Sperm

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1986. 31 :297-320
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SPERM UTILIZATION IN
SOCIAL INSECTS
Robert
E.
Page, Jr.
Department of Entomology, Univers ity of W isconsin, Madison, W isconsin
53706
Mating behavior and patterns of sperm utilizat ion have become important
issues in the study of social insect s since the important work of Hamilton
(56--58) and Parker ( 1 14) . Hamilton stressed the importance of sperm utiliza
tion in the context of how the genetic relationships of interacting individuals
affect the evolution of altruism QY k in selection; Parker discussed the effect s of
mat ing and sperm competit ion on the evo lution of insect mat ing systems. In this
review I discuss aspect s of mat ing behavior, sperni acquisition, and sperm
utilizat io n in both context s . I deal exclusively with this top ic as it pertains to the
eusocial Hymenoptera (ants, bees, and wasps). Although the Isoptera (ter
mites) are the o nly other insect order with eusocial representatives I have
emphasized the Hymenoptera because this order has been the subject of the vast
majority of social insect studies. In addition, I concentrate on the honey bee
(Apis mellifera), t he most diligently studied of all social insect s, with the
specif ic objective of covering one group in det ail .
MATING BEHAVIOR
Recent reviews have discussed mat ing behav ior and sperm utilizat ion in the
context of the evolut ion of insect mating systems (2,38, 1 14, 137, 143) and the
effect of polyandry ( multiple mat ing by females) on social evolut ion (3, 4,22,
28, 37, 57, 58, 72, 80, 106, 129, 130 , 139, 148) . Conclusions about the
expected and observed occurrences of single and mult iple mat ing of solitary
and eusocial hymenopteran females are highly varied. In this sect ion I present
evidence f or monoandry (single mat ing by females) and polyandry, evaluate
the different experimental methods used, examine trends and biases of reports
in the literature, and discuss current hypotheses f or the evolut ion of mat ing
behavior.
297
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Evidence for Polyandry and Monoandry

Reports of polyandry are common for eusocial wasp s (i .e . reports for 5 species
in 3 genera), bees (8 species , 4 genera), and ants (32 species, 13 genera), as are
reports of monoandry (3 species, 2 genera; 6 species, 2 genera; and 12 species ,
8 genera, respectively) . Overall , the bias i s for polyandry with 45 specie s (20
genera), compared to monoandry with 21 species ( 12 genera) (T able 1 ) . The
same trends are noted for non-eusocial Hyme noptera with 6 monoandrous
specie s (6 genera) and 18 p olyandrous species ( 14 genera) reported (22, 106).
Each of the four methods represented in Table 1 has an expected bias toward
the deter mination of either monoandry or polyandry:
OBSERVATION
Observational data are likely to be biased toward reports of
multiple mati ng because single matings are more difficult to verify . Observa
tions of multiple copulations, however , do not automatically imply multiple
inse mi nations . Observational data must be used in conjunction with other
methods to be reli able .
Di ssection can be effective for e stimating the minimum number

of males i nseminating female s . It is not effecti ve for estimating the actual or
effective number of mate s or for determining single i nsemination. The usual
method is as follows: (a) Females are cap tured, their spermathecae (or enti re
genital tracts) are di ssected, and the number of spermatozoa contained in the m
are counted. (b) Males are collected, their seminal vesicles (and sometimes the
testes) are dissected, and the number of spermatozoa are counted. (c) Multiple
i nsemi nation is inferred if female s, on t he average, have more spermatozoa i n
their spemathecae than male s have avai lable to transfer . Multiple copulation i s
inferred if a female's entire genital tr act contai ns more spermatozoa that one
male can produce . (d) If males can provide more spermatozoa than female s
store , single inse mi nation i s inferred. This conclusion is not justified, however,
because a female may mate repeatedly with different male s, even i f e ach
p roduce s sufficient sperm to fill her sperm atheca.
Corso & Serzedello (23) dissected t he genital organs of a sample of Atta
laevigata males and queens prior to mating flights, and of another sample after
mating flights. They the n de ter mined how much DNA was lost per male and
how much was gained per female, presumably via spermatozoa. Their method
re sulted in a minimum estimate of the number of inseminations for a female,
because the method could not deter mine if females had engaged in multiple
cop ulations, with e ach male contributing a fraction of its available sperm.
DISSECTION
VISIBLE MARKERS
Visible genetic markers have been used to e sti mate the
mati ng frequency ofApis mellifera queens . All methods assume random mating
and yield e stimates of the effective, rather than the actual, number of matings
SPERM USE
299
over the period of time that progeny samples were collected . None of the
methods a ssign confidence limits to the estimations.
Allozyme a na lyses allow random sampling of natural
populations. Reports are probab ly b iased toward monoandry because it is more
easily verified owing to the frequent uncertainty of how many queens contr ibute
progeny to the sample. This uncertainty may be a consequence of queen
usurpation, super sedure, or polygyny.
Most commonly , a ssumed pedigrees based on electrophoretic phenotypes of
nestmates are used to determine a minimum number of mates of the queen.
Wilson's ANOYA method (149) has also been applied to determine the mean
number of mating s a nd confidence limits for females ( 108). It is particularly
useful because it a lso provides a test for random mating .

