Download Review Kin Selection versus Sexual Selection: Why the Ends Do

Current Biology 17, R673–R683, August 21, 2007 ª2007 Elsevier Ltd All rights reserved
DOI 10.1016/j.cub.2007.06.033
Kin Selection versus Sexual Selection:
Why the Ends Do Not Meet
Review
Jacobus J. Boomsma
I redevelop the hypothesis that lifetime monogamy is
a fundamental condition for the evolution of eusocial
lineages with permanent non-reproductive castes,
and that later elaborations — such as multiply-mated
queens and multi-queen colonies — arose without
the re-mating promiscuity that characterizes nonsocial and cooperative breeding. Sexually selected
traits in eusocial lineages are therefore peculiar,
and their evolution constrained. Indirect (inclusive)
fitness benefits in cooperatively breeding vertebrates appear to be negatively correlated with promiscuity, corroborating that kin selection and sexual
selection tend to generally exclude each other. The
monogamy window required for transitions from solitary and cooperative breeding towards eusociality
implies that the relatedness and benefit-cost variables of Hamilton’s rule do not vary at random, but
occur in distinct and only partly overlapping combinations in cooperative, eusocial, and derived eusocial breeding systems.
Let’s start with the fact that sexual selection is to do
with social relations within species
H. Cronin (1991), The Ant and the Peacock
Sex is an antisocial force in evolution
E.O. Wilson (1975), Sociobiology, The New Synthesis
Introduction
The second half of the 20th century saw major advances
in our understanding of evolutionary conflicts. Hamilton’s [1,2] ‘gene-centered’ view of evolution made
reproductive altruism and reproductive conflict understandable [3,4] and allowed the fundamental intergenerational conflicts between parents and offspring to
be formulated [5]. Likewise the study of sexually selected conflicts was firmly reinstated in Darwin’s original adaptive framework [6–8], while also the Fisherian
runaway null-model of sexual selection was greatly refined [9]. More recently, Haig [10] combined insights
from inclusive fitness and sexual selection theory to formulate the concept of genomic imprinting. Although
exceptional in its mechanisms, the discovery of genomic imprinting underlines the general principle that
gene-level interactions may both be cooperative and
selfish [11]. The notion that there is no form or level of
biological cooperation that is not somehow threatened
by internal corruption is now increasingly penetrating
other fields of biology and medical science [12,13].
An interesting paradox is that selfish-gene approaches have allowed us to make progress in understanding the true general nature of cooperation,
Institute of Biology, University
Copenhagen, Denmark.
Email: [email protected]
of
Copenhagen,
2100
because they forced us to stare the omnipresent potential of conflict in the face. However, the actual perception of which interactions are cooperative and
which are conflict-prone has changed as more data
on paternity and family structure became available.
The original emphasis on cooperation in mate
choice and breeding — two unrelated individuals collaborating to produce and sometimes raise offspring
together — has gradually been replaced by concepts
emphasizing battles between the sexes and antagonistic co-evolutionary arms races [14,15]. The paradigm shifted because life-long monogamy, the crucial
condition for avoiding conflict between mating partners, turned out to be rare in birds and mammals
[16]. However, explicit studies of mating systems of
social insects have shown the opposite, i.e. that multiple paternity of queen offspring is much rarer than
previously assumed [17–19]. The advanced eusocial
insects have thus turned out to be fundamentally monogamous, whereas most of the remaining free-living
animal world is now confirmed to be mostly promiscuous (see Box 1 for a glossary of relevant terms used in
this review, including promiscuity).
As the quotes above illustrate, the conceptual interface between sexual selection and social evolution has
been confusing (but see [20]). While reproductive conflict thinking has been equally crucial for students of
both fields, their research agendas have diverged
(Figure 1). Apparently, very few animal model systems
with spectacular sexually selected traits also display
altruistic helping behaviour. Likewise, pinnacles of eusocial evolution have stimulated little effort to investigate sexually selected traits. Thus, the ‘ant’ and the
‘peacock’ that have determined much of the agenda
in evolutionary ecology during the last 40 years [7] do
in fact rarely meet. My main argument in this review
will be that this is not just a remarkable coincidence
of researchers in adjacent fields being blind for each
others merits, but a logical and fundamental consequence of the way in which the sexes interact [6].
