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10.1146/annurev.ento.50.071803.130416
Annu. Rev. Entomol. 2005. 50:395–420
doi: 10.1146/annurev.ento.50.071803.130416
c 2005 by Annual Reviews. All rights reserved
Copyright THE EVOLUTION OF MALE TRAITS IN
SOCIAL INSECTS
Jacobus J. Boomsma,1 Boris Baer,1 and Jürgen Heinze2
1
Institute of Biology, Department of Population Biology, University of Copenhagen,
Universitetsparken 15, 2100 Copenhagen, Denmark; email: [email protected];
[email protected]
2
Biologie I, Universität Regensburg, D-93040 Regensburg, Germany;
email: [email protected]
Key Words sexual selection, multiple mating, sperm competition, female choice
■ Abstract Pair formation in social insects mostly happens early in adult life and
away from the social colony context, which precludes promiscuity in the usual sense.
Termite males have continuous sperm production, but males of social Hymenoptera
have fixed complements of sperm, except for a few species that mate before female
dispersal and show male-fighting and lifelong sperm production. We develop an evolutionary framework for testing sexual selection and sperm competition theory across the
advanced eusocial insects (ants, wasps, bees, termites) and highlight two areas related
to premating sexual selection (sexual dimorphism and male mate number) that have
remained understudied and in which considerable progress can be achieved with relatively simple approaches. We also infer that mating plugs may be relatively common,
and we review further possibilities for postmating sexual selection, which gradually
become less likely in termite evolution, but for which eusocial Hymenoptera provide
unusual opportunities because they have clonal ejaculates and store viable sperm for
up to several decades.
INTRODUCTION
It is in sexual behavior that all animals can be considered “social.”
A.M. Stuart (118)
Most mating systems are characterized by a variance in male reproductive
success that is higher than that in females (127) and by competition among males
for fertilization of eggs. This strife is the driving force of sexual selection and
has produced effective fighting devices, costly ornaments and elaborate courtship
displays in males, and concomitant traits of mate quality assessment and choice
in females (8, 112, 126). Social insects, however, seem to be exceptions to this
rule. Their societies appear to represent the cumulative effort of sterile helpers
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(workers and occasionally soldiers) and specialized egg-layers (queens), in which
fatherhood is constant and males have few if any sexually selected traits. As a
result, the field of insect behavioral ecology has primarily addressed questions of
sexual conflict and mate choice in nonsocial insects and reproductive conflict and
kin selection in social insects. Male traits in social insects have been addressed
(20, 23, 32, 39, 44, 65, 111, 115), but the main emphasis was usually on the female
aspect of mating systems (31, 45, 92, 93, 114, 117), except for a recent review on
male bumble bees (10).
This review addresses questions of male mating strategies across all groups
of advanced eusocial insects—ants, social bees, social wasps, and termites. By
taking this broad comparative approach, we concentrate on convergent similarities
that allow us to place the available data in a common evolutionary framework. To
achieve this objective in a moderately sized paper, we often had to ignore details
and to cite earlier reviews rather than original sources. From this synthesis we
develop the outlines of an explicit research program for testing sexual selection
and sperm competition theory in social insects and we identify topics for which
progress can be realized and for which social insects may offer opportunities for
testing questions that are less accessible in nonsocial animals.
FATHERHOOD IN INSECT SOCIETIES
Partner-Commitment for Life and Other Idiosyncrasies
of Male Social Insects
Advanced insect societies are usually kin groups living in single or multiple nests.
Although most individuals are fully or partially sterile, species have almost invariably retained sexual reproduction (23, 33, 84, 136), but with inconspicuous roles
of males. In the eusocial Hymenoptera, males are short-lived and do not normally
engage in social activities. They die after one or a few matings, realized during a
brief mating period, and persist as long-lived sperm stored by the queen(s) with
whom they mated (65, 66, 84, 136). They are haploid, produce clonal sperm, and
sire only female offspring (10, 11, 23, 112). In contrast, a male termite is diploid
and may live as long as the queen, with whom he mates at regular intervals (91,
125, 132). Termite workers and soldiers can be of either sex and are often immatures without sex-specific traits (103, 111). Adult sexual dimorphism is negligible,
except for genital traits (91, 104), whereas queens and males of ants, bees, and
wasps can be very different.
The mating systems of social insects usually involve obligate partner-commitment for life (20, 23), and with such extreme and exclusive commitment, that
when the female dies or loses her fertility, the male stops reproducing as well and
does not obtain a new partner (in Hymenoptera because he is only represented
as stored sperm, in termites because he can no longer disperse). With only few
possible exceptions, queens of social Hymenoptera never remate later in life (23,
84, 106), and in as many as half of the studied species, females always mate with a
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single male and thus produce full-sibling offspring throughout their life (20, 117).
Although many species maintain polygyny (here defined as multiple queens per
colony and not as multiple female mates per male) by accepting newly inseminated
queens (23, 66, 69, 130), these queens are already inseminated by males that have
unequivocally committed their future reproductive fitness before the social status
of their mate was decided. Polygyny therefore does not imply promiscuity and
does not affect the forces of selection that create and maintain male-specific traits
in social insects.
Societies of higher termites are probably even more genetically closed than
hymenopteran societies, as reproductives that have left are not allowed back into
any nest (132). Inbreeding cycles with replacement reproductives occur (86, 111),
but they only decrease the genetic diversity of full siblings. Cofounding of colonies
by several reproductive pairs, with the possibility of promiscuity among them,
rarely results in more than one surviving independent breeder of each sex (33, 91,
103, 111, 123, 124). Fusion of mature colonies in lower termites seems to be the
only exception to this generalization (36, 83, 125), although it would likely induce
some form of serial monogamy rather than a new round of unconstrained mate
choice.
Irreversible partner-commitment for life implies that sexual selection is often
restricted to premating behavior, when the sexes disperse and compete for partners.
Apart from the limited options of secondary mate choice in the lower termites,
postmating sexual selection is possible only when females mate with multiple
males and store multiple ejaculates. This occurs in various lineages of the eusocial
Hymenoptera, most commonly as a facultative trait but obligatorily in some derived
clades (20, 117). However, in all these mating systems, females are receptive for
only a short period and males are normally unable to monopolize groups of females
because they cannot control female dispersal.
Selection for Long-Lived Males or Sperm
Sexuals of annual social bees and wasps tend to be agile flyers and forage on
their own, similarly to their solitary sister taxa, whereas sexuals of ants and higher
termites are often unable to forage as effectively as workers because of their more
elaborate specialization on a limited set of reproductive tasks later in perennial
life (for Hymenoptera this applies only to females, as males do not survive much
beyond their mating flight). This implies a higher vulnerability when workers are
not present, reinforcing selection to minimize exposure to external mortality factors
during partner selection and pair formation outside the colony. The interesting
question is thus not why social insect pair formation happens once early in adult life,
but rather why there are few reversals in clades in which pair formation secondarily
became decoupled from leaving the nest to disperse, so that the vulnerability
constraint became less significant.
Selection for minimizing the solitary exposure of reproductives during pair
formation has produced fundamentally different adaptations in the social Hymenoptera and the termites. As biparental care was ancestral in the termites (88,
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89, 103, 111), the increased longevity of queens induced selection for a similar life
span for males (111, 125). However, only the females build nests and provision
offspring in the Hymenoptera (115, 120), so that the longevity of stored sperm had
to increase with female life span. This happened multiple times in ants, social bees,
and social wasps and made somatic survival of males increasingly superfluous in
advanced clades in which males often survive for only a few hours after leaving
the nest to mate.
Males of both social and nonsocial Hymenoptera have generally completed their
lifetime spermatogenesis when they reach sexual maturity (37, 61, 65) and cannot
increase their supplement of sperm afterward. Male sperm limitation therefore did
not evolve as a result of social fatherhood, although a further reduced time frame
for mating probably reinforced selection to maintain this trait.
The long-lived queens of perennial hymenopteran societies in particular need an
efficient sperm storage process to maintain high sperm viability. Queen longevity
may be several decades in ants (66, 70, 95), so that the survival of stored sperm
matches the equally impressive survival of “kings” (resident males) in termites.
Survival of stored sperm for such long periods is a unique trait for ants and probably
incurs significant metabolic costs for maintenance (128). However, neither sperm
viability nor maintenance costs have yet been quantified or approximated.
To conclude, the result of once-in-a-lifetime partner selection after or during
dispersal is that established insect societies are normally inaccessible for immigrating single (i.e., unmated) reproductives. Although many efforts of mature colonies
are concerned with reproduction, the mate choice activities are normally a solitary activity (23) or rather the minimum extent of social interaction that most
organisms experience (118; see quotation, above). This is in marked contrast with
social vertebrates, in which most if not all individuals are potential reproducers
and in which many of the society’s social activities interact with partner selection and mating. However, pair formation within the nest and without preceding
dispersal has evolved multiple times, both as inbreeding cycles in the higher termites and in various derived mating systems of ants, which is dealt with in later
sections.