ALLOZYME MARKERS
PREFERRED METHODS
The most useful methods for determining polyandry
are (a) dissection to determ ine multiple mating only , and (b) the use of visible
and a llozyme markers for monoandrous queens, and for polyandrous queens
when colonies are known to have a single queen producing the progeny sample.
U sing these methods the data from Table 1 show that 6 species (5 genera) are
monoandrous and 14 species (7 genera) are polyandrous. The data overall are
not systematic and do not allow broad generalizations with respect to phylogeny
or socia lity and mating behavior . However , they do demonstrate that assump
tions of the rarity of polyandry or monoandry in eusocial or non-eusocial
species are not justifiab le.
Trends in the Data

Cole (22) pointed out that the literature is b iased toward mating behavior of
social insects in that the va st majority of reports concern species with populous
colonies. Cole further emphasized that a trend for polyandry in ant species with
populous colonies and for monoandry in species with smaller colonies is
evident. He suggested that polyandry evolved in response to a need for more
spermatozoa by queens of species with populous colonies. This hypothesis was
previously proposed (37, 1 14, 139) and aSSl'mes that an individual male of a
populous species does not produce suffi cient spermatozoa to completely in
seminate a female. Hamilton (57, 58) suggested that insufficient sperm occur s
i n only a very few highly eusocial species. This point was also made by Crozier
& Page (34) and is i llustrated in Figure 1.
A correlation exists between the numbers of spermatozoa produced by male
bees and the numbers retained in the spermathecae of females (r = 0.87,
P<O.0 1 for bees; r = 0.47, P>0.05 for wasps). In addition, males of both
wasps and bees were a lmost always able to provide sufficient number s for
complete insemination. Available data suggest that individua l males of highly
300
PAGE
Table 1
Monoandry and polyandry in eusocial Hymenopteraa
Species
No. of matings
Method
Reference
51
136
81
Family Vespidae
Single Mating

Polisles versicolor
Vespula germanica
Vespula pensylvanica
Multiple Mating
Polisles metricus
P. variatus
Vespa crabro
Vespula atropilosa
Vespula maculifrons
>1
89
>1
88
>1
>1
0,0
7
81
>1
O, A
118; K. Ross,
peTS. comm.
Family Apidae
Single Mating
Bombus bifarius
B . lucorum
B. variabilis
Melipona marginata
M. quadrifasciata
M. quinquefasciata
0
0
60
117
0
0
0,0
0
117
72
76
35
Multiple Mating
Apis cerana
A. mellifera
14-30
7-17
Bombus huntii
Bombus hypnorum
B. lerrestris
2-3
2-3
0
V,O,O,A
154
I, 42, 74, 106,
132,138
60
>1
0
0,0
60
117
>1
1-3
>1
0,0
0
0
6
5
115
0
0
27,29
134
135
108
0
0
21
21
Family Halictidae
Single Mating
Multiple Mating
Lasioglossum zephyrum
L. rohweri
Halictus marginatus
Family Formicidae
S ingle Mating
Aphaenogaster rudis
Formica dakotensis
F. obscuripes
F. transkaucasica
Harpagoxenus canadensis
H. sublaevis
lridomyrmex purpureus
Myrmica americana
Pheidole sitarches
Rhytidoponera chalybaea
R. con/usa
53,54
0
0
69
146
144,145
144, 145
A
A
SPERM USE
Table 1
30 1
(continued)
Species
No. of matings
SoLenopsis invicta
Method
Reference
64; K. Ross, pers.

comm.
Multiple Mating
Acromyrmex Landolti
>1
72; W. Kerr, pers.
Atta laevigata
A. sexdens
A. texana
Brachymyrmex depilis
Eciton burchelli
Formica aquilonia
F. bradleyi
F. exsecta
F. montana
F. opaciventris
F. pergandei
F. pressilabris
F. rufa
F. sanguinea
F. subintegra
F. yessensis
>3
3-8
>1
2-3
1-5
>1
2-3
1-2
>1
>2
>1
>1
>1
>1
2-4
>1
>1
>1
>1
4
5-6
2-4
D
D
D
0
0
0
0
23
70
96
102
116
III

comm.
Lasius flavus
L. niger
Monomorium salomonis
Mycocepurus goeldii
Myrmica rubra
Pogonomyrmex badius
P. barbatus
P. califomicus
P. desertorum
P. maricopa
P. occidentalis
P. rugosus
Polyergus lucidus
Prenolepis imparis
Solenopsis lou
4-5
1-6
2-3
2-3
>1
4-5
6
>1
>1
0
0
0
A
0
A
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
55
112
67
126
68
108
85
108;cf113
67
66
39
39,65
39
70
39
140
61
92
61
61
97
61
87
133
39
'Multiple mating is inferred from any laboratory or field study where multiple copulation was demonstrated.
Subjective decisions were made in those cases where multiple copulations or inseminations were found to be rare.
No attempt has been made to clarify nomenclatural discrepancie s based on synonymy. Abbreviations for methods
of determination: A = allozyme markers; 0 = dissection; 0 = observation; V = visible phenotypic marker. Data
primarily represent a compilation of verifiable listings from previuus reviews (22, 106, 130).
polyandrous species only transfer the app roximate number of sperm atozoa that
females can store (70, 76, 96, 150, 154).
Among species of wasp s, the number of females that a male can potentially
inseminate decre ase s with increasing levels of sociality. Like wise , the number
of spermatozoa ejaculated increases with soc iality (51). The number of sperm a-
PAGE
302
12
10
8
..

4
en
w
..J
oCt
::E
w
u.
2
0
-2
-4
-6
-8
-10
-12
ANTS
BEES
WASPS
9 10
11 12
MALES
Figure 1
Sperm counts for male and female Hymenoptera. Each point represents a different
species of ant (70, 96), bee (2, 4 1 ,76, 1 l7; 1 24), or wasp (5 1 ). Data were transformed by log,
(sperm count/IOOO).
tozoa retained by females i ncreases with colony population size for var ious
species of bees (4 1) .
Why Polyandry?
Croz ier & Page (34) revie wed the current hypotheses for the evolution of
polyandry in the social Hymenoptera in the context of generality, plausib il ity,
and how well these hyp otheses fit to the data trends noted by Cole (22). The
hypotheses are:
HI.
H2.
H3.
H4.
H5 .
H6.
Polyandry allows an increase of effective population size, thus favoring
population l ongevity (147) .

