+

Robert E. Ricklefs

The Economy of Nature, Fifth Edition

Chapter 20: Coevolution

and Mutualism
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Introduction

 The rabbit/myxoma story:

 rabbits are not native to Australia; a few rabbits were
introduced to a ranch in Victoria, Australia, in 1859
 within a very few years, hundreds of millions of rabbits
ranged throughout the continent, destroying
pasturelands and threatening wool production
 the myxoma virus, introduced in 1950 and spread by
mosquitoes, proved to be an effective biological
control agent, killing 99.8% of infected rabbits
 later outbreaks of the virus were less effective - why?
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Evolution of Resistance in Rabbits

 Decline in lethality of the myxoma virus in

Australia resulted from evolutionary
responses in both the rabbit and the virus
populations:
 geneticfactors conferring resistance to the
disease existed in the rabbit population prior to
introduction of the myxoma virus:
 the myxoma epidemic exerted strong selective pressure
for resistance
 eventually most of the surviving rabbit population
consisted of resistant animals
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Evolution of Hypovirulence in
Myxoma Virus
 Decline in lethality of the myxoma virus in
Australia resulted from evolutionary
responses in both the rabbit and the virus
populations:
 less virulent strains of virus became more prevalent following
initial introduction of the virus to Australia:
 virus strains that didn’t kill their hosts were more readily
dispersed to new hosts (mosquitoes bite only living rabbits)
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The Rabbit-Myxoma System Today

 Leftalone, the rabbit-myxoma system in

Australia would probably evolve to an
equilibrial state of benign, endemic disease, as
in South America:
 pest management specialists continue to introduce
new, virulent strains to control the rabbit population

 Contagious diseases spread through the

atmosphere or water are less likely to evolve
hypovirulence, as they are not dependent on
their hosts for dispersal.
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Coevolution

 When populations of two or more species

interact, each may evolve in response to
characteristics of the other that affect its
own evolutionary fitness. This process is
referred to as coevolution:
 plants
and animals employ structures and
behaviors to obtain food and to avoid being
eaten or parasitized:
 much of this diversity is the result of coevolution: natural
selection on the means of food procurement and escape
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Coevolution is mediated by
biological agents.
 The evolutionary effects of biological
agents are unlike those of physical factors
in two important ways:
 biological factors stimulate mutual evolutionary
responses; adaptations of organisms in response
to changes in the physical environment have no
effect on that environment
 biological agents foster diversity of adaptations
rather than promoting similarity
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Convergence

 In
response to biological factors, organisms
tend to diversify:
 organisms specialize, approaching feeding,
avoidance of predators and mutually beneficial
arrangements in unique ways

 In
contrast, organisms responding to similar
physical stresses in the environment tend to
evolve similar adaptations:
 this familiar process is known as convergence
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Identifying Coevolutionary
Responses
 Coevolutionrefers strictly to reciprocal
evolution between interacting populations:
 the evolution of strong jaws and associated
muscles by hyenas to crack the bones of their
prey is not coevolutionary, because the bones of
the prey have not evolved to resist being eaten
 the evolution of the ability of an herbivore to
detoxify substances produced by a plant
specifically to deter that herbivore is
coevolutionary
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Antagonists evolve in response to

each other.
 Charles Mode coined the term coevolution
in a 1958 article in Evolution:
 Mode’s emphasis was on the development of
mathematical models to understand mechanisms
for the continual evolution of host and pathogen
to evolutionary changes in the other:
 responses of each organism to the other result in a
continual cycling of virulent/avirulent pathogens and
susceptible/resistant hosts
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The Contribution of Ehrlich and

Raven
 In
a 1964 article in Evolution, Paul Ehrlich
and Peter Raven placed coevolution in a
more ecological context:
 they emphasized empirical patterns, observing
that closely related groups of butterflies tend to
feed on closely related species of tropical vines,
suggestive of a long evolutionary history
together:
 coevolution involved the abilities of butterflies to tolerate
the particular chemical defenses of their hosts
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Coevolution reveals genotype-

genotype interactions.
 Coevolution presupposes that each
population contains genetic variation for
traits that influence their interaction:
 studies of coevolution between wheat and wheat
pathogens (teliomycetid fungi causing rusts)
have revealed genotype-genotype interactions
affecting fitnesses of host and pathogen
 parallel genetic variation in local populations of
scale insects and individual ponderosa pine
hosts may also represent a genotype-genotype
interaction
+Consumers and resources can achieve an 13

evolutionary equilibrium.