MALE MATING STRATEGIES
Mate Location
Mating systems of social Hymenoptera can normally be categorized as either resource defense polygamy or scramble competition polygamy (126). Many bumble
bees and social wasps have resource defense polygamy, in which males patrol the
females’ foraging ranges or flight corridors (5, 17, 106). These mating systems
are typical when females emerge asynchronously from scattered sites and live
solitarily for a number of days or weeks before colony foundation or hibernation.
Scramble competition polygamy is usually associated with mating swarms at landmarks, i.e., synchronized mass-emergence of females over a short period across
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Figure 1 A classification of social insect mating systems based on the density of
virgin females present in aggregations for pair formation and/or mating (determined
in large part by colony density and size and by whether mating is individually or mass
initiated), and the extent to which virgin females disperse on the wing before mating,
a variable that closely reflects where pair formation (mating in social Hymenoptera)
takes place.
entire habitats, and is particularly common in ants and termites, but occurs also in
social bees and wasps (3, 16).
Hölldobler & Bartz (65) divided ant mating systems into a female-calling syndrome, in which individual females emit pheromones to attract males, and a male
aggregation syndrome, in which males first attract additional males and the mass
buildup of pheromones later attracts females (9, 64). Sivinski & Petersson (113)
argued that insects generally have two types of mating swarms, aerial swarms and
substrate-based swarms, a distinction that makes it relatively straightforward to
extend the Hölldobler & Bartz (65) scheme to bees and wasps and to syndromes of
mating in the nest, which have only recently become relatively well studied (Figure 1). The latter include all situations in which females mate before dispersal or
without dispersing at all. In some ants (see Male Territoriality and Lethal Fighting
as Derived Conditions in Ants, below) this implies that territorial ergatoid (fighting) males can monopolize groups of females, but more generally this category
refers to males hovering around the entrances of nests, where clutches of virgin
females mature. This occurs in some social bees and wasps (2, 5, 9, 108) but also
in polygynous (often unicolonial) ants (71).
Two key variables, local density and premating dispersal of females, seem to
explain most of the variation in social insect mate location systems. The lines
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separating the categories (Figure 1) are tentative and will likely be neither straight
nor sharp in real life (compare with Reference 24). For the social Hymenoptera, the
premating dispersal distance of females usually determines the location of mating,
but this is not so for termites, for which dispersal, mate choice, and mating are
strictly separated in time (118). For example, termites normally start with aerial
swarms to disperse before pair formation is initiated, but separation of these two
phases is less clear when males sit on branches and pounce on females passing by
and remain attached to them during the rest of the dispersal flight (91, 118). In other
termites, females call after a dispersal flight (91). Social Hymenoptera therefore
usually have a single position in the parameter space of Figure 1, whereas termites
generally start their dispersal activity somewhere in the upper center and complete
their mate choice activities toward the lower left of the diagram. However, dispersal
followed by calling is also known in some ants (53, 101).
The strength of sexual selection is dependent on female aggregation in space
and time (42): It increases with nonaggregation in time (asynchrony) and with
aggregation in space. Both factors allow a higher variance in male mating success,
with the best males focusing on a single location at a time and inseminating one
female after another. These criteria suggest that the strength of sexual selection
decreases from left to right in Figure 1, although the issue is complicated by the
fact that females are attracted by male aggregations in the top 80% of the figure,
whereas males are attracted by females at the bottom.
Sexual Dimorphism and Premating Sexual Selection
The different mate location systems allow predictions about the relative magnitude
of sexual dimorphism. In spite of the relative ease of collecting data and the
importance of estimating female-to-male cost ratios for studies of sex allocation
(18), sexual dimorphism is notoriously understudied in social insects (115, 120).
To encourage such work, we offer a crude comparative analysis to demonstrate that
simple measures of body size may give important information on the mate location
system and on the forces of premating sexual selection that would typically apply.
With females (queens) under consistent selection for high fertility (and thus
large body size) and males unable to monopolize groups of females, it seems
unlikely to find species in which males are larger than females. Indeed, as a rule
of thumb, social insect males have a body size that is identical to or smaller than
that of females (120), although they are rarely smaller than workers. However,
the variation in sexual dimorphism across species differs significantly among the
major groups of social insects (Figure 2). The rectangles in the figure show that
ants have high variation in sexual size dimorphism, ranging from both sexes being
about equal in size to queens having ∼3 times the body length and ∼25 times the
body mass of males. Variation in sexual dimorphism is much lower in the social
bees, in which queens are at best about 1.5 times as long and 5 times as heavy
as males, and minimal in our small sample of social wasps (difference in mass
is less than or equal to a factor of two). Sexual size dimorphism is universally
low in termites, most likely as a direct result of bi-parental care (90). The ant
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Figure 2 Patterns of sexual dimorphism at the time of mating in the major groups of
social Hymenoptera. The ant sample (n = 20) is from Reference 18, the samples for
bumble bees (n = 10) and social wasps (n = 4) are from Reference 63, and the sample
for honey bees (n = 3) is from Reference 74. Only a single species per genus (the first
one alphabetically in the lists) was included for the ants and social wasps to exclude
most taxonomic confounding. Sexual dimorphism was measured as the cube root of
the weight of a typical male divided by the weight of a typical queen, to be roughly
equivalent to the ratio of body lengths as reported in some handbooks. Species-specific
sexual dimorphism was plotted in a ranked order with different symbols (ants, black
circles; social bees, open circles; social wasps, open squares). The rectangles illustrate
the total variation per group.
genera that have degrees of sexual dimorphism beyond the range of values for
social bees tend to be characterized by mass aerial swarming without a need for
landmarks, a mate location system that does not seem to occur in the social bees
(except in honey bees) and wasps. These groups predominantly occupy the more
competitive mating niches, including male territoriality, which is extremely rare
in ants.
Pre-mating sexual selection has been documented in Pogonomyrmex harvester
ants, in which larger males mate more often and transfer more sperm during
substrate-based swarming (1a, 35, 133, 134). A negative correlation between thorax
weight and sperm content was found in Atta males, which suggests that trade-offs
with flight ability may occur (44). However, in honey bees and a tropical bumble
bee, male sperm load was positively correlated with body size (55, 110). Ants with
a female-calling system, honey bees, and the army ants also have low degrees of
sexual dimorphism. The last two show colony fission and extremely male-biased
sex ratios, selecting for male performance in flight or interference competition
(see The Number of Mating per Male, below), so that males of about the same
size as queens are expected (52, 98). Overall, these comparative data indicate that
sexual dimorphism is often a good predictor variable for mating systems (120)
and that a more systematic study of sex-specific variation in body size parameters
of social insects would give valuable insights into the factors that determine male
and female fitness during pair formation and mating.
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Male Territoriality and Lethal Fighting as
Derived Conditions in Ants
Territorial males of social bees and wasps may attack each other (126) and males
of harvester ants may physically compete for access to receptive queens (1a, 35,
126, 133, 134), but the outcome of such interferences always relies on body size
and stamina, whereas adaptations to harm or kill rival males seem almost completely absent in social insects (115). This makes sense, as the evolution of male
weaponry tends to be associated with the possibility to control groups of females
and to eliminate rival males intermittently and one by one (8). For social insects
this requires pair formation and/or mating in the confined area of the nest before
dispersal of either sex, a situation that is found only in some ants. Below, we review
the selective forces that have shaped the males of these rare ants and the general
concepts on which this understanding builds.
Mating in confined areas has led to the evolution of multiple male morphs
in numerous nonsocial arthropods, in which winged disperser males coexist with
local fighter males with reduced wings (34, 41, 58, 126). Such male polymorphisms
are evolutionarily stable when the number of reproductives eclosing in a specific
compartment is small and variable, so that broods might occasionally have only
females by chance (58). Winged males are then maintained by selection because
they can obtain more fitness by inseminating females in distant compartments
than by competing with brothers for a limited number of intranidal matings. A
comparative analysis in fig wasps has recently corroborated this hypothesis (28).
In ants, multiple male morphs and the complete replacement of winged males
by wingless ones are also associated with mating in the natal nest without prior
dispersal. As long as wingless males compete with brothers, fighting is unlikely to
evolve, because selection through local mate competition reduces the number of
males per clutch to the bare minimum needed to inseminate all females (57). For
example, colonies of some parasitic ants produce only a few peaceful males that
inseminate all their sisters (60, 135), and in another species wingless males and
virgin queens eclose after the death of the mother queen and mate in the nest without
any male-male aggression (139). Wingless males that do engage in lethal fighting
have evolved independently in Hypoponera (58, 140) and Cardiocondyla ants (62,
72, 119). In some of these species, aggressive wingless fighter males coexist with
docile winged disperser males, whereas related species have completely lost the
winged male morph.