Polyandry is favored because it increases genetic variation within broods
(143, 147): It either (a) results in more var iable queens , (b) provides a
basis for more variable caste determination, or (c) provides a greater mix
of worker genotypes .
Polyandry is favored because i t sets u p competition among (a) sperm
within spermathecae (130) or (b) sibling groups within colonies of
fissioning species (46).
Polyandry is favored because it increases the genetic output of queens
relative to that of their worker progeny (93) .
Polyandry is favored because it results in a worker -adjusted sex ratio
closer to that preferred by the queen (95 , 1 30) .
Polyandry occurs because it is easier for the queen to mate repeatedly
than to fight off pers istent males (2, 114).
SPERM USE
H7.

H8.
303
Polyandry is necessary in order for queens of species with populous

colonies to have sufficient sper matozoa to last their egg -lay ing l ives (22,
37, 114, 139).
Polyandry, under certain conditions of colony growth and genic s ex
deter mination , leads to higher individual f itness of queens (34 , 100 ,
106).
Although each of these hypotheses has plaus ible elements , Crozier & Page
concluded that only hypotheses H2b, H2c, and H8 are suff iciently general,
plausib le, and predictive to serve as useful guides for further research . Of these,
Croz ier & Page cons ider hypothesis H8 the most plausible and the best explana
tion of the data trends.
Hypothesis 8 was originally proposed to explain the high degree of polyandry
in honey bees. Sex in honey bees is determined by a s in g le g ene locus with
multiple alleles . Individuals that are ho mozygo us at this locus develop into
diploid males that are eaten by the workers, with a substantial detrimental effect
on the colony (82, 151, 152, 157, 158). At equil ibrium all al leles are expected
to be equally frequent because of complete overdo minant selection . The num
ber of sex alleles in the population will determine the proportion of diplo id
males produced. The number of males that inseminate queens will affect the
distr ibution of brood viability among colonies but w ill not affect the average
proportion of diploid males produced within pop ulations (l, 105, 128, 156,
161). If the relationship bet ween worker viab ility (as a consequence of diplo id
male inviab ility) and queen f itness is convex about the mean of the distr ibution
of worker viability , then g enotypes for s ingle mating are favored because they
result in greater var iance in viab ility among queens . If , ho wever , the relation
ship is concave, polyandrous genotypes are favored because they have lower
variance. If the relationship is linear (the least robus t assumption) then numb ers
of matings, by this model, are selectively neutral .
Crozier & Page (34; see a lso 30 , 106) proposed that this model is readily
generalizable to the social Hymenoptera , assuming (a) the g eneral ity of the
heterozygous sex a llele hypothesis for sex determination (26) and (b) a direct
relationship between colony f itness and the number of workers present at the
time the colony produces its reproduct ives . Colonies that produce reproduc
tives during the accelerating phase of log istic growth (99) are likely to have
convex relationships between brood viab ility and f itness that favor monoandry .
Those producing reproductives during the decelerating phase are l ikely to have
concave f itness relationships that favor polyandry.
Croz ier & Page expanded the model to the case of two sex-determining loci
and demonstrated that the results still hold. The sex determination system and
the consequent production of dip lo id males is unlikely to hold for all cases
within the Hymenop tera (see 7 1, 72 for a competing hypothesis). Nonetheless ,
it holds not only for special cases and is receiving increasing suppor t from
theoret ical and allozyme studies ( 19 , 28) .

304
PAGE
Hypothesis 8 has been called "genet ic benefits po ly andry ," and has been
considered a special case for the evolution of polyandr y in insects (137); but is
it? The basic model is. one of selection for r is k adaptedness to the genetic load
(99, 1 19 ); t his may explai n monoandry and polyandr y in nonsoci al ,
nonhymenopteran speci es. If, for a given clutch size, interactio ns among
members of a brood are mutualistic and result in a net increase in fitness Per
i ndividual (convex relationship), then monoandry may be favored. If in
teractions are competitive and result i n a net decrease i n fitness per individual ,
then polyandry may be favored. Page & Metcalf ( 106) pointed out that for those
cases w here there appears to be selective neutrality (linear ity) , Gillespie's
pri nciple of selection for reduced w ithin-generation variance in offspring num
ber may apply (48-50). In these cases selection favors polyandry. The point is
that the genetic and ecological environments of the population will always be
factors in the evolution of mating behavior and s hould always be considered.
It may be possible to test the robustness of hypothesis 8 by st udying some of
the appar ent exceptions . Good candidates are the stingless bees (Meliponi ni ) ,
the paper w asps (Polistinae) , and the fire ant , Solenopsis invicta. Some sting
less bees produce sig nificant numbers of diploid males but are apparently
monoandrous . Melipona spp . have a unique genetic caste-determinat ion s ys
tem that results i n workers killing a high percentage of newly emerged diploid
adults or g ynes (72, 73), perhaps keeping the average worker population i n
convex reg ions of the fitness curve. M ale Trigona postica larvae prey o n female
larvae (8), again reducing aver age brood viability . Some Polistes spp . are
polyandrous but have small colonies . However, reproductives emerge fro m
colonies of P. Juscatus and P. metricus after the leveling-off phase o f colony
growth (36 , 88 , 89); this perhaps supports the model. Solenopsis invicta
apparently exhibits a s ingle locus sex-determination system simi lar to that o f
the honey bee (Ross , Fletcher , unpublished manuscript), populous colonies
(86) , and monoandry ( l 18a) . Productio n of reproductives is initiated at rel
atively early stag es of colony growth. Polyg yny, however, complicates both
the model and the interpretat ion of the results .
SPERM ACQUISITION'
P ar ker ( 1 14) identified char acterist ics of insect mating behavior , reproductive
mor pho logy, and patterns of sper m usage. He suggested that insects are
rc e
'Mating and spen n-use t erminology h as f reque ntly been used imp e is ly. I provide definitions
of the following terms to standardize their meanings: Fertilization is the penetration of an ovum by a
spermatozoon with the resulting formation of a zygote. Insemination is the deposition of spennato
zoa into the long-term sperm-storage organ (the spermatheca) of a female. Sperm competition is
direct competition among spennatozoa for insemination or fertilization. Insemination competition
is competition among m al es to m aximize the 'rel ative numbers of their spennatozoa that are

