDNA data are
and H. semilineatus, genetic diversity (21) is an sequences from the southernmost refugial sites
order of magnitude larger in the central (Bahia) [population 1 (Fig. 3A)] and from localities in more variable and readily collected and often
refugium relative to the less stable (southern) unstable areas south of the refugium [population provide key insights into biological response
portion of the forest. Diversity of H. faber in 2 (Fig. 3A)] to contrast two alternative historical to environmental modification (1). Although
this southern area is higher than the other spe- models across the three codistributed species, single-locus inference can be imprecise in the
cies because of the presence of two lineages that while allowing the taxon-specific demographic face of coalescent variance and the possibility of
co-occur in the adjacent refugia. In all species, parameters to vary. In H1, the long-term persis- selection (26), our method benefits from a mulaverage net nucleotide differences across locali- tence model, two contemporary populations split titaxon approach, while explicitly accounting
ties (22) reflects high geographic structure with- from an ancestral population prior to the LGM for the stochasticity of a single-locus coalescent
in refugia (2.6 to 6.2% divergence). In contrast, (120,000 to 1.2 million years before present, or across taxa. Combining data sets from several
sites located outside (south of) the refugia are Mybp, Fig. 3A). In H2, the recent colonization codistributed groups into a single hierarchical
genetically more similar to each other, although model, population 2 is modeled as being colo- Bayesian analysis allowed us to estimate conto a lesser extent in H. faber (0.1 to 1.6%). Sig- nized from refugial population 1 subsequent to gruence across species, while borrowing strength
natures of population expansion (23) are found the LGM (0 to 20 kybp; Fig. 3A). The results from the full comparative phylogeographic samin the unstable area for H. albomarginatus and indicate that all three species colonized the ple (24). This can translate into higher analytical
H. faber, as well as in the Bahia refugium area southern (unstable) areas after the LGM (Z2 = 3, power and be more informative than qualitative
for H. faber and H. semilineatus. The lack of the number of species evolved under H2), even comparisons of species-specific analyses. By
signature of population expansion in the south- when allowing for postisolation migration (Fig. capturing the historical signal that emerges from
ernmost localities of H. semilineatus may reflect 3, B and C). When Bayes factor is used (25), larger, combined multispecies molecular data
low statistical power because of the exception- there is strong support for recent colonization in sets, HABC will offer the possibility of looking
ally low levels of diversity observed in this spe- all three species (Z2 = 3) under the no-migration at patterns of historical community assembly in
cies. As predicted, isolation by distance is not model [B(Z2 = 3, Z2 < 3) = 35.16], and moderate codistributed nonmodel organisms for which
observed in unstable regions, but is detected support under a postisolation migration model barcode-type DNA sequence information (e.g.,
within refugial areas for H. albomarginatus and [B(Z2 = 3, Z2 < 3) = 5.70].
mtDNA data) can be feasibly collected.
Using the same framework to test for longCollectively, the results identify the central
H. faber.
The hierarchical approximate Bayesian com- term persistence of refugial populations, we region as a hotspot within the Atlantic rainforest
putation (HABC) method (24) allows us to use compare mtDNA sequences between the pre- hotspot and a refuge for biodiversity during
data from all three species at once to test for dicted Pernambuco refugium [population 1 (Fig. climatic extremes of the Late Pleistocene.
assemblage-wide responses to Late Quaternary 3A)] and adjacent (northern) populations from This is not to say that southern areas entirely
climate change. These analyses support both the Bahia refugium [population 2 (Fig. 3A)] to lacked forested habitats in the late Pleistocene:
model-driven hypotheses of (i) simultaneous, contrast alternative historical models H1 and H2. The existence of species and genera endemic
multispecies colonization of unstable areas from In this case, the HABC results infer long-term to the southern forests (27), as well as some
adjacent refugial populations since the LGM, persistence of populations in isolated refugia for palaeoecological and genetic evidence (28),
as opposed to long-term persistence of popu- all three species (Z2 = 0, i.e., Z1 = 3), even when offer evidence to the contrary. Rather, the
lations in unstable areas, and (ii) assemblage- allowing for postisolation migration (Fig. 3, D phylogeographically validated palaeomodels
Model
Validation

s hiermimicry
lack the
and of.
species
li (12):
studied
nsals or
with ants
e acouslthough
s attracts
s to siga basal
t expect
nea.
ecies of
icularly
Diptera,
ays the
nts hicue has
ate and