Figure 3 summarizes the mating system variation in Cardiocondyla ants as a
function of relatedness and colony size (7, 58). The tropical species Cardiocondyla
obscurior, C. wroughtonii, C. emeryi, and C. minutior have typically small colonies
of less than 50 workers. The first two have up to 15 queens per colony and the
last two somewhat fewer. Worker relatedness is therefore variable (particularly in
C. obscurior and C. wroughtonii owing to the unstable nest sites of these species)
and relatively low on average. All four species produce sexuals in small numbers
throughout the year. Under normal conditions a single territorial ergatoid male
monopolizes mating with emerging nestmates by killing rival males. In the first
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Figure 3 Colony size (log scale) and relatedness among nestmates as key variables
that affect the occurrence and polymorphism of dispersing winged males and territorial fighting (ergatoid) males in Cardiocondyla ants. The triangle indicates that
high-relatedness colonies are rarer than low-relatedness colonies. The relatedness limits of the rectangles and triangle are approximate, as they are inferences based on queen
number per colony. LMC, local mate competition.
two species, ergatoid males have elongated mandibles, with which they injure and
kill callow males and also hold adult rivals while marking them with a pheromone
so that they are subsequently killed by nestmate workers (72, 119). The last two
species have shorter sturdy mandibles, which are used to kill callow rivals but are
less efficient against rivals that have managed to survive long enough to harden their
cuticle. This implies that several ergatoid males may coexist in larger colonies. In
all four species, successful ergatoid males live for several weeks, until their tenure
is taken over by a younger male. Normal winged males are also produced, but
probably only under stressful conditions (29). They disperse, presumably to mate
with virgin queens in other small colonies that have accidentally remained without
an ergatoid male (72). Winged males often mate with nestmate females before
dispersing, apparently escaping attack from the ergatoid male by mimicking the
odor of virgin queens (30).
Colonies of C. mauritanica have up to 200 workers and produce sexuals seasonally (59). With such larger clutches it is highly unlikely that broods remain
without any males. Winged males are thus never produced, but as in C. emeryi and
C. minutior, more than one ergatoid male is occasionally found in larger colonies.
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C. mauritanica is also similar to these two species in that its ergatoid males kill
only callow rivals. Colonies of Cardiocondyla elegans, C. ulianini, and C. batesii
are even larger (100 to 400 workers), but they have a single queen (and thus high
relatedness) and contain several mutually tolerant ergatoid males when the female
sexuals emerge (82).
Multiple queens per colony and low relatedness have likely been ancestral
in the genus Cardiocondyla (J. Heinze, A. Trindl, B. Seifert & K. Yamauchi,
unpublished data), so we infer that males remained polymorphic until colony size
passed a certain threshold at which winged males were lost completely. High
relatedness and mutually tolerant ergatoid males (top-right corner in Figure 3)
would thus be a derived condition, associated with inbreeding, so that relatedness
could potentially increase to values above 0.75. No Cardiocondyla species seems
to follow the most simple local mate competition model with small colonies,
female-biased sex ratios, and one or a few wingless, nonfighting males. Rare and
transient monogynous colonies of C. obscurior and C. wroughtonii tend to have
these colony characteristics but always produce a few ergatoid males, all of which
but one are eliminated by fighting.
Although their typical colony sizes are unknown, similar scenarios may apply in
the two Hypoponera species that have male fighting morphs coexisting with normal
males (58, 140), such that they would fit somewhere at the bottom-left corner of
Figure 3. Several other Hypoponera species (47, 79, 141) have extensive mate
guarding as an alternative to male fighting: Wingless nonfighting males cling to
the cocoons of queen pupae for hours or even days while inserting their genitalia
through an opening in the cocoon in order to mate before these queens eclose.
Another case of male polymorphism in which both morphs have retained their
wings and differ only slightly in dispersal has been reported in two Formica ant
species (48).
Cardiocondyla ants have evolved yet another remarkable adaptation together
with male fighting. Their ergatoid males are the only Hymenoptera known to
date that have life-long spermatogenesis (61), such that the lifetime number of
matings of these males is no longer constrained. Although these social insects
are tiny, this is a spectacular development comparable to that of the hypothetical
descendants of whales, which become terrestrial by re-evolving proper legs. This
illustrates that the forces of sexual selection in social insects can be strong when the
right combination of conditions (low relatedness and the possibility to monopolize
groups of females) is present.
The Number of Matings Per Male
Earlier reviews have hypothesized that most ant males mate only once (23, 32, 65)
and are thus equally monogamous as termite males. However, exceptions seem
common and show male mating frequencies of up to 10 times (64, 135, 137).
Similar inferences in leafcutting ants (19, 45, 99) were recently confirmed by
showing that multiple ejaculations could be provoked from a specialized part of
the accessory testis, which is refilled after each ejaculation (11). Multiple mating
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by males is common in bumble bees and social wasps (2, 105, 126), whereas male
honey bees and stingless bees mate singly (84, 115).
The probability that an average male obtains more than one mating is a function
of the operational sex ratio (23, 126). In most mating systems this ratio depends on
sexual dimorphism (Figure 2), because the same equilibrium sex ratio in terms of
investment may translate into different numerical sex ratios depending on sexual
dimorphism (18, 63). Local mate competition and lethal male fighting may shift
the operational male-to-female sex ratio to values far below 1, whereas colony
fission induces extremely male-biased sex ratios (23). Selection always tends to
maximize the probability of obtaining a first mating, but this is unlikely to be
the case for additional matings (23, 126). Assuming that every male mating is
essentially a random event, the probability of mating 0, 1, 2, or 3 times should be
Poisson distributed. When the operational sex ratio becomes more male-biased,
the mean number of matings per male decreases, but the probability of obtaining
multiple matings decreases much faster than the probability of mating once (Figure 4). Selection thus increasingly promotes traits that maximize the chance of
obtaining any mating instead of traits that allow additional matings. The occurrence of short-lived males with fixed amounts of sperm must therefore imply that
the ability to mate multiply is lost when the operational male-to-female sex ratio
is more male-biased than some threshold value. The vertical arrows in Figure 4
illustrate the additional effect of interference competition (relaxing the assumption
of randomness). This increases the variance in male mating success, i.e., increases
the proportion of multiple matings for the males that manage to mate at all.
Suicidal mating of male honey bees and stingless bees (115) is consistent with
this model, and the same must apply to army ants, which shed their wings when
entering a foreign colony and copulate for hours (23). In ants with sex allocation
ratios between the respective worker and queen optima of 3:1 and 1:1, we expect
that species with aerial swarms and high degrees of sexual size dimorphism also
have males that can mate only once. Expectations such as this are given in Figure
4, but they need to be explicitly tested by further comparative studies of the size
and compartmentalization of the accessory testes (11). The species that mate in
the nest without either sex dispersing before mating (see Male Territoriality and
Lethal Fighting as Derived Conditions in Ants, above) are at the far left of Figure
4. This illustrates once more that the Hamiltonian (57) decoupling of mating and
dispersal shapes these mating systems. That females stay in their maternal colony
allows males to monopolize groups of them, either uncontested (when relatedness
is high; 60, 135, 139) or after killing rivals (when relatedness is low; Figure 3).
POSTMATING SEXUAL SELECTION
Accessory Glands: Have Mating Plug Functions
Been Overlooked?
The accessory glands of male insects are now generally considered to be an extra
set of manipulative chemical genitalia that may affect virtually all aspects of female
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Figure 4 The Poisson probability of mating more than once (i.e., 2, 3, 4. . . times:
(eµ -µ-1)/µ) divided by the Poisson probability of mating once (µ/eµ ) expressed as
proportion, 1-(µ/eµ -1), for operational (male-to-female, m/f) sex ratios between 1:10
and 100:1. µ is the mean number of matings that a male can statistically expect assuming
that queens mate once. Multiple queen-mating has the same effect as shifting the
operational sex ratio toward females. Vertical arrows indicate the effect of interference
competition among males, which is expected when territoriality increases toward the
left-hand side of the figure. The expected position of various mating systems of social
Hymenoptera is indicated. LMC, local mate competition.
reproduction (40, 56). In many insects these glands produce spermatophores or
mating plugs, which are meant to monopolize paternity of a clutch (56, 126).
Similar mechanisms have been hypothesized to help males of social Hymenoptera
to monopolize paternity of a queen’s lifetime reproduction (23). Males of Carebara
and Diacamma ants leave spermatophores in the female genital tract (6, 100, 101).
In Diacamma, male mating is suicidal (6), which suggests that excessive accessory
gland use for paternity guarding may make males lose the ability to mate more
than once even if the operational sex ratio is not male-biased.