SPERM USE
305
preadapted to h i gh levels o f sperm competition because (a) females often mate

with more than one male after they have viable sperm stored from previous
matings; (b) females typically have specialized sperm storage organs that
mai ntai n viable sperm for long periods of time; and (c) females have high
sperm- ut ilization efficiency during egg fertilization.
Eusocial Hymenoptera exemplify conditions for sperm competition because
of the frequent occurrence of polyandry, the large number of species with
long- li ving queens, the tendency for queens of most species to mate o nly during
a single short period a nd store a lifeti me supply of spermatozoa , and the large
numbers of reproductive proge ny .
Sperm Acquisition in Apis spp.
The following discussion of the process of mating is adopted in part from
previous reviews (40 , 120 , 160). These reviews dea lt- with A . mellifera;
however, the genera l mating biology appears to be quite similar for A. cerana
(124 , 155).
Matings take place whi le bees are in flight , at specific locations where many
males congreg ate ( 123) . One such congregation area was estimated to have
more than 25,000 droncs from more than 200 colonies in attendance at one time
(N. E. Gary , personal communication; cited in 106) . Queens make one or
several fl i ghts to these areas within several days of their e mergence as adults
(150 , 153). Males i n the area are attracted to them and copulate with them in
rapid succession. A queen will copulate with up to 17 drones on a single flight
( 150) a nd will copulate o n the a verage with 7 to 17 males , depending on the
population (1, 132). Following ejaculation, each male undergoes rapid p aral
ysis , falls to the ground, and dies . Copulations last several seconds (42) .
Males apparently cannot gain access for copulation until the queen opens the
sting c hamber; t hus potenti ally t he queen has consider able control over mating
(42 , 76a). During copulation, the male everts his genitalia into the sting
available to fertilize a female. It can take the form of (a) sperm displacement-the physical removal
or repositioning of spermatozoa of p revious mates within the genital tract of the female; andior (b)
sperm replacement-the replacement of spermatozoa by a male after disp lace ment or after the
female voluntarily or involunt arily voids sperm from the genital tract.
Sperm precedence
occurs
when the spermatozoa of any male fertilize ova before those of another. There may be partial
mixing , but the sperm of a preceding male must initially fertilize a proportion of ova greater than th e
prop ortion of that male's sperm repres ented overall in the spermatheca. Sperm bias is the unequal
frequency of fertilization of ova by spermatozoa of different males, as a consequence of unequal
numerical representation within the spermatheca. Copulation is the act of pairing and intromis sion ,
which may, but does not necessarily, result in the deposition of spermatozoa in the reproductive
tract of the female. Mating competition is competition among male for copUlations. Mate and
copulate are considered synonyms.

306
PAGE
chamber of the queen . Eversion and subsequent ejaculation re sult from increas
ing pressure from the male's hemolymph with contraction of the abdomen.
Ejaculation is explosive; the endophallus ruptures and semen containing abo ut
6 mi llion spermatozoa (76) is propelled forward into the median oviduct of the
queen (see F igure 2). The queen probably lowers the valvefold between the
vagina and the median oviduct before succe ssful insemination occurs (78).
Semen deposited in the oviduct by previous mating s is displaced a nteriorly into
the latera l oviducts, probab ly by the force of subsequent ejaculations (see 120,
F ig ure 11).
A l arge quantity of mucous is deposited in the vagina a nd bursa following
propulsion of the semen. The bulb of the endophallus separates from the drone
and the mucous rapidly coagulate s; togethe r they form a plug , called a mating
sign. This plug does not prevent subsequent copulatio ns on a given f light (76a) .
The workers a ssist the queen in rapidly removing the last plug w hen she returns
to the hive.
Species that undergo colony f ission as a component of female reproduction
tend to have extremely male-biased numerical sex ratios and to have males that
mate once and die by automutilation (20, 107) . This is true for stingless bees
(35, 76), army ants (127), and at least two species of honey bee (125). It is
possibly an evolutio nary consequence of extreme mating and insemination
competition among males, and a result of their overabundance. Honey bees
have a male: female numerical sex ratio that may exceed 20,000: 1 ( 1 07) .
The mating s ig n is not very effective for prevent ing subsequent copulations .
Double mating s igns are occasionally observed in queens returning from mating
flights (160). When this occurs , the semen is found depos ited behind the
anterior mating sign, suggesting a blocked copulation . In stingless bees,
however, the mating s ign apparently guarantees single copulation by queens
SPD
POV
VG VPvo
MOV VF
BP
Figure 2 Lateral aspect of the reproductive tract of a queen honey bee. Anterior is left. POV ;;
paired lateral oviduct; MOV = median oviduct; SPD = spermathecal d uc t; VF = valvefold; VG =
vagina; VP = vaginal passage; VO = vaginal orifice; BP = bursal pouch; SC = sting chamber.
Figure courtesy of H. H. Laidlaw with permission of Alan R. Liss, Tnc. (78, Figure 5).