22 July 2008; accepted 28 November 2008

10.1126/science.1163583

Diversity
Distribution
Modeling
Diversity

REPORTS

Audio S1 to S4

Hypothesis
Formulation

7. K. Schnrogge et al., J. Chem. Ecol. 30, 91 (2004).

8. T. Akino, J. J. Knapp, J. A. Thomas, G. W. Elmes, Proc. R.
Soc. London Ser. B 266, 1419 (1999).

Model
Validation

is admitted and accepted as a member of a host

society, it mimics adult ant acoustics (particularly queens) to advance its seniority toward the

37

presence of two lineages that co-occur inAthe ad-

6.2% divergence). In contrast,

B sites located

population expansion
(23) are found in the
C

refugial
(stable)
versus
unstable
areasaverage
unstable
area
H. albomarginatus
and H. faber,
refugiaare
aregenetically
geneticallyunstable
jacent refugia.
all species,
average
net nuclearea for
H. for
albomarginatus
and H. faber,
outside(south
(south of)
of) the
the refugia
jacent In
refugia.
In
all species,
net nucle- outside
in
thedifferences
Brazilian
Atlantic
rainforest.
as well
as in
the refugium
Bahia refugium
area
for H. faber
similar
althoughto to
a lesseras well
otide
across across
localities
(22) (22)
reflects
as in the
Bahia
area for H.
faber
more
similartotoeach
each other,
other, although
a lesser
otide differences
localities
reflects more
(Top)
Species-specific
stability
maps;
H. semilineatus.
The lack
of lack
signature
of
extent
faber (0.1
(0.1 to
of ofand and
high geographic
structure
within
refugia
H. semilineatus.
The
of signature
of
ininH.H.faber
to 1.6%).
1.6%).Signatures
Signatures
high geographic
structure
within
refugia
(2.6 (2.6
to to extent
Pernambuco
modeled refugia in black. (A) H.
refugium
albomarginatus, (B) H. semilineatus,
Fig. 2. diversity
Genetic diversity
in putative
C
Fig.H.2.faber.
Genetic
in putative
A
B
(C)
Note
the
absence
of
large
C
B
refugial (stable) versus unstable areas A
Bahia refugium
refugialregions
(stable)
unstable
areas
stable
the southern
portion
in theinversus
Brazilian
Atlantic
rainforest.
*
in the
the forest
Brazilian
Atlantic
rainforest.
*
of
of the Bahia
andmaps;
(Top)(south
Species-specific
stability
(Top)Paulo
Species-specific
stability
Pernambuco
modeled
refugia
in black.
So
refugia)
relative
tomaps;
the(A) H.
refugium Pernambuco
albomarginatus,
(B) H.
semilineatus,
modeled
refugia
in areas.
black.
(A)
H.
central and
northern
Asterisks
S o Paulo refugium
refugium
(C) H. faber.
the
absencethe
of large
albomarginatus,
(B) Note
H. semilineatus,
denote
refugia
inferred
beyond
Bahia refugium
stable
regions
in the southern
portion
(C)
H. faber.
Note
the
absence
of
large
current
ranges
of
the
target
species.
5.4%
*
*
of theinforest
(south of the
Bahia and
Bahia refugium
stable regions
the southern
portion
Symbols
indicate
localities
sampled
So Paulo
refugia)
relativeforto the
*
*
of
the
forest
(south
of
the
Bahia
and
molecularcentral
analysis.
bar, areas.
400 km.
andScale
northern
Asterisks
S o Paulo refugium
So PauloThe
refugia)
relative
the the
(Bottom)
50%
majority-rule
condenote
refugia
inferredtobeyond
central
and
northern
areas.
Asterisks
current ranges
of the target
species.
sensus Bayesian
phylogenetic
trees,
5.4%
7%
S o Paulo refugium
7.8%
Symbols
indicatefrom
localities
denote with
refugia
inferred
beyond
the for
rooted
sequences
thesampled
othmolecular
Scale
bar, 400 km.
current
of analysis.
thespecies
target
species.
er two ranges
congeneric
studied
5.4%
(Bottom)localities
The 50%sampled
majority-rule
Symbols
for con(root
notindicate
shown).
Thick
internodes
de5.3
sensus Bayesian phylogenetic trees,
7%
molecular
analysis.
Scale bar,
400 km.
note clades
withwith
posterior
probability
7.8%
4%
5.8%
rooted
sequences
from the oth(Bottom)
The
50%
majority-rule
congreater
than
Percentages
indicate
er 90%.
two
congeneric
species
studied
sensus
Bayesian
trees, deTamura-Nei
corrected
distances
(root
not phylogenetic
shown).
Thick between
internodes
7%
5.3
7.8%
rooted(20).
with
the probability
othnotesequences
clades withfrom
posterior
4%
clades
5.8%
5.6%
greater than 90%.
Percentages
indicate
er two congeneric
species
studied
Tamura-Nei
corrected
distancesdebetween
(root not shown).
Thick
internodes
5.3
clades
note clades
with(20).
posterior probability
4%
5.8%
5.6%
greater than 90%. Percentages indicate
Tamura-Nei corrected distances between
clades (20).
5.6%