I will start by noting that promiscuity discourages
permanent commitments to reproductive altruism in
the same way as it corrupts cooperation between the
sexes. I will then combine this logic with the currently
known mating system characteristics of the eusocial
ants, bees, wasps and termites to develop the hypothesis that strict lifetime monogamy (Box 1) was the single pervasive condition for the evolution of permanently sterile helper castes. In subsequent sections I
will address some of the implications:
1. The three terms in Hamilton’s rule (br > c; Box 1)
were unlikely to have varied at random when eusociality evolved, and marginal ergonomic (b/c)
benefits of becoming a reproductive helper must
have sufficed to tip the balance away from independent, solitary reproduction when parents
were constrained to be monogamous for life.
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Box 1
Glossary.
Caste: A social phenotype that becomes permanently specialized for reproduction (queen, king), defence (soldier) or labour
(worker), before reaching maturity [55].
Cooperative breeding: A form of social organisation characterised by cooperative brood care, usually between one or both
parental breeders and one to several offspring helpers, but without any of them having fixed caste characteristics.
Eusociality: An advanced state of social organization characterized by generation overlap, cooperative brood care and fixed
castes with division of labour, of which at least one (workers or soldiers) has irreversibly specialized on a subset of the original
behavioural or physiological spectrum so that direct fitness is reduced (i.e. the caste has lost totipotency) [55].
Evolutionary (reproductive) conflict: Any situation in which the reproductive interests of genes in females, males and/or their
offspring are not completely aligned, such that manipulative traits may evolve that preferentially serve the interests of genes
expressed in specific focal individuals.
Hamilton’s rule: The inequality (br > c) specifying the conditions under which the expression of reproductive altruism can be
promoted by natural selection. r is the relatedness of the recipient of help to the donor, b is the increment in reproductive success
of the recipient owing to the help received, and c is the decrease in personal reproductive success of the donor [100].
Haplodiploidy hypothesis: The idea that relatedness of 0.75 between female full-siblings, which occurs in animals with
a haplodiploid sex determination system (e.g. the Hymenoptera), would by itself increase the likelihood for eusocial helper castes
to evolve.
Kin selection: Process by which traits are favoured because of their beneficial effects on the fitness of relatives [88].
Monogamy: Pair-bonding for life between a single male and female, here defined in its strictest possible sense of exclusive mating
between that male and female, for the purpose of their reproduction only. In this context, a stored ejaculate (e.g. as found in
Hymenopteran queens) is equivalent to a live mate.
Promiscuity: All mating systems that are not strictly monogamous. Promiscuity includes the following sub-categories:
Polygamy: Lifetime simultaneous pair-bonding between a single female and multiple males or their stored sperm (polyandry),
or a single male or his sperm and multiple females (polygyny). The latter is unlikely in eusocial insects, because males cannot
defend harems. Here, the term polygyny therefore refers to multiple queens breeding in the same nest or colony, each of them
mated to a different male (or sometimes different multiple males).
Re-mating promiscuity or promiscuity sensu stricto: Change of mates during a focal breeder’s lifetime, such that younger
offspring or later clutches are half siblings rather than full siblings. This includes serial monogamy, i.e. changing monogamous
partner so that clutches of mixed parentage are avoided, because overlapping generations of helpers and breeders will usually
imply that helpers should raise at least some half siblings.
Reproduction in eusocial insects: The production of sexual offspring: virgin queens, which are usually winged and often disperse
during mating flights, and males, which almost always disperse on the wing. The production of workers is normally not considered
to be reproduction, but colony growth.
Sexual selection: Process by which traits are favoured that increase competitive abilities for mating opportunities among males or
efficiency of partner selection by females. The roles are reversed in some species.
2. Secondary elaborations of eusocial mating systems
away from strict lifetime monogamy have evolved
only when re-mating promiscuity could be avoided.