Male bumble bees deposit mating plugs, which effectively prevent intromission by subsequent males and demotivate queens to continue sexual activity (13,
14, 25, 109). Similar mating plugs occur in fire ants (85) and most likely in
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fungus-growing ants (11). Females are obligatorily singly mated in most of these
cases except Bombus hypnorum (25) and Acromyrmex and Atta leafcutter ants
(131). In the last two, accessory gland size is reduced, so that the size ratio of
the accessory testes (the enlarged parts of the seminal vesicles that store mature
sperm) and accessory glands (mating plug investment) can be used as a predictor of single and multiple mating (11). The inquiline social parasite Acromyrmex
insinuator has reverted almost completely to single queen-mating (121), but its
male genitalia only partly reflect this reversal (11). Investments in sperm and accessory gland mass are both intermediate, but together they exceed an investment
that would fit on a linear trade-off line. This suggests that partial multiple mating
of queens imposes disproportionate costs that render an intermediate mating system unstable in fungus-growing ants. Partial multiple mating of queens has indeed
never been found in any free-living species (131), in spite of this being a relatively
common mating system in other social Hymenoptera (20, 117). Similar measurements in other social insect tribes that combine single and multiple queen-mating
and have both free-living and socially parasitic species would be valuable to test
the generality of these trends.
Mating plugs can be highly functional even when invisible from the outside (14,
38, 109). This implies that they may be much more widespread than previously
assumed and that explicit studies of their presence and function should have high
priority to establish whether they do occur in most if not all social Hymenoptera
with obligatorily singly mated queens (20, 117). A general association of mating
plugs and single queen-mating would imply that there is much more male-control
over mating in social Hymenoptera than has previously been acknowledged. This
conclusion would stand even when secondary developments occasionally reverse
male-control, as seems to have happened in Apis honey bees with their derived
“mating signs” (73, 138), but not in the predominantly singly mating stingless bees
(96, 97).
In the lower termites, accessory gland compounds with unknown functions are
expelled with the sperm (132), but the accessory glands have apparently been lost
in the higher termites. It would be interesting to establish whether this loss precedes, coincides with, or follows the emergence of aflagellate sperm (see below)
and whether either of these transitions is linked to the emergence of central site
nesting, i.e., the separation of nest site and foraging range, which effectively precluded colony mixing and enforced lifelong functional monogamy. The direction
of change suggests that accessory glands are ultimately redundant in an exclusively
monogamous mating system.
Further studies of accessory glands in social insects may also help to shed light
on male precedence in paternity. This has been extensively studied in nonsocial
insects (112), but it is difficult to address in social insects, because copulations
can be observed in only a few species. The studies that are available only concern
patterns of multiple paternity and show significant inequalities in paternity among
males (21, 25, 43, 46, 49, 51, 94, 121). In Lasius and Formica ants the extent of
paternity skew tends to be negatively correlated with the frequency of multiple
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mating (21, 22). This pattern may be consistent with mating plugs becoming less
effective when multiple mating increases in frequency (so that later males can store
more equal amounts of sperm; 25), but a number of other explanations are also
potentially applicable (21, 22).
Paternity Manipulation, But No Sperm Displacement
Displacement of sperm, a typically promiscuous trait in nonsocial insects, seems
to be absent in social insects (23) and the active killing of rival males appears rare
(Figure 3). In species with multiply mated queens, sperm of different males is normally deposited in the bursa copulatrix some distance away from the spermatheca
so that sperm competition for storage will occur.
Accessory gland compounds that play an active role in this competition process are increasingly discovered (56), but the evolution of such traits in social
Hymenoptera is constrained. In nonsocial insects, mechanisms of sperm competition that negatively affect female survival might be selected when oviposition
takes place shortly after mating (26, 56), but not in social insects in which male
reproductive fitness comes with a considerable time lag because colonies will not
produce reproductives unless a number of cohorts of sterile workers have been
produced first (10, 11). As a result, arms races between males and females (26,
67) are less likely to evolve in social insects, so that postmating sexual selection
is more likely to be based on cryptic female choice (40). The only mechanism
for directly manipulating the sperm storage process during or immediately after
mating that has been demonstrated is ejaculation directly into the spermatheca.
This has been documented in two species of dwarf honey bees (75, 76), in which
drones are significantly more powerful in flight performance than drones of other
honey bees (98). A similar mechanism has evolved in Atta leafcutting ants (B.
Baer, unpublished data).
Sperm Length Versus Sperm Number: Production
and Storage Constraints
When competing for storage, longer sperm likely moves faster but is more expensive to produce and store. Although the generality of this idea is currently being
disputed (112), it is almost unimaginable that it would not apply to social insects
because of the idiosyncratic production and storage constraints in the Hymenoptera
and the general monogamy of the termites. When males eclose with a fixed amount
of sperm, there is a trade-off between making many short sperm and fewer longer
sperm, and when the size of mature colonies increases, shorter sperm is likely
to be favored because more of it can be stored to fulfill the lifetime reproductive
potential of a hymenopteran queen and her mate. In social Hymenoptera, sperm
length should thus decrease with colony size as long as there is one singly mated
queen per colony. This trend is expected to reverse when polygyny evolves in
species with medium-to-large colonies, as this would relax the fertility demands
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of queens, and when multiple queen-mating evolves, as this would add a novel
directional selection component for faster sperm. In termites, however, there are
neither production nor storage constraints, such that the need for longer and faster
sperm should reflect the likelihood of deviations from lifetime monogamy. Concepts such as this assume that there is additive genetic variation for sperm length
so that it can respond to selection, a contention that was recently confirmed for
the bumble bee Bombus terrestris (B. Baer, G. de Jong, P. Schmid-Hempel, R.
Schmid-Hempel, J.T. Høeg & J.J. Boomsma, unpublished manuscript).
Bombus hypnorum has facultatively multiply mated queens (25) and significantly longer sperm than B. terrestris and B. lucorum, which have singly mated
queens (15). No obligatorily multiply mating bumble bees are known, but sperm
length is significantly longer in Apis honey bees than in any of these bumble bees
(80), which suggests that higher queen-mating frequencies in social bees are associated with longer sperm. Sperm length in termites has apparently evolved in the opposite direction. The most basal termite family still has flagellate sperm, but sperm
tails were lost subsequently when amoeboid sperm evolved. The most derived termites (Rhinotermitidae and Termitidae) have completely nonmotile round-shaped
sperm (68). The termite data thus indicate that a permanent absence of sperm competition allows sperm to get shorter, even when males do not hatch with a fixed
amount of sperm.
In the fungus-growing ants, sperm is long in the most basal genera with small,
short-lived colonies. It decreases in length with increasing colony size in the more
derived clades, only to increase again in some Atta leafcutting ants (B. Baer &
J.J. Boomsma, manuscript in preparation). This fits the trade-off and constraint assumptions outlined above (Figure 5). The ancestral fungus-growing ants had single
queen-mating and small, relatively short-lived colonies (11, 131). Small ejaculates
thus sufficed and rapid sperm storage probably had some fitness advantage, maintaining long sperm in the absence of significant storage constraints. When colony
size and queen longevity increased, shorter sperm evolved because the advantage
of storing more sperm probably became significant. Attine colonies never became
large before multiple queen-mating evolved, but the sperm of Solenopsis fire ants
with obligatorily singly mating queens (107) and large colonies is shorter than that
of any attine ant, which is consistent with expectation (81).
Multiple queen-mating evolved in the ancestor of the Acromyrmex and Atta leafcutter ants (131) and is expected to select for longer sperm, unless spermatheca
storage constraints preclude such development. These constraints are illustrated
by the two vertically arrowed rectangles in Figure 5, indicating that their position may be anywhere between the typical sperm length before multiple mating
evolved and some biologically feasible maximum. The data seem to confirm this,
with Acromyrmex sperm having not increased in length, whereas sperm length is
significantly longer in some Atta species than in sister genera of higher attine ants
that have maintained single queen-mating (B. Baer & J.J. Boomsma, manuscript
in preparation). Spermatheca size (both absolute and relative to queen body size
and fecundity) may explain part of this variation, as the size of the sperm storage
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Figure 5 The inferred trade-off between sperm length and sperm number in eusocial
Hymenoptera, assuming that longer sperm moves faster and reaches the storage organ
more effectively but has higher production costs. The vertical line marks the transition
from single to multiple mating, as happened, for example, in the ancestor of the leafcutting ants and the honey bees. The concave, decreasing curve represents the normal
sperm storage constraint, applying to all species. The two curves toward the right are
hypothetical increases in sperm length after multiple mating evolved, until stopped by
some dynamic ultimate storage constraint (vertically arrowed rectangles).
organ may vary considerably even among species with queens of similar size (e.g.,
C. obscurior and C. minutior; E. Darouzzet, unpublished data).
Sexual selection for longer sperm in social Hymenoptera with obligate multiple
mating is expected to reach some dynamic equilibrium with the female storage
constraints. However, these constraints may become relaxed when queen body
size increases, which is likely as obligate multiple mating of queens is associated
with large colony size (20). At such dynamic equilibrium, males may well produce
sperm longer than necessary for the lifetime reproductive success of queens. This
may be one of the few female-male arms races that can be maintained in social
Hymenoptera, because its consequences (a lower number of lifetime fertilized
eggs) affect the survival of colonies that have already reached the reproductive
phase and not the probability of colonies reaching that stage. The evolution of
dwarf honey bee males depositing their sperm directly into the spermatheca would
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be an ultimate male move in this arms race to which females would probably
have no response. It would be interesting to know whether these bees have shorter
sperm, as the strength of selection for longer sperm is likely to be lower when
competition for storage no longer applies.