Mybp, Fig. 3A). In H2, the recent colonization

model, population 2 is modeled as being colonized from refugial population 1 subsequent to

coalescent variance and the possibility of selection (26), our method benefits from a multitaxon
approach, while explicitly accounting for the

southern regions. This reassures us that the processes uncovered by the amphibian data may be
generalized to and help to explain patterns of

Fig. 3. HABC analyses.

(A) Simulated models
H1 (long-term persistence) and H2 (recent
colonization). In both
cases, each species was
modeled as two contemporary populations
with mutation-drift parameters q1 and q2 that
split from an ancestral
population at a time t in
the past. Ancestral population sizes are represented by (qt)1 and (qt)2;
ybp, years before present. (B to E) Hyperposterior (bars) and hyperprior
(dashed) densities of Z2
(number of species evolved
under H2) given data from
three codistributed frog
species. (B) and (C) Models of refugial sites (population 1) and unstable,
southern areas (population 2). (D) and (E) Models
of Pernambuco refugium
(population 1) and Bahia
refugium (population 2). (B) and (D) Postisolation migration not included in model; (C) and (E) postisolation migration included in model.
At a broader level, the congruence between

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providing access to collections MNRJ and

MZUSP; O. Peixoto, M. Gomes, A. Muri, R.
Kautskyi, S. Lima, E. Santos, J. S. Filho, J.
V. Filho, G. Barros, J. Queiroz, R. Arajo, L.
Japp, H. Japp, J. Giovanelli, J. Alexandrino,
L. Toledo, O. Arajo, G. Egito, J. Zina, D.
Loebmann, D. Pavan, R. Amaro, V. Verdade,
F. Curcio, M. Dixo, and J. Cassimiro for field
work assistance; W. Monahan and R. Hijmans
for discussions about the modeling work; L.
Smith and D. Turong for DNA-sequencing
assistance; R. Pereira, R. Damasceno, S.
Rovito, J. Kolbe, S. Singhal, R. Puschendorf,
and A. Pounds for discussions about earlier
versions of the manuscript. Funding was
provided by the NSF (awards DBI 0512013
to A.C.C., DEB 0743648 to M.J.H., DEB
416250 and DEB 0817035 to C.M.), Fundao
de Amparo Pesquisa do Estado de So Paulo
and Conselho Nacional de Desenvolvimento
Cientfico e Tecnolgico (grants to C.F.B.H.
and M.T.R.). Sequences are deposited in
GenBank (FJ502639-FJ502822). A.C.C. and
C.M. designed the study; A.C.C., C.F.B.H.,
and M.T.R. collected the data; A.C.C., C.M.
and M.J.H. analyzed the data; A.C.C. wrote
the paper. All authors discussed the results
and commented on earlier versions of
the manuscript.

788 model-based demographic hypotheses

6 FEBRUARY
2009
VOL 323Museum
SCIENCE
32. We thank U. Caramaschi and H. Zaher for
2008 (American
of Naturalwww.sciencemag.org
History,
and
q, and average D values of the former were obtained not only from the total