3. The operation of sexual selection in eusocial systems with multiply mating queens is constrained,
so that unusual adaptations are expected, which
allow for testing aspects of sexual selection theory that are normally not accessible in promiscuous mating systems.
4. Monogamy as a necessary condition for the evolution of eusociality is expected to apply in all
non-clonal eusocial arthropod lineages, but explicit mating system studies are needed to verify
the generality of this principle.
5. Confirmation of this hypothesis would establish
that eusociality can evolve from cooperative
breeding only via an intermediate monogamous
breeding system.
6. None of the cooperatively breeding vertebrates
have evolved mating systems without re-mating
promiscuity, with the possible exception of the
ancestors of the two species of mole rats which
are often characterized as being eusocial.
7. Re-mating promiscuity and indirect fitness benefits seem to be negatively correlated across
cooperatively breeding birds, suggesting that
also in vertebrates the more extreme forms of
sexual selection preclude kin selection and vice
versa.
8. Monogamy as a working hypothesis for the evolution of sterile castes may help to put recent discussions on the merits of kin selection for explaining social evolution to rest.
Lifetime Monogamy as the Key Condition
for Becoming Eusocial
Ring chromosomes and inbreeding cycles have been
proposed as key factors for the evolution of eusociality
in the diplo-diploid termites, because of their potential
to increase sibling relatedness beyond 0.5, but both
turned out to be problematic as they were not typical
for the lower termites [21–23]. However, the crucial
point is not whether relatedness becomes elevated,
but rather that breeding systems must ensure that relatedness among siblings does not drop below the value
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BES
BE
140
120
Number of papers
Figure 1. ‘Kin selection’ and ‘sexual selection’ in the literature.
The number of times that the terms ‘kin selection’ and ‘sexual selection’ were found
in the titles or key words of articles published in two representative journals,
Behavioral Ecology and Sociobiology
(BES; light grey) and Behavioural Ecology
(BE; dark grey) in 2004. More than 50% of
the articles contained at least one of these
key words but only ca. 3% contained
both. Relative to the expected frequencies, articles addressing both kin selection
and sexual selection are clearly underrepresented (c2 = 5.54, P = 0.019 for BES and
4.75, P = 0.029 for BE).
100
80
60
40
–
20
c
le
+
0
–
n
Ki
se
+
Sexual selection
of 0.5 that applies to own offspring if reproductive altruism is to evolve de novo in the easiest possible way.
Throughout the termites, the 0.5 relatedness condition is achieved by obligate lifetime monogamy [24].
Even a low probability of some ancestral termite offspring being half-siblings rather than full-siblings
would have required a step-wise, non-gradual b/c advantage for starting evolution towards eusocial worker
castes. In fact, we now know that the sister-group of
the termites, the nest-building cockroach Cryptocercus, is also biparentally monogamous and shares
many of the cellulose-digesting bacterial symbiont lineages that may have contributed to the ergonomic (b/c)
fitness benefits of eusocial organization [22–29].
However, symbiont acquisition by immature individuals does not preclude adult dispersal, which suggests that initial cooperative breeding in the lower
termites could only evolve into eusociality because
monogamy was maintained. This implies that the
multiple origins of soldiers and permanent workers
in termites are easy to conceptualize, because the
r-term in Hamilton’s rule was fixed at 0.5.
It has gradually become clear that lifetime monogamy is also the default breeding system in the ants, eusocial bees and eusocial wasps, which are all haplodiploid, but this fact is less widely appreciated. By
the time inclusive fitness theory [1,2] became influential, the belief had somehow become established that
multiple mating was common enough to discredit the
generality of the conceptual kin-selection framework
(for example, see [26,30]), even though Hamilton
[1,2], Wilson [25] and Andersson [31] had argued that
multiple mating would not be a problem for explaining
the origins of eusociality across the Hymenoptera, if it
could be proven that such mating systems developed
secondarily after workers had irreversibly lost the capacity to mate. Over the decades that followed, the
necessary comparative data did become gradually
available and showed that strict monogamy is highly
likely to have been the basal condition in all three major
clades of eusocial Hymenoptera [17–19]. This implies
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that in ancestral lineages the average relatedness of
helpers to female and male siblings under outbreeding
and 1:1 Fisherian sex allocation was predictably 0.5 —
the average between a relatedness of 0.75 to sisters
and a relatedness of 0.25 to brothers — equivalent to
the relatedness to own offspring [21].