Sperm Competition after Storage and Cryptic Female Choice
In termites, sperm mortality has been hypothesized to be potentially significant (40)
because females mate repeatedly with the same male so that sperm is abundantly
available and not selected for longevity. In contrast, the Hymenoptera have limited
amounts of long-lived sperm and use it efficiently after storage, an economy that is
undoubtedly influenced by the lack of intraejaculate sperm competition due to the
clonal nature of hymenopteran sperm (10, 11, 112). Some social Hymenoptera are
incredibly economic, such as monandrous Solenopsis fire ant queens, which use
on average only 2.6 to 3.5 sperm per fertilized egg (128, 129). Honey bee queens
mate with 10 to 20 males, store one male’s worth of sperm, and use 5 to 14 sperm
per egg (10). This implies that even with multiple matings, prestorage and poststorage sperm competition are of the same order of magnitude. In Atta colombica
both figures are also similar and probably below 5 sperm per egg (44, 45), whereas
Dolichovespula wasps with facultative multiple mating of queens (49) seem intermediate with approximately 7 sperm per egg (116). Overall, these sperm-to-egg
ratios are similar to those found in nonsocial, parasitoid Hymenoptera (27), but
that they can be maintained after years or even decades of sperm storage illustrates
the amazing viability of sperm in social Hymenoptera and suggests that stored
sperm may be physiologically quite different from sperm found in noneusocial
Hymenoptera (56). However, even though sperm viability is universally high, both
genetic and environmental variations are likely to exist. These variations and their
possible causes and results deserve to be explicitly studied, either by comparing
sperm storage and reproductive fitness of queens inseminated with semen of specific males (15, 77) or by comparing the representation of patrilines throughout
the years in long-lived colonies (122).
A re-analysis of comparative data (32, 54, 92) for ants (n = 5), social bees
(n = 28), and social wasps (n = 11) showed that the number of sperm stored by
a queen tends to increase isometrically (log-log slope ∼ 1) or allometrically (loglog slope >1) with the sperm complement of a typical conspecific male. However,
these steep slopes are an artifact of the taxonomic heterogeneity of these overall
data sets, as slopes within bee genera were lower than 1 (Bombus: slope = 0.632,
standard error (SE) = 0.152, n = 7, probability (P) = 0.052 for difference with
a slope of 1; Apis: slope = 0.398, SE = 0.095, n = 7, P < 0.001 for difference
with a slope of 1). The latter slopes indicate that stored sperm does not increase
proportionally to male sperm stores, either because males of larger Bombus species
mate with more females so that ejaculate size is a smaller fraction of their sperm
store, or because queens of larger Apis species mate with more males but without
storing more sperm.
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For ants it has further been established that the number of stored sperm increases
allometrically (slope = 1.599, SE = 0.231, n = 26, P = 0.0163 for difference
with a slope of 1) with queen ovariole number (128). Also this steep slope may
be an artifact of the heterogeneity of the data set, but an alternative explanation
may be that the rate of oocyte production per ovary increases in species with more
fertile queens (87). Atta and Acromyrmex leafcutting ants store more sperm than
predicted on the basis of their typical number of ovarioles (128), but this does not
necessarily imply a steeper allometric slope, as the two basal attine ants in the
same data set have positive residuals as well. A re-analysis (ANCOVA) of the data
(128) separating attine (n = 4) and nonattine (n = 22) ants indicated that the
slopes were homogeneous (P = 0.984) but that the difference of intercepts was
approaching significance (P = 0.095). A larger sample is needed to settle this issue,
but there is yet no convincing evidence that multiply mated attine queens store and
use more sperm per egg than singly mated attine queens, for example, to allow for
competition among the sperm of different fathers for the fertilization of eggs. In the
honey bee, evidence for such sperm competition is also negative or ambiguous (51
and references therein). Sperm mixing is already substantial in the bursa copulatrix
and tends to be almost complete a few months after storage (50, 78). In contrast,
considerable sperm clumping and variable patterns of paternity across years were
observed in the facultatively multiply mating ant Formica truncorum (122). Here,
however, relatedness-induced split sex ratios make sperm clumping a direct fitness
interest for the fathers. This adaptive response suggests that sperm clumping is a
heritable trait that can be selected if there is a clear fitness interest.
Most known mechanisms of female choice (40) are not applicable to the social
insects, but some seem to offer realistic possibilities for cryptic postmating female
choice. First, queens may resist the transport of sperm from unwanted males to the
sperm storage organ. This seems likely, as the sperm storage process is affected
by active and passive female factors in honey bees (75). Second, multiply mating
queens may have evolved sperm storage barriers, for example, in the form of a long,
contorted, and complicated spermathecal duct, which may serve for both cryptic
female choice in sperm storage and differential sperm use for fertilization (40).
Third, male ants (23) and social bees (102) may have elaborate genital architecture.
These traits are in part naturally selected to help males stay attached to queens
during mating, but they may also represent Fisherian runaway sexual selection
following cryptic female choice (67), particularly when the extent of elaboration
is higher in species with multiply mated females, as data for bees (102) indicate.
This contrasts with genital morphology in termites, which is simple compared with
their cockroach-like ancestors (40, 132).
CONCLUSIONS
A key question in sexual selection is whether it is the males or the females that
determine the identity of successful males (24). Also, in social insects there
is no simple answer to this question, but we have offered some contours of a
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conceptual framework that may ultimately allow an integrated understanding of
the male and female components of sexual selection across the different groups of
eusocial insects. In all four major groups considered here, sexual selection seems
relatively weak in both males and females, as entire groups such as the higher
termites and the obligatorily singly mating ants, bees, and wasps may not have any
sexual selection beyond premating partner choice. However, the ample availability
of these monogamous groups allows a relatively precise comparative evaluation of
sexually selected traits in sister groups in which one or both sexes mate multiply.
Other interesting contrasts are provided by bizarre adaptations in some derived
taxa, such as the fighting Cardiocondyla males with continuous sperm production, and by the major differences in longevity and sperm storage between the
annual and perennial social Hymenoptera and between the perennial ants and
termites.
The short available time frame for lifetime mate choice in social insects may
well imply that queens can discriminate only according to innate minimum criteria of male quality and mate with the first male(s) that fulfills these. Starr (115)
argued that this leaves little room for female choice, and Alexander et al. (4)
added that this was particularly true for arbitrary female choice of male traits
shaped by runaway selection. However, the social Hymenoptera do not leave
much room for the alternative of female choice for direct benefits or good genes
either, although these mechanisms may play a role in termite mate choice. On
the basis of the data reviewed here, we tentatively conclude that (cryptic) female choice seems to be a more attractive general framework than sexual conflict
models, although antagonistic sexual coevolution may happen occasionally. We
further stress that premating male manipulation strategies via mating plugs have
probably been systematically overlooked, such that the mating systems of social Hymenoptera may be more male controlled than previously acknowledged.
Both detailed comparative analyses and in-depth experimental studies are badly
needed. Of these, the comparative study of sexual dimorphism and male genitalia seem relatively easy and straightforward, whereas others, such as the explicit study of male precedence, sperm traits, female genitalia and spermathecae,
and the selectiveness and cost of long-term sperm storage, will be technically
challenging.
ACKNOWLEDGMENTS
Our work was supported by a research award from the Alexander von Humboldt
Foundation (JJB), grants from the Danish Natural Science Research Council (JJB
and BCB) and the Deutsche Forschungsgemeinschaft (JH: He 1623/12–2), and
the EU-Research-Training Network INSECTS (contract HPRN-CT-2000–00,052).
Walter Tschinkel and Rob Page provided unpublished data from previous reviews,
and David Nash helped with the formatting of the figures. The final version benefited from comments by Duur Aanen, Sophie Armitage, Barbara Baer Imhoof,
Lisbeth Børgesen, Sylvia Cremer, Patrizia D’Ettorre, Mischa Dijkstra, Susanne
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Foitzik, Judith Korb, Daniel Kronauer, David Nash, Jes Pedersen, and Michael
Poulsen.