Table 1. Population genetic summary metrics used in model validation. n,

Table 1. Population genetic summary metrics used in model validation. n,
Sample size;
S, number
of segregating
sites. sites.
The diversity
parameter
Sample
size; S, number
of segregating
The diversity
parameterq qand
andmean
mean
Da across Dlocalities
are given per base pair (bp). Hs test (23) is used to detect
a across localities are given per base pair (bp). Hs test (23) is used to detect
populationpopulation
expansion.
BA, Bahia;
SP, So
refugia.
Because
expansion.
BA, Bahia;
SP, Paulo
So Paulo
refugia.
Becausepredicted
predicted
refugia
oftenthan
larger
than predicted
unstable
(recently
colonized)areas,
areas,n,
n, S,
S,
refugia were
oftenwere
larger
predicted
unstable
(recently
colonized)

a
of the former were obtained not only from the total
q, and average Da values
numberofofsamples,
samples,
all possible
combinations
of spatially
number
but but
also also
from from
all possible
combinations
of spatially
contiguouslocalities
localities
distributed
the geographic
of the unstable
contiguous
distributed
withinwithin
the geographic
extensionextension
of the unstable
area.Parentheses
Parentheses
encompass
minimum
and maximum
values
from subsamples.
area.
encompass
minimum
and maximum
values from
subsamples.
valuesininbold
bold
highlight
statistical
significance
0.05 probability
level.
PPvalues
highlight
statistical
significance
at 0.05 at
probability
level.

SS n,
Table 1. Population
genetic summary
metrics usednin nmodel validation.
Species Species
Area Area
(min.;
max.) (min.;
max.)
Sample size; S, number of segregating sites. The diversity
parameter
q(min.;
and mean
(min.;
max.)
max.)

qq
Mean
Hs
corr.
a
ofDthe
were obtained
notMantels
onlycoef.
from
the coef.
total
q, and average
Da values
Mean
Dformer
Hs Mantels
corr.
a
(min.;
max.)
value)
(P value) (P value)
number
ofmax.)
samples,(min.;
but
alsomax.)
from(Pall
possible
of spatially
(min.;max.)
(min.;
(P value)combinations

albomarginatus
(BA) (bp). Hs test 36
D across H.
localities
are given per Stable
base pair
(23) is used to 207
detect
H.a albomarginatus
Stable (BA)
36
207155)
(970 bp)
(13; 23)
(81;
population expansion.
BA, Bahia; SP, So Paulo refugia.
Because predicted
(970 bp)
(13;
23)
(81;
155)
Unstable
refugia were often larger than predicted
unstable (recently27
colonized) areas,22n, S,

0.076 localities distributed

0.062 within20.546
0.499 of the unstable
contiguous
the geographic extension
0.076
0.062
20.546 (0.001) 0.499
(0.034;
0.072) encompass
(0.020; 0.082)
area.
Parentheses
minimum(0.141)
and maximum values
from subsamples.
(0.034;
(0.020;
0.082)
(0.001)
0.003
0.001
11.498(0.141)
P values
in0.072)
bold highlight
statistical
significance
at 0.050.140
probability
level.