The current empirical evidence for monogamy as an
ancestral trait of eusocial taxa can be summarized as
follows: The vespid wasps [32] and the corbiculate
bees [33] seem both highly likely to have had singlequeen monogamous ancestors. In ants, both multiple
mating [17,19] and multi-queen colonies [34] are very
likely to be derived, so that monogamous ancestry is
a logical inference. Explicit mating system studies in
other relevant taxa are not available, but indirect evidence suggests that basal clade monogamy is likely
to apply also in the single known ‘eusocial’ sphecid
wasp [35], the thrips with soldiers [36], the social ambrosia beetles [37,38], as well as the snapping shrimps
and other social Crustacea [39,40]. The clonal aphids
with a soldier caste are an exception that proves the
rule, as parthenogenesis instead of outbred monogamy doubles the inclusive fitness benefit of helping
and eliminates the variance [41].
In retrospect, it seems surprising that monogamy
has not been pursued more forcefully as a crucial condition for the evolution of eusociality, because it is so
obviously consistent with Hamilton’s inclusive fitness
theory [1,2]. Part of this is likely due to the unfortunate
initial emphasis on the elevated haplodiploid relatedness to full sisters, although the notion that the 0.75 relatedness to sisters is compensated by 0.25 relatedness to brothers was established in formal models
decades ago [42,43]. However, both before and after
the demise of the haplodiploidy hypothesis for the evolution of eusociality [44], references to monogamy
were usually brief or implicit [2,7,21,23,45–48]. The
most transparent acknowledgment of the general significance of monogamy for the evolution of obligate reproductive altruism that I have been able to find is in
the endnotes of the second edition of The Selfish
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Gene, where Dawkins [3] states that self’s monogamous mother is worth as much reproductively as self
or, as Cronin [7] reiterates, as valuable as an identical
twin. The reason is that, under outbreeding and 1:1
sex allocation, all such mothers will predictably produce offspring to whom self is related by 0.5 on average. This principle should, thus, be at the core of any
general argument about the evolution of sterile worker
castes.
The monogamy hypothesis is consistent with all
evolutionary developments towards eusociality having
followed the so-called ‘subsocial’ (parent-offspring)
route, so that the parasocial route (multiple same generation foundresses), which has been quoted as an alternative for decades, would be rendered invalid, consistent with evidence already available a decade ago
[21,23,46,47]. Also today, we know of no single case
in which communal or parasocial breeding of unrelated females has selected for the emergence of
a worker caste that has lost the capacity to mate and
express full reproductive potential [47,49]. This is consistent with reproductive skew models which predict
that subordinates in matrifilial associations will give
up reproduction, whereas this will only partially take
place in sibling associations with the same relatedness
[50,51]. Comparative data confirm this prediction [50].
Moreover, communal and eusocial breeding appear to
be mutually exclusive across the latest phylogeny of
the Halictid bees — a clade in which eusociality is evolutionarily labile [52].
The transition to a eusocial state with helper castes
of permanently reduced fecundity is a discontinuous
point of no return in social evolution [53] that deserves
to be added to seven other examples of irreversible
evolution [54]. Once eusociality has progressed beyond the facultative stage, the helper castes are
always maintained except in some social parasites in
which queens came to depend on workers of a different species, but without ever returning to a morphology
and behavioral syndrome reminiscent of the ancestral
solitary state [25,26]. The strict definition of eusociality
(Box 1) [55] uses this irreversibility of worker castes,
but not soldier castes, as a defining trait for extant eusociality. The hypothesis outlined here suggests that
these same worker castes could only arise via strict
lifetime monogamy.
The monogamy hypothesis implies that the three
variables in Hamilton’s rule are unlikely to vary at random when they assume values that fulfil the conditions
for an evolutionary transition towards eusociality.