The Annual Review of Entomology is online at http://ento.annualreviews.org
LITERATURE CITED
1. Abe T, Bignell DE, Higashi M, eds. 2000.
Termites: Evolution, Sociality, Symbiosis,
Ecology. Dordrecht: Kluwer Academic
1a. Abell AJ, Cole BJ, Reyes R, Wiernasz DC.
1999. Sexual selection on body size and
shape in the western harvester ant, Pogonomyrmex occidentalis Cresson. Evolution
53:535–45
2. Akre RD. 1982. Social wasps. See Ref.
63a, 4:1–105
3. Alcock J, Smith AP. 1987. Hilltopping,
leks and female choice in the carpenter
bee Xylocopa (Neoxylocopa) varipuncta.
J. Zool. 211:1–10
4. Alexander RD, Marshall DC, Cooley JR.
1997. Evolutionary perspectives on insect
mating. See Ref. 27a, pp. 4–31
5. Alford DV. 1975. Bumblebees. London:
Davie-Poynter. 352 pp.
6. Allard D, Gobin B, Ito F, Tsuji K, Billen
J. 2002. Sperm transfer in the Japanese
queenless ant Diacammasp. (Hymenoptera: Formicidae). Neth. J. Zool. 52:77–
86
7. Anderson C, Cremer S, Heinze J. 2003.
Live and let die: why fighter males of
the ant Cardiocondyla kill each other but
tolerate their winged rivals. Behav. Ecol.
14:54–62
8. Andersson M. 1994. Sexual Selection.
Princeton, NJ: Princeton Univ. Press. 599
pp.
9. Ayasse M, Paxton RJ, Tengö J. 2001. Mating behavior and chemical communication in the order Hymenoptera. Annu. Rev.
Entomol. 46:31–78
10. Baer B. 2003. Bumblebees as model organisms to study male sexual selection
in social insects. Behav. Ecol. Sociobiol.
54:521–33
11. Baer B, Boomsma JJ. 2004. Male reproductive investment and queen mating frequency in fungus growing ants. Behav.
Ecol. 15:426–32
12. Deleted in proof
13. Baer B, Maile R, Schmid-Hempel P, Morgan ED, Jones GR. 2000. Chemistry of
a mating plug in bumblebees. J. Chem.
Ecol. 26:1869–75
14. Baer B, Morgan ED, Schmid-Hempel P.
2001. A non-specific fatty acid within the
bumblebee mating plug prevents females
from remating. Proc. Natl. Acad. Sci. USA
98:3926–28
15. Baer B, Schmid-Hempel P, Hoeg JT,
Boomsma JJ. 2003. Sperm length, sperm
storage and mating system characteristics
in bumblebees. Insectes Soc. 50:101–8
16. Beani L, Cervo R, Lorenzi CM, Turillazzi S. 1992. Landmark-based mating
systems in four Polistes species (Hymenoptera: Vespidae). J. Kans. Entomol.
Soc. 65:211–17
17. Beani L, Turillazzi S. 1990. Overlap at
landmarks by lek-territorial and swarming
males of two sympatric polistine wasps
(Hymenoptera: Vespidae). Ethol. Ecol.
Evol. 2:419–31
18. Boomsma JJ. 1989. Sex investment ratios
in ants: Has female bias been systematically overestimated? Am. Nat. 133:517–
32
19. Boomsma JJ, Fjerdingstad EJ, Frydenberg J. 1999. Multiple paternity, relatedness and genetic diversity in Acromyrmex
leafcutter ants. Proc. R. Soc. London Sci.
Ser. B 266:249–54
20. Boomsma JJ, Ratnieks FLW. 1996. Paternity in eusocial Hymenoptera. Philos.
Trans. R. Soc. London Ser. B 351:947–75
28 Oct 2004 20:17
AR
AR234-EN50-17.tex
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
SOCIAL INSECT MALES
21. Boomsma JJ, Sundström L. 1998. Patterns
of paternity skew in Formica ants. Behav.
Ecol. Sociobiol. 42:85–92
22. Boomsma JJ, van der Have TM. 1998.
Queen mating and paternity variation in
the ant Lasius niger. Mol. Ecol. 7:1709–
18
23. Bourke AFG, Franks NR. 1995. Social
Evolution in Ants. Princeton, NJ: Princeton Univ. Press. 529 pp.
24. Bradbury JW. 1985. Contrasts between insects and vertebrates in the evolution of
male display, female choice, and lek mating. See Ref. 65a, pp. 273–89
25. Brown MJF, Baer B, Schmid-Hempel R,
Schmid-Hempel P. 2002. Dynamics of
multiple mating in the bumblebee Bombus hypnorum. Insectes Soc. 49:315–19
26. Chapman T, Arnqvist G, Bangham J,
Rowe L. 2003. Sexual conflict. Trends
Ecol. Evol. 18:41–47
27. Chevrier C, Bressac C. 2002. Sperm storage and use after multiple mating in Dinarmus basalis (Hymenoptera: Pteromalidae). J. Insect Behav. 15:385–98
27a. Choe JC, Crespi BJ, eds. 1997. Mating
Systems in Insects and Arachnids. Cambridge, UK: Cambridge Univ. Press
27b. Choe JC, Crespi BJ, eds. 1997. Social
Behavior in Insects and Arachnids. Cambridge, UK: Cambridge Univ. Press
28. Cook JM, Compton SG, Herre EA, West
SA. 1997. Alternative mating tactics and
extreme male dimorphism in fig wasps.
Proc. R. Soc. London Sci. Ser. B 264:747–
54
29. Cremer S, Heinze J. 2003. Stress
grows wings: environmental induction of
winged and dispersal males in Cardiocondyla. Curr. Biol. 13:219–23
30. Cremer S, Sledge MF, Heinze J. 2002.
Male ants disguised by the queen’s bouquet. Nature 419:897
31. Crozier RH, Fjerdingstad EJ. 2001.
Polyandry in social Hymenoptera: disunity in diversity? Ann. Zool. Fenn.
38:267–85
32. Crozier RH, Page RE. 1985. On being the
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
P1: GCE
415
right size: male contributions and multiple mating in social Hymenoptera. Behav.
Ecol. Sociobiol. 18:105–15
Crozier RH, Pamilo P. 1996. Evolution
of Social Insect Colonies. Oxford, UK:
Oxford Univ. Press. 306 pp.
Danforth BF, Desjardins CA. 1999. Male
dimorphism in Perdita portalis (Hymenoptera, Andrenidae) has arisen from
preexisting allometric patterns. Insectes
Soc. 46:18–28
Davidson DW. 1982. Sexual selection
in harvester ants (Formicidae: Pogonomyrmex). Behav. Ecol. Sociobiol. 10:245–
50
DeHeer CJ, Vargo EL. 2004. Colony genetic organization and colony fusion in the
termite Reticulitermes flavipes as revealed
by foraging patterns over time and space.
Mol. Ecol. 13:431–41
Dumser JB. 1980. The regulation of spermatogenesis in insects. Annu. Rev. Entomol. 25:341–69
Duvoisin N, Baer B, Schmid-Hempel P.
1999. Sperm transfer and male competition in a bumblebee. Anim. Behav.
58:743–49
Eberhard WG. 1985. Sexual Selection and
Animal Genitalia. Cambridge, MA: Harvard Univ. Press. 244 pp.
Eberhard WG. 1996. Female Control:
Sexual Selection by Cryptic Female
Choice. Princeton, NJ: Princeton Univ.
Press. 501 pp.
Emlen DJ. 1997. Alternative reproductive tactics and male-dimorphism in the
horned beetle Onthophagus acuminatus
(Coleoptera: Scarabaeidae). Behav. Ecol.
Sociobiol. 41:335–41
Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating
systems. Science 197:215–23
Fernández-Escudero I, Pamilo P, Seppä P.
2002. Biased sperm use by polyandrous
queens of the ant Proformica longiseta.
Behav. Ecol. Sociobiol. 51:207–13
Fjerdingstad EJ, Boomsma JJ. 1997. Variation in size and sperm content of sexuals
28 Oct 2004 20:17
416
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
AR
AR234-EN50-17.tex
BOOMSMA
BAER
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
P1: GCE
HEINZE
in the leafcutter ant Atta colombica. Insectes Soc. 44:209–18
Fjerdingstad EJ, Boomsma JJ. 1998. Multiple mating increases the sperm stores of
Atta colombica leafcutter ant queens. Behav. Ecol. Sociobiol. 42:257–61
Fjerdingstad EJ, Gertsch PJ, Keller L.