Unstable(south of BA)
27
22
0.003
0.001
11.498 (0.580) 0.140
(0.004)
H. semilineatus
Stable
(BA)
0.031
0.036
0.054
(south
of BA)
(0.004)
(0.580)
n 28
S71
q
Mean Da 17.778
Hs
Mantels
corr. coef.
Species
Area
(718 bp)
(6;
13)
(14;
58)
(0.009;
0.034)
0.041)
H.
semilineatus
Stable
(BA)
71max.)
0.031
0.036
17.778
(min.;28
max.)
(min.;
(min.;
max.) (0.007;
(min.;
max.) (0.029)
(P
value) (0.460) (P0.054
value)
Unstable
15
0.0030.034)
0.004 0.041) 0.114(0.029)
0.436 (0.460)
(718 bp)
(6; 13)
(14; 958)
(0.009;
(0.007;
H. albomarginatus
Stable (BA)
36
207
0.076
0.062
20.546 (0.248) 0.499
(south of BA)
(0.357)
Unstable
15
9
0.003
0.004
0.114
0.436
H. faber
Stable (BA)
28
0.0180.072)
0.026 0.082)38.111(0.141)
0.803 (0.001)
(970 bp)
(13; 23)
(81; 94
155)
(0.034;
(0.020;
(south of BA)
(0.357) (0.0003) (0.248)
(771 bp)
(13;
23)
(42;
80)
(0.012;
0.022)
(0.001;
0.044)
(0.003)
Unstable
27
22
0.003
0.001
11.498
0.140
H. faber
Stable Stable
(BA) (SP)
28 15
94
0.018
0.026
0.803
48
0.023
0.028
5.98138.111
0.305 (0.580)
(south of BA)
(0.004)
(771 bp)
(13; 23)
(42; 80)
(0.012; 0.022)
(0.001; 0.044) (0.115)(0.003) (0.221) (0.0003)
H. semilineatus
Stable (BA)
28
71
0.031
0.036
17.778
0.054
40
0.015
0.016
13.2555.981
0.0001 0.305
Stable Unstable
(SP)
15 18
48
0.023
0.028
(718 bp)
(6; 13)
(14; 58)
(0.009; 0.034)
(0.007; 0.041)(0.014)(0.029) (0.456) (0.460)
(south of SP)
(0.115)
(0.221)
Unstable
15
9
0.003
0.004
0.114
0.436
Unstable
18
40
0.015
0.016
13.255
0.0001
(south of BA)
(0.357)
(0.248)
(south of SP)
(0.014)
(0.456)
H. faber
Stable (BA)
28
94
0.018 6 FEBRUARY 0.026
38.111
0.803
www.sciencemag.org
SCIENCE
VOL 323
2009
787
(771 bp)
(13; 23)
(42; 80)
(0.012; 0.022)
(0.001; 0.044)
(0.003)
(0.0003)
Stable
48 related groups
0.023
0.028 in this region
5.981relative to the
0.305
much more distantly
presented here show that
the (SP)
central
region 15
estation
more ex- 787
www.sciencemag.org
SCIENCE
VOL 323of Atlantic
6 FEBRUARY
2009
(0.115)
(0.221)
had much higher stability relative to the south. forest endemics.
tensive forests in So Paulo and southern Brazil
40 efforts, molecular
0.015 studies, (9,
0.016
13.255
0.0001
diversity
Forest lizards (14, 29) andUnstable
birds (30) also show 18 Because collection
31). Not only
could much unique
(south ofofSP)
(0.014)
(0.456)could
high diversity in the central portion
the biome and conservation priorities have been heavily be lost, but ongoing
habitat destruction
relative to southern areas, and provide evidence biased toward southern and southeastern Brazil quickly erase the signature of the historical
for population expansion in southern regions. (8, 9, 31), we predict that genetic diversity and processes that led to it, preventing a full underwww.sciencemag.org
SCIENCE
VOL corridor
323 6ofFEBRUARY
2009
in the central
the standing
This reassures us that the processes uncovered
of the mechanisms underlying local en- 787
narrow endemism
by the amphibian data may be generalized to biome have been substantially underestimated. demism and, therefore, impeding more effective
and help to explain patterns of diversity in other, This is serious, given the higher rate of defor- conservation measures.

38

joint, multispecies analyses of mtDNA diversity

shows that palaeoclimatic niche models and
assemblage-scale molecular genetic analyses
can be used to forecast spatial patterns of
diversity in poorly explored, highly threatened
ecosystems. In a world of ever-accelerating
environmental changes, this approach can help
to guide research and conservation in other
global hotspots or similarly complex tropical
ecosystems.
References and Notes

1. G. Hewitt, Nature 405, 907 (2000). [CrossRef]

2. F. E. Mayle, D. J. Beerling, W. D. Gosling, M.
B. Bush, Philos. Trans. R. Soc. London B Biol.
Sci. 359, 499 (2004).
3. E. P. Lessa, J. A. Cook, J. L. Patton, Proc.
Natl. Acad. Sci. U.S.A. 100, 10331 (2003).
4. B. W. Nelson, C. A. C. Ferreira, M. F. da
Silva, M. L. Kawasaki, Nature 345, 714
(1990).
5. C. H. Graham, C. Moritz, S. E. Williams,
Proc. Natl. Acad. Sci. U.S.A. 103, 632 (2006).
6. W. Jetz, C. Rahbek, R. K. Colwell, Ecol. Lett.
7, 1180 (2004).
7. A. Hugall, C. Moritz, A. Moussalli, J. Stanisic,
Proc. Natl. Acad. Sci. U.S.A. 99, 6112 (2002).
8. L. P. C. Morellato, C. F. B. Haddad,
Biotropica 32, 786 (2000).
9. M. T. Rodrigues, Conserv. Biol. 19, 659
(2005).
10. C. Kremen et al., Science 320, 222 (2008).
11. Materials and methods are available as
supporting material on Science Online.
12. M. B. Arajo et al., Ecography 31, 8 (2008).
13. D. R. Frost, Amphibian Species of the World:

14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.

28.
29.
30.
31.

Supporting Online Material

www.sciencemag.org/cgi/content/
full/323/5915/785/DC1
Materials and Methods
Figs. S1 to S6
Tables S1 and S2
References
8 October 2008; accepted 9 December 2008
10.1126/science.1166955

39

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