When relatedness to siblings is predictably 0.5 because of lifetime monogamy, any marginal gain in the
benefit/cost ratio of rearing siblings suffices to start
an evolutionary process towards eusocial organisation
[2,56]. This is fundamentally different in cooperative
breeders in which strict monogamy is not required,
such that significantly positive b/c ratios are crucial
to maintain temporary helping behaviour. The social
spiders are an illustrative example. Inbreeding appears to have been a precursor of cooperative breeding in many lineages and b/c ratios are likely to be positive [57]. However, none of the social spiders ever
became eusocial, which is consistent with the monogamy hypothesis, as new colonies are founded by more
individuals than a single lifetime committed pair and
re-mating promiscuity is part of normal social life.
The arguments above imply that students of social
evolution would benefit from loosening their focus
on, or aversion to, relatedness per se and try to understand the fundamental characteristics of the mating
and breeding systems that produce specific relatedness values in colonies. As long as there is no evidence
for anything else than lifetime monogamous mating
systems and outbreeding during pair formation in the
basal lineages of extant eusocial clades, it is most parsimonious to consider inbreeding and the various
ergonomic conditions that contribute to the maintenance of established eusocial systems as secondary
developments. A corollary of the monogamy hypothesis is that there is only room for relaxing the lifetime
monogamy condition after a transition towards permanent reproductive altruism has been completed.
Eusocial Insects May Evolve to Be Polygamous
but Not to Change Mates
Breeding systems where queens always mate with
more than a single male (polyandry) have evolved in
several derived clades of ants, but appear to be restricted to very few taxa in the bees, essentially only
the honeybees, and wasps, essentially only some genera of vespine wasps. In the eusocial Hymenoptera,
polyandry merely means that more than one, sometimes many, males commit their lifetime reproductive
success to the sperm storage organ of a single or
sometimes a few queen(s) who will never re-mate
[58]. The result is an inseminated queen ‘matriarch’
maintaining a ‘harem of deceased males’ that survive
as her internalized private sperm bank. This early acquired sperm store is all she will ever have. Even
army ant queens, the last standing case where remating has been deemed likely, were recently shown
not to be able to re-mate effectively, as was in fact
predicted by inclusive fitness theory [47,59]. Thus, as
far as the eusocial Hymenoptera have secondarily
evolved non-monogamous mating systems, they
have become polygamous (i.e. polyandrous) without
being promiscuous in the strict sense of changing
mates.
As far as we know, virtually all termites have maintained their ancestral, strictly monogamous mating
system, the only functional difference to monogamous
ants being that the termite male (king) lives as long as
the queen and has exclusive lifetime mating rights because he shares a royal nest chamber with his mate
[58]. One study suggests that some termites may
have secondarily become facultatively polygamous
with multiple unrelated queens coexisting in the
same nest, possibly with the same number of males.
However, this occurs only as a rare alternative to default monogamy [60] and re-mating promiscuity has
not been confirmed with genetic markers. A more
common elaboration is the retention of reproductive
neotenic offspring in the nest and having them established in additional royal nest chambers where they
mate incestuously with a sibling [22,23,28]. Also this
elaboration does not violate the principle that termite
colonies are genetically closed systems that may go
through a few inbreeding cycles after having been
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1.0
Full-sibling relatedness (A)
Average relatedness to siblings
Full- and half-sibling relatedness among a single queen’s offspring (B)
Sibling and more distant relatedness among multiple queen’s offspring (C)
Full- and half-sibling relatedness when one parent breeds with a new partner
Death
0.5
Death
Maximal tenure or
life-span of helpers
Death
A
B
C
0
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Figure 2. Drastic sibling relatedness effects of re-mating promiscuity.