2003. The relationship between multiple
mating by queens, within-colony genetic
variability and fitness in the ant Lasius
niger. J. Evol. Biol. 16:844–53
Foitzik S, Heinze J, Oberstadt B, Herbers
JM. 2002. Mate guarding and alternative
reproductive tactics in the ant Hypoponera opacior. Anim. Behav. 63:597–604
Fortelius W, Pamilo P, Rosengren R,
Sundström L. 1987. Male size dimorphism and alternative reproductive tactics
in Formica exsecta ants (Hymenoptera,
Formicidae). Ann. Zool. Fennici 24:45–54
Foster KR, Ratnieks FLW. 2001. Paternity, reproduction and conflict in vespine
wasps: a model system for testing kin selection predictions. Behav. Ecol. Sociobiol. 50:1–8
Franck P, Coussy H, Le Conte Y, Solignac
M, Garnery L, Cornuet J-M. 1999. Microsatellite analysis of sperm in honeybee.
Insect Mol. Biol. 8:419–21
Franck P, Solignac M, Vautrin D, Cornuet J-M, Koeniger G, Koeniger N. 2002.
Sperm competition and last-male precedence in the honeybee. Anim. Behav.
64:503–9
Franks NR, Hölldobler B. 1987. Sexual
competition during colony reproduction
in army ants. Biol. J. Linn. Soc. 30:229–43
Franks NR, Sendova-Franks AB,
Sendova-Vassileva M, Vassilev L. 1991.
Nuptial flights and calling behaviour in
the ant Leptothorax acervorum (Fabr.).
Insectes Soc. 38:327–30
Garofalo CA. 1980. Reproductive aspects and evolution of social behavior in
bees (Hymenoptera, Apoidea). Rev. Bras.
Genet. 3:139–52
Garofalo CA, Zucchi R, Muccillo G.
1986. Reproductive studies of a neotrop-
56.
57.
58.
59.
60.
61.
62.
63.
63a.
64.
65.
65a.
66.
ical bumblebee, Bombus atratus (Hymenoptera, Apidae). Rev. Bras. Genet.
9:231–43
Gillott C. 2003. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev.
Entomol. 48:163–84
Hamilton WD. 1967. Extraordinary sex
ratios. Science 156:477–88
Hamilton WD. 1979. Wingless and fighting males in fig wasps and other insects. In
Sexual Selection and Reproductive Competition in Insects, ed. MS Blum, NA
Blum, pp. 167–220. New York: Academic
Heinze J. 1999. Male polymorphism in
the ant Cardiocondyla minutior (Hymenoptera: Formicidae). Entomol. Gener.
23:251–58
Heinze J. 2000. Testes degeneration and
limited sperm supply in ant males with
intranidal mating. Mitt. Dtsch. Ges. Allg.
Angew. Entomol. 12:207–10
Heinze J, Hölldobler B. 1993. Fighting for
a harem of queens: physiology of reproduction in Cardiocondyla male ants. Proc.
Natl. Acad. Sci. USA 90:8412–14
Heinze J, Hölldobler B, Yamauchi K.
1998. Male competition in Cardiocondyla
ants. Behav. Ecol. Sociobiol. 42:239–46
Helms KR. 1994. Sexual size dimorphism
and sex ratios in bees and wasps. Am. Nat.
143:418–34
Hermann HR. 1982. Social Insects, Vols.
3, 4. New York: Academic
Hölldobler B. 1976. The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex).
Behav. Ecol. Sociobiol. 1:405–29
Hölldobler B, Bartz SH. 1985. Sociobiology of reproduction in ants. See Ref. 65a,
pp. 237–57
Hölldobler B, Lindauer M, eds. 1985. Experimental Behavioral Ecology and Sociobiology. Stuttgart/New York: Gustav
Fischer
Hölldobler B, Wilson EO. 1990. The Ants.
Cambridge, MA: Harvard Univ. Press.
732 pp.
28 Oct 2004 20:17
AR
AR234-EN50-17.tex
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
SOCIAL INSECT MALES
67. Hosken DJ, Stockley P. 2004. Sexual selection and genital evolution. Trends Ecol.
Evol. 19:87–93
68. Jamieson BGM. 1987. The Ultrastructure
and Phylogeny of Insect Spermatozoa.
Cambridge/New York: Cambridge Univ.
Press. 320 pp.
69. Keller L, ed. 1993. Queen Number and
Sociality in Insects. Oxford: Oxford Univ.
Press. 439 pp.
70. Keller L. 1998. Queen lifespan and colony
characteristics in ants and termites. Insectes Soc. 45:235–46
71. Keller L, Passera L. 1992. Mating system,
optimal number of matings, and sperm
transfer in the Argentine ant Iridomyrmex
humilis. Behav. Ecol. Sociobiol. 31:359–
66
72. Kinomura K, Yamauchi K. 1987. Fighting
and mating behaviors of dimorphic males
in the ant Cardiocondyla wroughtoni. J.
Ethol. 5:75–81
73. Koeniger G. 1990. The role of the mating sign in honey bees, Apis mellifera L.:
Does it hinder or promote multiple mating? Anim. Behav. 39:444–49
74. Koeniger G, Koeniger N, Tingek S, Kelitu
A. 2000. Mating flights and sperm transfer
in the dwarf honeybee Apis andreniformis
(Smith, 1858). Apidologie 31:301–11
75. Koeniger N, Koeniger G. 2000. Reproductive isolation among species of the
genus Apis. Apidologie 31:313–39
76. Koeniger N, Koeniger G, Wongsiri S.
1989. Mating and sperm transfer in Apis
florea. Apidologie 20:413–18
77. Korner P, Schmid-Hempel P. 2003. Effects of sperm on female longevity in
the bumblebee Bombus terrestris L. Proc.
R. Soc. London Sci. Ser. B (Suppl.) 270:
S227–29
77a. Krishna K, Weesner FM, eds. 1969. Biology of Termites, Vol. 1. New York: Academic
78. Laidlaw HH, Page RE. 1985. Polyandry in
honey bees (Apis mellifera L.): sperm utilization and intracolony genetic relationships. Genetics 108:985–97
P1: GCE
417
79. LeMasne G. 1956. La signification des reproducteurs aptères chez la fourmi Ponera
eduardi Forel. Insectes Soc. 3:239–59
80. Lensky Y, Ben David E, Schidler H. 1979.
Ultrastructure of the spermatozoan of the
mature drone honey bee Apis mellifera. J.
Apic. Res. 18:264–71
81. Lino Neto J, Dolder H. 2002. Sperm
structure and ultrastructure of the fire ant
Solenopsis invicta (Buren) (Hymenoptera, Formicidae). Tissue Cell 34:124–
28
82. Marikovskii PI, Yakushkin VT. 1974. Muraveij Cardiocondya uljanini Em., 1889 i
sistematicheskoe polozhenie “paraziticheskogo murav’ya Xenometra”. Izv. Akad.
Nauk Kazakhskoy SSR Ser. Biol. 3:57–62
83. Matsuura K, Nichida T. 2001. Colony fusion in a termite: What makes the society
“open”? Insectes Soc. 48:378–83
84. Michener CD. 1974. The Social Behavior of the Bees. Cambridge, MA: Harvard
Univ. Press. 558 pp.
85. Mikheyev AS. 2003. Evidence for mating
plugs in the fire ant Solenopsis invicta. Insectes Soc. 50:401–2
86. Miles TG, Nutting WL. 1988. Termite
eusocial evolution: a re-examination of
Bartz’s hypothesis and assumptions. Q.
Rev. Biol. 63:1–23
87. Murakami T, Higashi S, Windsor D.
2000. Mating frequency, colony size,
polyethism and sex ratio in fungusgrowing ants (Attini). Behav. Ecol. Sociobiol. 48:276–84
88. Nalepa CA, Bandi C. 2000. Characterizing the ancestors: paedomorphosis and
termite evolution. See Ref. 1, pp. 53–
76
89. Nalepa CA, Bell WJ. 1997. Postovulation
parental investment and parental care in
cockroaches. See Ref. 27b, pp. 26–51
90. Nalepa CA, Miller LR, Lenz M. 2001.
Flight characteristics of Mastotermes darwiniensis (Isoptera, Mastotermitidae). Insectes Soc. 48:144–48
91. Nutting WL. 1969. Flight and colony
foundation. See Ref. 77a, 1:233–82
28 Oct 2004 20:17
418
AR
AR234-EN50-17.tex
BOOMSMA
BAER
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
P1: GCE
HEINZE
92. Page RE Jr. 1986. Sperm utilization in social insects. Annu. Rev. Entomol. 31:297–
320
93. Page RE Jr, Metcalf RA. 1982. Multiple
mating, sperm utilization, and social evolution. Am. Nat. 119:263–81
94. Palmer KA, Oldroyd BP. 2001. Mating
frequency in Apis florea revisited (Hymenoptera, Apidae). Insectes Soc. 48:40–
43
95. Pamilo P. 1991. Life span of queens in
the ant Formica exsecta. Insectes Soc.