SPERM USE
307
(35 , 71, 72) . In both groups , the mating sign may prevent the backflow of
semen following ejaculation (9), confining t he semen of the last male near the
sper mathecal duct in optimal position for insemination.
I mmedi ately after the queen returns from a mating flight , the spermatheca
contains few sper matozoa but the l at eral oviducts are greatly distended and
packed with semen (9, 78) . The forceful ej aculation of the drone does not
directly fill the spermatheca; instead, insemi nation occur s over a period of
about 40 hr (159) . Delayed sperm migration ha s also been reported for the sweat
bee, Lasioglossum zephyrum (6). The paired l at eral oviducts have fine longitu
dinal muscle fibers for ming a one-layer sheath; the median oviduct has a
complex muscul atur e . T he combined functioning of these muscles, alo ng with
abdominal contractio ns of the queen, result in the backward movement of the
semen through the oviducts, past the spermathecal duct and v alvefold, i nto the
vagina , throug h the vaginal orifice, and out i nto the sting chamber . The same
mechanism probably applies for passing egg s po steriorly during oviposition
(78 ) .
Some mixing of spermato zoa of different males probably occurs within the
oviduct s as a consequence of displacement by forceful ejaculations and abdom
i nal contractions of the queen. However, mixing i n t he oviduct s i s not necessar y
t o effect insemination b y a l l mates. The queen may control the transfer o f
spermatozoa fro m the oviduct into the spermatheca and the inseminatio n
success of different males by controlling the rate of po sterior flow of semen
fro m the oviducts into the sting chamber . Some sper matozoa may be forced i nto
the spermatheca by the backward compression of semen and the action of the
valvefold, but the quantity is probably negligible; active migration of spermato
zoa into the spermatheca i s probably more i mportant (43 , 12 1 , 122) .
Spermatozoa have access to the spermathecal duct and the spermatheca from
the median oviduct and the vagina, near the valvefold. Spermatozoa that pass
thro ugh the vaginal passage i nto the sting chamber are unlikely to enter the
spermatheca. The rate at which semen flows po steriorly determines the pro
portions of spermatozoa of different males and the overall efficiency of filling .
Rapid passage results in low efficiency; err atic passage results i n i ncreased
sperm bias .
Woyke (159) counted the spermatozo a migrating into queen spermathecae
over a 40-hr period following injection with different volumes of semen. He
observed similar rates o f sperm migration for the fir st few hours. Rates of
migration for small-volume injectio ns decreased rapidly thereafter, suggesting
that mo st of the semen had passed the spermathecal duct . For large-volume
i nseminations, migration rates were nearly constant over a 24-hr period and
then decreased .
The vaginal passage and the v alvefold, which control the backward flow o f
semen, may r eg ul ate i nsemination effi ciency b y i nfluencing the time needed for

308
PAGE
spermatozoa to reach the spermathecal duct. A. cerana has a lower insemina

tion efficiency thanA . melli/era and lacks the vag inal passage ( 125 , 154 , 155).
Sting less bees of the genus Melipona have very high insemination efficiency
( 35, 72, 76) but apparently lack a valvefold. H igher efficiency is probably a
consequence of higher sperm motility and longer persistence ofthe mating sig n.
When full, the spermatheca conta ins a total of about 5 . 3-5 .7 mill io n sperma
tozoa (76,84, 150), which probab ly represent the contr ibutions of all ejaculates
(79). As the spermatozoa migrate into the spermatheca, they disperse through
out the availabl e space (104) . However , it is not known if this disper sa l is under
queen control or is a consequence of sperm motility. Possibly, sperm disper sal
is a consequence of sperm competition. A normal queen may lay 200,000 fertile
egg s that develop into nonreproductive worker s before she lays the few egg s
that eventually develop into queens ( 10 I). If poorly dispersed spermatozoa near
'
the duct have precedence in fertilization, they are more l ikely to fertilize egg s
destined to beco me nonreproductive worker s rather than queens and are prob
ably less fit than disper sed spermatozoa .
A s the spermatheca beco mes more densely packed there is less room for
spermatozoa to disper se, and spermatozoa fro m a g iven male are more l ikely to
be clo sely associated. It is l ikely that the fir st spermatozoa depo sited in the
median oviduct will be disp laced to ward the a nterior ends of the lateral oviducts
a nd be the last to pass the spermathecal duct and migrate into the spermatheca .
There may be less room in the spermatheca for late-arriving spermatozoa and,
consequently, lower representation of ear ly mates of a g iven mating flight;
hence a sperm bias favoring late-mating males is established. A filled sper
matheca may a l so account for a b ias toward mates from early flights when
successive mating flights occur .
Mackensen (83) showed a relationship between the amount of semen injected
into queens and the number of spermatozoa retained in the spermatheca . The
fir st injection (perhaps the equivalent of a sing le mating flight) of a given
a mount of semen resulted in a greater increase in the number of spermatozoa in
the spermatheca than did a second injection of the same amount.
Taber ( 131) injected virgin queens with the semen of wild-type and geneti
cally mar ked dron es. He injected one group with semen from the wild-type
dro nes fir st, fol lowed two day s later by an approximately equal volume of
semen from the marked drones; the order was reversed for a second group.
Taber's results showed a sperm bias for the sperm type that was injected first.
Laidlaw & Page (79) injected each of four virg in queens with sperm from
different drones (each of a different and distinguishable genotype) each day for
four consecutive day s. Their results showed no significant sperm bias with
respect to order of injection. However, the low volume injected each day may
have resulted in low sperm migration into the spermatheca and therefore
abundant space may have been availabl e for spermatozoa of subsequent in
jectio ns.