Diagram illustrating the effect of re-mating promiscuity in cooperative breeders on relatedness of helpers towards siblings under the
assumption that a single dead parent (‘Death’) is replaced by an unrelated floater (thick black line). Such changeovers imply that helpers
will experience sudden transitions from raising full-siblings (r = 0.5) towards raising half-siblings (r = 0.25). This may make them disperse
to breed on their own if their b/c ratio of helping is <2, so that the new breeding pair will have to produce their own offspring before they
can recruit new helpers. For comparison, also the relatedness among offspring of lifetime monogamous parents has been drawn
(dashed line A at 0.5), as well as an example of the expected average relatedness among female offspring of a eusocial multiply mated
queen (in large colonies, variation is negligible when stored sperm of different males is mixed; dashed line B) and among female
offspring of a eusocial group of co-breeding queens (fluctuations are expected to be larger as reproductive skew may vary over
time, not least because new offspring queens may be adopted as breeders; dotted line C).
founded by an outbred monogamous pair, a habit they
appear to have in common with some ambrosia beetles [37,61] and the naked mole rat. However, no new
genes ever seem to enter an established termite society, which implies that the termites may have remained
non-promiscuous throughout.
In ants and some eusocial wasps and bees, multiple
queens are often found breeding in the same nest (polygyny [62]). This normally does not come about through
inbreeding with full siblings, although lesser degrees of
inbreeding are common in ants [48]. It is important to
note that also these derived breeding systems do not
involve re-mating promiscuity. Multiple reproducing
queens will reduce the relatedness between nestmates,
but — as in single-queen societies — each queen carries the lifetime committed sperm of a single male or,
more rarely, multiple males in her sperm storage organ.
Re-mating later in life is not known to take place, so that
cooperatively breeding (polygynous) queens can neither select new mates nor exploit opportunities for extra
pair copulations, options that are normally available in
cooperatively breeding vertebrates. Thus, unlike the
termites, new genes do enter established polygynous
colonies of eusocial Hymenoptera, but they do so in
mutually committed pairs of queens and stored ejaculates such that there is no re-mating promiscuity.
Neither polyandry nor polygyny induce the same
high-amplitude shifts in inclusive fitness benefits for
helper castes that characterize cooperative breeding
systems with re-mating promiscuity (Figure 2). Multiple males mated to the same queen may contribute unequal amounts of sperm, but sperm mixing normally
assures that average offspring relatedness in a colony
varies very little over time. Multiple nest queens may
partition reproduction according to similar rules as
do cooperative breeders that have not become eusocial [63]. However, reproductive skew in cooperative
breeders is always a matter of settled or unsettled reproductive conflict among totipotent breeders of similar status and is thus often moderate [50]. However,
changes in vigour of established queens, and the
adoption of new queens, may induce variation in relatedness to siblings over time (Figure 2).
The fact that males of eusocial Hymenoptera are
only posthumously part of colony life may have been
an important factor for the evolution of secondary social elaborations — such as polyandry and polygyny —
because already stored sperm can no longer ‘become
promiscuous’ in the strict sense of re-mating. Such
elaborations have not or hardly happened in the termites, quite possibly because multiple live queens
and kings in a colony would make promiscuous behaviour inevitable and would thus have eliminated the necessary lifetime inclusive fitness benefits for immature
helpers to become permanent workers or soldiers. In
other words, polygamy was a secondary option only
in those clades where it could be implemented without
re-mating promiscuity. Lifetime sperm storage secured this by default in the Hymenoptera, but not in
the termites.