38(2):111–20
96. Paxton RJ. 2000. Genetic structure of
colonies and a male aggregation in the
stingless bee Scaptotrigona postica, as revealed by microsatellite analysis. Insectes
Soc. 47:63–69
97. Peters JM, Queller DC, ImperatrizFonseca VL, Roubik DW, Strassmann JE.
1999. Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc. R. Soc. London Sci. Ser. B.
266:379–84
98. Radloff SE, Hepburn HR, Koeniger G.
2003. Comparison of flight design of
Asian honeybee drones. Apidologie 34:1–
6
99. Reichardt AK, Wheeler DE. 1996. Multiple mating in the ant Acromyrmex versicolor: a case of female control. Behav.
Ecol. Sociobiol. 38:219–25
100. Robertson HG. 1995. Sperm transfer in
the ant Carebara vidua F. Smith (Hymenoptera: Formicidae). Insectes Soc.
42:411–18
101. Robertson HG, Villet M. 1989. Mating behavior in three species of myrmicine ants
(Hymenoptera: Formicidae). J. Nat. Hist.
23:767–73
102. Roig-Alsina A. 1993. The evolution of the
apoid endophallus, its phylogenetic implications, and functional significance of the
genital capsule (Hymenoptera, Apoidea).
Boll. Zool. 60:169–83
103. Roisin Y. 2000. Diversity and evolution of
caste patterns. See Ref. 1, pp. 95–119
104. Roonwal ML. 1975. Sex ratios and sexual
105.
106.
107.
108.
109.
110.
111.
112.
113.
114.
115.
dimorphism in termites. J. Sci. Ind. Res.
34:402–16
Röseler PF. 1973. Die Anzahl der Spermien im Receptaculum Seminis von
Hummelköniginnen (Hymenoptera, Apidea, Bombinae). Apidologie 4:267–74
Ross KG, Carpenter JM. 1991. Population
genetic structure, relatedness, and breeding systems. In The Social Biology of
Wasps, ed. KG Ross, RW Matthews, pp.
451–79. Ithaca, NY: Cornell Univ. Press
Ross KG, Vargo EL, Fletcher DC. 1988.
Colony genetic structure and queen mating frequency in fire ants of the subgenus
Solenopsis (Hymenoptera: Formicidae).
Biol. J. Linn. Soc. 34:105–17
Sakagami SF. 1982. Stingless bees. See
Ref. 63a, 3:361–423
Sauter A, Brown MJF, Baer B, SchmidHempel P. 2001. Males of social insects
can prevent queens from multiple mating. Proc. R. Soc. London Sci. Ser. B
268:1449–54
Schlüns H, Schlüns EA, van Praagh J,
Moritz RFA. 2003. Sperm numbers in
drone honeybees (Apis mellifera) depend on body size. Apidologie 34(6):577–
84
Shellman-Reeve JS. 1997. The spectrum
of eusociality in termites. See Ref. 27b,
pp. 52–93
Simmons LW. 2001. Sperm Competition
and Its Evolutionary Consequences in the
Insects. Princeton, NJ: Princeton Univ.
Press. 434 pp.
Sivinski JM, Petersson E. 1997. Mate
choice and species isolation in swarming
insects. See Ref. 27a, pp. 294–309
Starr CK. 1979. Origin and evolution of
insect sociality: a review of modern theory. In Social Insects, Vol. 1, ed. HR Hermann, pp. 35–79. New York: Academic
Starr CK. 1984. Sperm competition, kinship and sociality in the aculeate Hymenoptera. In Sperm Competition and
the Evolution of Animal Mating Systems,
ed. RL Smith, pp. 427–64. London: Academic
28 Oct 2004 20:17
AR
AR234-EN50-17.tex
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
SOCIAL INSECT MALES
116. Stein KJ, Fell RD, Holtzman GI. 1996.
Sperm use dynamics of the baldfaced hornet (Hymenoptera: Vespidae). Environ.
Entomol. 25:1365–70
117. Strassmann J. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc. 48:1–13
118. Stuart AM. 1969. Social behavior and
communication. See Ref. 77a, 1:193–
232
119. Stuart RJ, Francoeur A, Loiselle R. 1987.
Lethal fighting among dimorphic males
of the ant, Cardiocondyla wroughtonii.
Naturwissenschaften 74:548–49
120. Stubblefield JW, Seger J. 1994. Sexual
dimorphism in the Hymenoptera. In The
Differences Between the Sexes, ed. RV
Short, E Balaban, pp. 77–103. Cambridge,
UK: Cambridge Univ. Press
121. Sumner S, Hughes WOH, Pedersen JS,
Boomsma JJ. 2004. Ant parasite queens
revert to mating singly. Nature 428:35–
36
122. Sundström L, Boomsma JJ. 2000. Reproductive alliances and posthumous fitness
enhancement in male ants. Proc. R. Soc.
London Sci. Ser. B 267:1439–44
123. Thorne BL. 1985. Termite polygyny: the
ecological dynamics of queen mutualism.
See Ref. 65a, pp. 325–41
124. Thorne BL. 1997. Evolution of eusociality
in termites. Annu. Rev. Ecol. Syst. 28:27–
54
125. Thorne BL, Breisch NL, Haverty MI.
2002. Longevity of kings and queens and
first time of production of fertile progeny
in dampwood termite (Isoptera; Termopsidae; Zootermopsis) colonies with different reproductive strategies. J. Anim. Ecol.
71:1030–41
126. Thornhill R, Alcock J. 1983. The Evolution of Insect Mating Systems. Cambridge,
MA: Harvard Univ. Press. 547 pp.
127. Trivers RL. 1972. Parental investment and
sexual selection. In Sexual Selection and
the Descent of Men 1871–1971, ed. B
Campbell, pp. 136–79. Chicago: Aldine
128. Tschinkel WR. 1987. Relationship be-
129.
130.
131.
132.
133.
134.
135.
136.
137.
138.
139.
P1: GCE
419
tween ovariole number and spermathecal sperm count in ant queens: a new allometry. Ann. Entomol. Soc. Am. 80:208–
11
Tschinkel WR, Porter SD. 1988. Efficiency of sperm use of queens of the
fire ant, Solenopsis invicta (Hymenoptera
Formicidae). Ann. Entomol. Soc. Am.
81:777–81
Turillazzi S, West Eberhard MJ. 1996.
Natural History and Evolution of Paper
Wasps. Oxford: Oxford Univ. Press. 400
pp.
Villesen P, Murakami T, Schultz TR,
Boomsma JJ. 2002. Unraveling the transition between single and multiple mating
in attine ants. Proc. R. Soc. London Sci
Ser. B 269:1541–48
Weesner FM. 1969. The reproductive system. See Ref. 77a, 1:125–60
Wiernasz DC, Sater AK, Abell AJ, Cole
BJ. 2001. Male size, sperm transfer, and
colony fitness in the western harvester
ant, Pogonomyrmex occidentalis. Evolution 55:324–29
Wiernasz DC, Yencharis J, Cole BJ. 1995.
Size and mating success in males of the
western harvester ant Pogonomyrmex occidentalis (Hymenoptera: Formicidae). J.
Insect Behav. 8:523–31
Winter U, Buschinger A. 1983. The reproductive biology of a slavemaker ant,
Epimyrma ravouxi, and a degenerate
slavemaker, E. kraussei (Hymenoptera:
Formicidae). Entomol. Gener. 9:1–15
Wilson EO. 1971. The Insect Societies.
Cambridge, MA. Harvard Univ. Press.
558 pp.
Woyciechowski M. 1990. Mating behaviour in the ant Myrmica rubra (Hymenoptera: Formicidae). Acta Zool. Cracov. 33:565–74
Woyciechowski M, Kabat L, Król E.
1994. The function of the mating sign in
honey bees, Apis mellifera L.: new evidence. Anim. Behav. 47:733–35
Yamauchi K, Furukawa T, Kinomura K,
Takamine H, Tsuji K. 1991. Secondary
28 Oct 2004 20:17
420
AR
AR234-EN50-17.tex
BOOMSMA
BAER
AR234-EN50-17.sgm
LaTeX2e(2002/01/18)
P1: GCE
HEINZE
polygyny by inbred wingless sexuals in
the dolichoderine ant Technomyrmex albipes. Behav. Ecol. Sociobiol. 29:313–
19
140. Yamauchi K, Kimura Y, Corbara B, Kinomura K, Tsuji K. 1996. Dimorphic ergatoid males and their reproductive behavior
in the ponerine ant Hypoponera bondroiti.
Insectes Soc. 43:119–30
141. Yamauchi K, Oguchi S, Nakamura Y, Suetake H, Kawada N, Kinomura K. 2001.
Mating behavior of dimorphic reproductives of the ponerine ant, Hypoponera nubatama. Insectes Soc. 48:83–87