SPERM USE
309
There is no evidence that sperm displacement, replacement, precedence, or

bias results from sperm competition among male ejaculates. Laidlaw & Page
(79) serially injected semen from five or six different males, each with pheno
typically distinct genetic mar kers , into the oviducts of seven virgin queens.
They found no relationship between the phenotype of the drone father or the
order in which the semen went into the oviduct and the distribution of fertiliza
tion success. They also injected each of four virg in queens with 7 mm3 of semen
from wild-type drones on two occasions, two days apart, and then injected the
semen of two additional m arked drones two days later . They found that the
spermatozoa from the last injection fertilized about half as many eggs as would
be expected if the quantity of spermatozoa contributed by each injection were
proportional to the volume of semen injected. Each drone contributed about the
proportion of spermatozoa that would be expected if sperm m igration efficiency
were to decrease as the spermatheca filled with spermatozoa (83) .
SPERM UTILIZATION
Sperm utiliz ation by multiply inseminated females is important because of its
relationship to kin selection theory and the evolution of eusocial ity (3, 4 , 22,
32, 56-58, 75 , 106, 129, 130, 139, 142). The genetic environment and the
interactions of individuals are the essential components of kin selection.
Polyandry and patterns of sperm use affect the distribution of the total genetic
variance within the population . A high number of matings increases the within
family (colony) variance and decreases the between-family variance, which
leads to increased potential for within-group selection and decreased potential
for between-group selection ( 142) . Here I present available data for patterns of
sperm use by po lyandrous reproductive females (again concentrating on the
honey bee), discuss the effect of nonrandom usage on the genetic relationship
among nestmates, and present current evidence for deterministic nestmate
interactions .
Patterns of Sperm Use

Polistes variatus queens use the spermatozoa of two males at a r atio of
approximately 9: 1 during brood rearing (89). Metcalf & Whitt (89) measured
allozyme frequencies in early-season worker s and late-season reproductives
separ ately in three nests and found no evidence for sperm preccdence . Pamilo
( l08) showed a similar sperm bias in Formica sanguinea, F. transkaucasica,
and F. pressilabris; however, he did not present data for a test of sperm
competition or precedence .
I ncomplete mixing of spermatozoa of different ejaculates within spermathe
cae has been demonstrated in A. mellifera, but cvidcnce for sperm precedence
or sperm competition is lacking . Taber (131) studied patterns of sper m u se for
35 natur ally and instrumentally inseminated queens. Each was inseminated

310
PAGE
with the sperm of wild-type and genetically marked males . He was able to
distinguish two phenotypes of worker offspring corresponding to the male
genotypes used, and reported the ir frequencies in colonies headed by test
queens o ver a period of up to three years . H is data showed no obvious
differences between sperm-use patterns of natur ally or instr umentally in
seminated groups. He concluded, "Sperm from multiple m atings does not m ix
appreciably inside the spermatheca during mating or after . . . " (131, p. 525).
H is conclus io n was widely approved until Croz ier & Bruckner (32) and Page &
Metcalf (106) po inted out that h is conclusion was not suppor ted by h is data. I n
all cases, queens used the sperm of both male genotypes at all times, usually at
frequencies appro aching 1: 1 . Taber did, ho wever, demonstr ate that sperm is
not completely m ixed with in the spermatheca; this was an expected result based
on the mechanism of filling .
Kerr et al (75) presented data for 32 hone y bee queens that had m ated
natur ally with dro nes of Italian and African r aces in a controlled, isolated area.
Wor ker progeny were s ampled at 15-16-day intervals for a per iod of 9-10
months, and the paternity was determined for each . The results of the study
were s imilar to T aber's: Phenotypic frequencies fluctuated considerably o ver
time, suggesting incomplete m ixing of spermatozo a of different ejaculates
within queen spermathecae . Altho ugh the y concluded, as did Taber, that sperm
from different male ejaculates does not mix appreciably, thcir data demo n
str ated that the sperm of at least two males was available to fertilize eggs at any
g iven time, and that in most cases pheno typic frequencies fl uctuated around
.
1: 1 .
Page & Metcalf (106) used alloz yme analysis to investig ate sperm-utiliz atio n
patterns in 1 2 o ne-year-old naturally mated honey bee queens . Their data
showed fluctuations in genotypic frequencies o ver 11 weeks for the three
distinguishable m arkers; however, they also showed that queens were us ing the
sperm of at least three males at all times .
L aidlaw & Page (79) injected seven hone y bee queens with spermatozoa
from five or six phenotypically distinct males and showed that queens used
sperm from all m ales in representative proportions o ver a 22-month period.
They concluded that the spermatozo a from different ejaculates do not m ix
completely in the spermatheca. Ho wever, fluctuatio ns did occur around repre
sentative frequencies for each inseminating male, and these fluctuations do not
result in the preponderance of fertilization s uccess by o ne or a few m ales at any
time . Laidlaw & Page der ived compo nents of vari ance for short-term fluctua
tions in sperm use and differential insemination success, and they concluded
that the majority of var iance in fcr tilization success of males is attributable to
insemination competition rather than to intraspermathecal sperm competition
or precedence .
Moritz (94) reported a s imilar study where poo led, dilute semen from m ales
of e ight distinct genotypes was serially injected into the o viducts of five honey