The monogamy hypothesis for the evolution of eusociality, its subsequent further extensions towards multiple queen mating and multi-queen colonies, and
its connections with Hamilton’s rule are illustrated in
Life-time nestmate/offspring relatedness
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Inbreeding
Eusocial inbreeding cycles
1
Eusocial breeding
and restricted
promiscuity
0.5
0.2
Solitary/communal breeding
and normal promiscuity
Cooperative breeding
and normal promiscuity
0.1
0.1
0.2
0.5
1
2
5
10
Hamiltonian benefit-cost ratio (b/c)
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Figure 3. The white area has the solitary and communal
breeders in the lower left quadrant — where neither relatedness nor ergonomic benefits are sufficient to
meet Hamilton’s rule — and the cooperative breeders
in the right hand triangle — where b/c ratios favour
helping behaviour for some of the individual’s lifetime,
but where total lifetime relatedness benefits are insufficient for permanent helper castes to evolve. Mating
system transitions can occur freely throughout the
white area and will usually imply re-mating promiscuity. Transitions towards eusociality — both from solitary/communal breeding and from cooperative breeding — are hypothesized to occur only via the central
(black circle) monogamy window where the sibling/offspring relatedness ratio is equal to 1, so that initial b/c
ratios only need to be marginally >1 to make the transition into the grey eusociality area. This contrasts with
prevailing — often implicit — interpretations of Hamilton’s rule that assume the diagonal towards eusociality can be crossed anywhere, i.e. with many different
combinations of relatedness and b/c ratios. After eusociality has been irreversibly established, relatedness
ratios may remain equal to 1 (e.g. termites) or may decrease to lower values because of polyandry and polygyny, while b/c ratios will tend to increase relative
to values that applied to the ancestors that made the
transition. Cyclic inbreeding as a secondary elaboration in termites (and naked mole rats) has been indicated by an arrow with positive slope. Inbreeding as
an ancestral trait (the white area towards the upper
left) is not known to have given rise to eusocial developments independent of monogamy, but was almost
certainly the precursor of cooperative breeding in several clades of spiders where it was not coupled to monogamy [57].
Constrained and Unusual Forms of Sexual
Selection in Eusocial Insects
Obligate multiple mating of queens must have evolved
via facultative multiple mating — some queens mate
once, others multiple times — but the extant genera
Figure 3. The monogamy hypothesis for
the evolution of eusociality.
The axes represent the crucial variables in
Hamilton’s rule over the lifetime of an individual: the ratio of relatedness (r) towards
nestmate siblings versus outbred offspring (y) and the ratio of benefits versus
costs of helping (x). Both axes are logarithmic such that ratios become linearised.
The grey area towards the upper right represents all x,y combinations where Hamilton’s condition for reproductive altruism
(br > c) is fulfilled across the lifetime of
the individual such that permanent helper
castes are expected to evolve. The highest
value of y is fixed at a value of 2, because
inbreeding cannot increase nestmate (sibling) relatedness beyond 1, i.e. twice the
relatedness to outbred offspring. Arrows
indicate that all transitions towards eusociality are hypothesized to pass via a narrow lifetime monogamy window (the black
circle in the centre) and that it is not possible to cross the diagonal elsewhere.
of eusocial Hymenoptera with multiple mating belong
to either the facultative or the obligate category
[17,19]. All these multiple mating systems had monogamous ancestors with only the most basal form of sexual selection, i.e. assortative mating based on overall
vigour [26,64,65]. To the extent that more elaborate
sexually selected traits did evolve in clades with multiply mated queens, we may thus expect them to be independently novel and possibly convergent. They are
also likely to differ from those in non-social breeding
systems, because of the unusual lack of re-mating
promiscuity.
Male mating efforts in ants, eusocial bees and eusocial wasps may either result in exclusive paternity
when a mating plug prevents additional matings and
makes females lose interest [66–68] or in shared paternity when females mate with a number of males in
quick succession [69–71]. Males may actively compete
for access to females in bees and wasps [72], but this
is uncommon or absent in ants and honeybees [58,71].
Females of many social bees and wasps are able to reject unwanted mates [72], but this seems more exceptional in ants in which queens are less agile flyers and
have often been selected to minimize the duration of
their mating flight to reduce exposure to predators
and diseases [58]. Thus, as far as pre-mating sexually
selected behaviours were present, they seem to have
been largely lost in the advanced eusocial taxa with
perennial societies.
Lethal male fighting has evolved in connection with
incestuous mating within the nest, but it occurs in
just a few genera of ants and bears many similarities
to male fighting in fig wasps [73]. Mating in the nest
provides an unusual selection arena in which males
have access to multiple females without having to
make much of an effort, whereas rivals tend to be relatively few and cannot escape. The evolution of male
fighting, therefore, illustrates that relatedness between
contenders is not decisive for preventing aggression
when competition is local [74]. Breeding systems of
this kind have been extensively studied in the ant
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genus Cardiocondyla [58,75]. Some lineages of these
ants have males with sable-shaped mandibles who
kill rivals that eclose after them [76]. These wingless
fighting males often coexist with winged brothers
with normal (harmless) mandibles that disperse to
mate in neighbouring colonies [77]. Most remarkable,
the Cardiocondyla fighting males are the only ant
males known that mature sperm throughout their adult
lives, as ant males normally hatch with a fixed amount
of sperm that is determined in the pupal stage [76].