A simple model relates the rate of evolution

of consumer and resource to the efficiency
with which the consumer exploits the
resource:
 theconsumer has a decreasing function of
evolutionary rate with increasing exploitation:
 as the prey population is reduced, selective value of
further increases in predator efficiency is also reduced
 theresource has an increasing function of
evolutionary rate with increasing exploitation:
 the selective value of adaptations to avoid predation
increase
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Evolutionary Equilibrium and the

Red Queen
 Thesimple model of changing rates of
evolution of consumer and resource
suggests a stable equilibrium at which the
rates of evolutionary change of consumer
and resource are equal, and the rate of
exploitation remains constant:
 this
situation is essentially a stalemate in the
evolutionary process, as predicted by the Red
Queen hypothesis
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Competitive ability exhibits

genetic variation.
 Competitive ability should be subject to coevolutionary
change:
 competitive ability cannot be detected by examining traits of
individuals, but can be inferred from the outcome of competition
 experiments conducted by Ayala demonstrate clearly the
evolution of competitive ability in populations of fruit flies grown
under competitive situations
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Interspecific competitive ability

evolves rapidly at low density.

 Sparsepopulations can evolve interspecific

competitive ability more rapidly than dense
populations. Why?
 perhaps different and conflicting adaptations
determine the outcome of intra- and interspecific
competition
 if so, selection for increased interspecific
competitive ability will be stronger in the rarer of
two competitors
 as shown by experiments conducted by Ayala
and Pimental, this process can result in a sudden
reversal in competitive superiority
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Traits of competing populations

may diverge.
 Ifcompetition is a potent evolutionary force,
competitors should have shaped each
other’s adaptations:
 however, observations that related species living
together differ in their use of resources is not
sufficient evidence for evolution of such
differences as the result of competition
 a way around this objection is to compare species where
they live apart (allopatric populations) and together
(sympatric populations)
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Character Displacement

 Ifcharacter traits of two closely related species

differ more in sympatric regions than in
allopatric regions, this pattern may have arisen
from strong selective pressure for divergence
in sympatry, a process called character
displacement:
 ecologists disagree on the prevalence of character
displacement in nature
 patterns consistent with the operation of character
displacement have been observed among Darwin’s
finches of the Galápagos Islands
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Mutualists have complementary

functions.
 Interactionsbetween species that benefit
both participants, called mutualisms, can
also lead to coevolution:
 each party is specialized to perform a
complementary function for the other
 a highly coevolved mutualism is seen in lichens,
partnerships between algae and fungi:
 such intimate associations, in which the members form a
distinctive entity, are examples of symbioses
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Trophic Mutualism

 Trophic mutualisms usually involve

partners specialized for obtaining energy
and nutrients:
 typically
each partner supplies a limiting nutrient
or energy source that the other cannot obtain by
itself
 examples include:
 Rhizobium and plant roots that form nitrogen-fixing root
nodules
 cellulose-digesting bacteria in the rumens of cows
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Defensive Mutualism

 Defensive mutualisms involve species

that receive food or shelter from their
partners in return for a defensive function:
 thedefensive function may protect one partner
against herbivores, predators, or parasites
 examples include cleaner fish and shrimp in
marine ecosystems
 cleaners remove parasites from other fish and benefit
from the food value of the parasites removed
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Dispersive Mutualism

 Dispersive mutualisms involve animals

that:
 transport pollen in return for rewards such as
nectar:
 these mutualisms tend to be more restrictive
(specialized) as it is in the plant’s interest that pollen be
transferred to another plant of the same species
 transportand disperse seeds in return for the
nutritional value of fruits or other structures
associated with seeds:
 these mutualisms tend not to be restrictive, with
dispersers usually consuming a variety of fruits and one
kind of fruit being eaten by many dispersers
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Coevolution involves mutual

evolutionary responses.
 Coevolution applies only to reciprocal evolutionary
responses between pairs of populations.