SPERM USE
311
bee queens. All genotypes were present in all progeny samples . He found no
significant fluctuations over a 2 1-day sample period, but did find a significant
b ias associated w ith the serial order of injection; the order of representation of
sper m in the spermatheca was opposite the order of injection (unpublished
manuscr ipt) . The comb ined results of Laidlaw & Page (79), Moritz (94;
unpublished manuscript) , and Woyke (159) suggest (a) sper m of different
ejaculates does not mix to a great extent in the oviducts of queens; (b) queens
pass the semen of the different ej aculates by the spermathecal duct at a fairly
constant r ate; and (c) the spermatozoa of different ejaculates mix w ithin the
sper matheca.
Harbo (59) presented data and a model suggesting that honey bee queens
release a constant volume of spermathecal fluid for each egg fertilized. The
spermathecal fluid is replaced, resulting in a rapid decrease in the concentration
of sper matozoa w ithin the spermatheca as i ncreasing number s of eggs ar e laid.
Initia lly each aliq uot contains a large number of spermatozoa, of which all but
one are wasted. H igher sperm-utilization efficiency occurs as more egg s are
laid. The spermatozoa must become redistributed within the spermatheca;
otherwise only the spermatozoa near the duct w il l be used and queens w il l
prematurely r un out of usable sperm cells.
Some reported fluctuat ions in progeny phenotypes may be a consequence of
differential phenotypic susceptibility to disease and stress . Laidlaw & Page (79)
reported such fluctuat ions with the onset of a brood disease in a single colony of
honey bees containing six worker patrilines (lines from the same drone father).
Two wor ker patrilines decreased in frequency, approaching zero, while one
patriline dr amatically increased in frequency relat ive to the other five. After the
colony w as treated with antibiot ics, the phenotypic frequencies returned to
preinfection l evel s .
Genetic Relatedness
Although the theory of the evolution of altruism, and hence eusociality, has
proven to be considerably more complex than was originally conceived, the
genetic relationship of interacting individuals remains an important component
(24 , 25 , 31, 91 , 109 , 141 , 142) . A clear demonstr ation of widespread polyan
dry and low degrees of genetic relat ionship among altruistic interactant s would
cast doubt upon the importance of haplodiploidy as an expl anation for the
frequent occurrence and high levels of sociality within the Hymenopter a com
pared to male diploid org anisms.
Sperm utilization patterns affect the genetic rel ationships of diploid progeny
within broods (worker s and reproduct ives) , which in turn may alter the likeli
hood and the rate at which kin selection can occur. Hamilton (57) provided a
formula for the averag e degree of genetic relationship [See Pamilo & Crozier
(110) for a complete discussion of the different ways to measure this quantity
and the appropriateness of each; in this sect ion I use the symbol s that were used
312
PAGE
by the original authors .] between diploid progeny under conditions of polyan

dry with sperm bias:
n
(112
L f})/2,
1.
j
where jj
the frequency of fer tilizations by the lh of n males. For the case
where all n males contribute equally, the formula becomes

(1/2
lIn)/2 ,
which H amilton stated, and Wade (142) proved, is a minimum value for
any g iven n. Starr (129, 130) designated the value
2.
for
L J}
11
from Equations 1 and 2 the effective promiscuity index, Pe.

L ai dlaw & Page (79) der ived the genetic relationship among diploid off
spring as a function of the difference between the expected colony relatedness
(Re) when all males contribute equally to the progeny (Equation 2) and the
actual distribution of fertilizations:
Rc - Rc +
_
'
2
nO'
/2 .
3.
This is equivalent to
(112
lIm)12 ,
4.
where
5.
m is equivalent to Pe'

SPERM USE
3 13
Equat ions 4 and 5 can be expressed in terms of the insemination effective

number of mat ing s, m), which reflects fer tilization success of males over the
lifetime of the queen, or the short-term effective number, m2, which is the
effective number of males contributing spermatozoa for fertilizations over a
sample interval of any g iven per iod. The term m) pr imar ily reflects differences
in the insemination abilities of different males and event s that take place during
sperm m igration into the spermatheca, which can be considered mostly ex
traspermathecal. F or the honey bee, var iability in amounts of spermat,ozoa
ejaculated, viscosity and concentration of semen, sperm displacement and
replacement, i nsemination and i ntraoviductal sperm competition, and variabil
ity in the r ate at which the queen voids the oviducts determine the insemination
success of different male s . I ntraspermathecal sperm viability also adds to this
v ariance. The number m2 is determined by both intra- and extraspermathecal
events, genotypic v ariation in survivor ship due to environmental effects, and
sampling error . I ntraspermathecal events include incomplete mixing of sperm
within the spermatheca and differential motility, viability, and survival of
spermatozoa of different male s .
F or n m ales, the appropriate variance for calculating m ) in Equation 5 i s
fj
(Pj
p)2In,
6.
where Pj i s the frequency of fertilizations of the P male over the egg-layi ng

lifetime of the fem ale . The appropriate variance for calculating m2 is:
n
II (Pij
p)2Ink,
7.
where Pij i s the frequency of fertilizations of the ith sample for thefh m ale . The
variance expressed by Equation 6 is an additive component of Equation 7;
therefore the difference between m 1 and m2 reflects primarily intraspermathecal
events.
W ade (142) showed that n in Equation 2 should be replaced with iI, the
h armonic mean number of males inseminating females, to calculate the average
genetic relationship within broods , over a population, when females mate with
different numbers of males and each m ale contributes equally to fer tilizations.
A more general formula that takes into account unequal contribution ofmale s i s
easily derived from Equations 4 and 5 by substituting iii for m i n Equation 4:
iii
iIl(n2a.2
1),
8.
314
PAGE
where n2a2 is averaged over all queens with the appropriate a2 from Equation 6
or 7 above . The net result is that the average relatedness among diploid siblings
within the population is a function of the variance in fertilization by different
mates and the harmonic mean number of matings per female, with higher
variance and fewer matings affecting the mean more than lower variance and
more numerous matings.

Kin Recognition
The ability of workers in eusocial insect societies to distinguish among nest
mate and non-nestmate kin and non-kin has become a central issue in sociobiol
og y ( 1 0, 1 4, 33, 44, 45, 62, 63, 77, 90). Polyandry results in potential
reproductive competition between members of different colony patrilines. If
nestmate sibs of polyandrous queens interact deterministic ally on the basis of
kinship, then the averag e genetic relationships among nestmates as c alculated
above may be inappropriate because of the importance of the relationship
between the interactants and the net effect of the interactions on fitness .
Recent studies of bees have shown consider able potential for deterministic
interactions among worker nestmates of Lasioglossum zephyrum ( 1 7, 52) and
A. mellifera ( 1 3, 1 5,46,47; see also review by Gamboa et ai, this volume, for
wasps) . Noonan (98), Page & Erickson ( 1 03), and P. K . Vi scher (personal
communic ation) have observed that honey bee workers show preferential
treatment toward grafted queen larvae that have a close genetic relationship.
H owever, using a different methodology, Breed et al ( 1 6) and Page & Erickson
(unpublished manuscript) found no evidence for preferential emergency queen
rearing based on kinship, though Page & Erickson did find differential re
sponses based on larval phenotypes .
Boch & Morse ( 1 1 ) and Breed ( 1 2) demonstrated that worker honey bees can
learn recognition labels of an individual queen and can recognize queens that
are rel ated or unrelated to the learned queen. Page & Erickson (unpublished
manuscript) demonstrated that virgin queens have genetically determined
labels and that workers in cage studies can recognize queens on the basis of
these labels .
I n summary, these studies show that adult workers and larval and adult
queens have phenotypic (and probably genotypic) labels that workers can
recog nize and use as a basis for responding to various exper imental conditions .
However, the tests to date have been s implistic and perhaps out of context with
natural conditions . As a consequence, the biolog ical significance of intr anidial
kin recognition remains to be demonstrated .
CONCLUDING REMARKS
Polyandry in the social Hymenoptera is certainly not rare, but more systematic
studies are needed to determine i ts extent and s ignificance. More studies are

SPERM USE
3 15
needed, such as those of Pamilo ( 108) in which effective numbers of queen

matings were estimated with confidence limits.
Hypotheses for the evolution of polyandry are abundant but these hypotheses
have not been tested. It is likely that the genic mechanism of sex determination
is an important component of the evolution of mating behavior in some species.
Bull ( 18) suggested that the single-locus sex-determining system may be
ancestral , and a necessary step in the evolution of haplodiploidy. lf this is true ,
it presents an evolutionary paradox: The same mechanism that increases genetic
relationships among interactants , and thereby favors the evolution of sociality
(haplodiploidy) , may also favor polyandry, which is a disadvantageous system.
Honey bee studies show that queens have the potential to control their
number of mates and to regulate the insemination success and sperm utilization
of each. Anatomical and behavioral specializations arc abundant; they may be
con seque nce s of natural selection for mating and sperm-utilization efficiency.
The honey bee should serve as a model for further studies .
Average genetic relationships among colony nestmates are probably lower
than kin selection theorists originally anticipated because of polyandry , polygy
ny , queen supersedure, and colony usurpation. Howevcr, the relationship
between interacting individuals and the nature of the interactions are important.
Recent studies of polyandrous social bees suggest that some interactions among
nestmates may be directed on the basis of genetic relationship. Directed
interactions depend on kin recognition. As a result, the biological and evolu
tionary significance of kin recognition continues to be a promising area of
research .
ACKNOWLEDGMENTS
I thank Eric Erickson and the USDA Bee Research Unit, Department of
Entomology, University of Wisconsin, Madison for continuing financial sup
port and encouragement. Harry Laidlaw contributed extensively to my interest
in sperm utilization and it is impossible to separate his intellectual contributions
from my own. I am grateful to Michele Page for the original graphics and for
much of the editing; any remaining errors are my own.
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Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Department of Entomology, Univers ity of W isconsin, Madison, W isconsin

0066-4 170/86/0 10 1 -0297$02 .00

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Evidence for Polyandry and Monoandry

Di ssection can be effective for e stimating the minimum number

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Trends in the Data

Monoandry and polyandry in eusocial Hymenopteraa

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

64; K. Ross, pers.

72; W. Kerr, pers.

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Polyandry allows an increase of effective population size, thus favoring

population l ongevity (147) .

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Polyandry is necessary in order for queens of species with populous

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

preadapted to h i gh levels o f sperm competition because (a) females often mate

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

spermatozoa to reach the spermathecal duct. A. cerana has a lower insemina

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

There is no evidence that sperm displacement, replacement, precedence, or

Patterns of Sperm Use

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Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

by the original authors .] between diploid progeny under conditions of polyan

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

from Equations 1 and 2 the effective promiscuity index, Pe.

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Equat ions 4 and 5 can be expressed in terms of the insemination effective

where Pj i s the frequency of fertilizations of the P male over the egg-layi ng

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

needed, such as those of Pamilo ( 108) in which effective numbers of queen

social behavior. Ann. Rev. Ecol. Syst.

Lasioglossum zephyrum (Halictidae).

7. Batra, S . W. T. 1 980. Sexual behavior

and pheromones of the European hornet,

Annu. Rev. Entomol. 1986.31:297-320. Downloaded from www.annualreviews.org

in queenright colonies of Trigona (Scap

recognition alleles? Am. Nat. 1 2 1 :74954

I I . Boch, R . , Morse, R. A . 1 982. Genetic

factor in queen recognition odors of hon

tion and learning of queen odors by work

Natl. Acad. Sci. USA 82:3058-6 1

Bioi. 1 00: 329-39

2 1 . Busc h i nger, A . , Alloway, T. M. 1 979.

Sexual behaviour in the slave-making

ant, Harpagoxenus canadensis M. R .

!canus (Emery), and H. sublaevis (Ny

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evolution of social behavior in the Hyme

study of multiple mating habit in Aua

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J. Theor. Bioi. 1 00:379-97

26. Crozier, R. H . 1 97 1 . Heterozygosity and