 The term coevolution has sometimes been used broadly to

describe the close association of certain species and groups
of species in biological communities. Are these examples of
coevolution?
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Are close associations

coevolutionary?
 Do pairs of species undergo reciprocal evolution or do
“coevolved” traits arise as responses of populations to
selective pressures exerted by a variety of species, followed
by ecological sorting?

 Are species organized into interacting sets based on their

adaptations, coevolved or not?
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Coevolution in ants and aphids?

 Consider the mutualism (on ironweed

plants) in which various species of ants
protect aphids and leafhoppers and receive
nutritious honeydew in return:
 smaller ants (Tapinoma) tend to protect aphids
and larger ants (Myrmica) tend to protect
leafhoppers
 the two genera of ants rarely co-occur on one
plant

 Is this mutualism coevolved?

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Coevolution in ants and aphids?

 The ant-aphid-leafhopper mutualism has all the elements

expected of coevolution.

 Can we be sure the adaptations of the various parties

evolved in response to each other?
 we cannot be sure this is a coevolutionary situation because
alternative explanations for the various features of this mutualism
exist...
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Coevolution in ants and aphids?

 Mostinsects that suck plant juices produce large

quantities of nutritious excreta.

 Antsare voracious generalists that are likely to

attack any insect they encounter.

 The association of different genera of ants with

different honeydew sources may simply reflect
different sizes and levels of aggression, evolved in
response to unrelated environmental factors.

 Antsmay fail to attack aphids and leafhoppers

because ants have evolved to protect other nectar
sources, such as flowers and specialized nectaries.
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The Yucca Moth and the Yucca

 Yuccas (genus Yucca) and yucca moths (genus Tegeticula) are

involved in mutually beneficial and obligatory relationships
that have been carefully studied:
 the approach of phylogenetic reconstruction has been used to
address the coevolutionary questions surrounding this mutualism
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Details of the Yucca/Yucca Moth

Mutualism
 The yucca/yucca moth relationship is obligatory
(the moth larvae have no other food source and the
yucca plants have no other pollinator):
 adult female yucca moths carry balls of pollen between
yucca flowers by means of specialized mouthparts
 during pollination, the female moth deposits eggs in the
ovary of the yucca flower
 after the eggs hatch, the developing larvae feed on some of
the developing yucca seeds, not exceeding 30% of the
seed crop
 the yucca exerts selective pressure on the moths (through
abortion of heavily infested fruits) to limit moth genotypes
predisposed to lay large numbers of eggs (cheaters)
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Is the Yucca/Yucca Moth Mutualism

Coevolutionary?
 Many aspects of the mutualism are present
in the phylogenetic lineage of
nonmutualistic moths within which
Tegeticula evolved:
 many of of the adaptations (such as host
specialization and mating on the host plant)
appear to have been present in the moth lineage
before the establishment of the mutualism itself,
evidence for preadaptation
 what appear to be coevolved traits may have
been preadaptations that were critical to
establishment of the mutualism in the first place
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Summary 1

 Interactionsamong species are major

sources of selection and evolutionary
response.
 Coevolution is the interdependent evolution
of species that interact ecologically.
 Evidence of evolutionary changes in
consumer-resource systems comes from
studies of host-parasitoid interactions.
 Studies
of pathogens of crop plants have
revealed the genetic basis for virulence and
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Summary 2

 Predatorsand prey can achieve an

evolutionary equilibrium.
 Competition can exert strong selective
pressure on competitors. One
consequence of such selection may be
character displacement.
 Mutualisms are relationships between
species that benefit both.
 Mutualisms may be trophic, defensive, or
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Summary 3

 Phylogeneticanalysis allows us to infer the

evolutionary history of interspecies
interactions
A carefully studied case of an obligatory
mutualism involves yuccas and their
pollinators, yucca moths.
 Identification of coevolved relationships is
difficult, and preadaptations may
complicate evolutionary interpretation.