However, just like any other ant, the Cardiocondyla
mating system does not appear to have female re-mating promiscuity. Whether singly or multiply inseminated [78], and whether they leave the colony or stay,
also queens of Cardiocondyla are receptive for only
a very short time and do not re-mate later in life.
Also post-mating sexual selection in eusocial Hymenoptera with multiple paternity is peculiar. At first
sight, the possibilities for sperm competition appear
to be substantial because ejaculates normally overlap
almost completely in time and space. However, of the
seven mechanisms of sperm precedence listed by
Simmons [79] only three — sperm loading, sperm
stratification and sperm selection — may apply in eusocial Hymenoptera. Three of the four remaining
mechanisms — sperm flushing, sperm displacement
and sperm removal — are unknown and the fourth —
sperm incapacitation — is unlikely.
Sperm loading, i.e. males transferring different
amounts of sperm when mating with the same female
to bias what would otherwise be a fair sperm storage
raffle, is probably common in eusocial Hymenoptera.
However, after the brief mating window has passed,
transferred sperm is never threatened by rival sperm.
Even during this window, it merely risks being diluted,
not being displaced. Every time that multiple mating
evolved from monogamous ancestors, some selection
pressure may have arisen for ejaculates to reduce the
share in paternity of non-related sperm. However, the
mechanisms available for the evolution of such traits
are constrained [58,68]. Manipulative traits that would
negatively affect queen fitness before the onset of reproduction would likely be selected against, as newly
founded colonies produce only sterile workers during
the first months in most bees and wasps and for several years in most ants. It is, therefore, difficult to conceive of direct mechanisms by which stored ejaculates
could obtain significant selfish benefits in the reproductive phase, without suffering large collective costs
in the ergonomic phase of colony development. In
growth phases, it would in fact increase male fitness
to have eggs fertilized by rival sperm, so that less of
this is left in storage when reproduction starts. Even after reaching the size to reproduce, perennial ant colonies will continue to produce at least an order of magnitude more sterile workers than virgin queens, so that
incapacitation of stored rival sperm may still backfire
when it affects colony productivity. This implies that
the evolution of sperm traits that damage queen fitness is less likely than in non-eusocial insects and
that any such traits that did evolve are expected to
have relatively mild effects [58].
Targets for sexual selection that remain available in
polyandrous eusocial Hymenoptera are traits that
affect sperm mobility and viability. These topics have
recently been reviewed elsewhere [58,80]. They are
all affected by the unusual circumstances that longlived queens — in particular those of ants that may
live for decades — are assumed to potentially use all
their stored sperm before dying, such that sperm supply ultimately becomes the limiting factor for lifetime
reproductive success. Even if this assumption would
turn out not to be strictly true, it would still be a fair approximation as sperm becomes a limiting resource
when re-mating later in life is not an option. This implies that we should expect specific adaptations to
keep sperm maximally viable during storage and to
minimize sperm waste during fertilization [81], both
of which are not expected in mating systems with remating promiscuity. The relevant questions related to
sexual selection, sperm competition and cryptic female choice in polyandrous eusocial Hymenoptera
therefore often differ from those addressed in noneusocial mating systems, but their unusual character
may allow interesting experimental tests of the generality of sexual selection theory that cannot be performed in more promiscuous model systems [58,80].
Sexual Selection and Kin Selection
in Cooperatively Breeding Vertebrates
The comparative study of cooperatively breeding vertebrates has progressed significantly during recent
decades [82–85]. An important synthesis was recently
provided by Griffin and West [86] who analyzed comparative data from 11–15 species of birds as well as
two to three species of mammals and showed that
there is a strong positive correlation between the degree to which helping is preferentially directed towards
kin and the extent to which helping results in increased
production or survival of offspring of dominant
breeders. The necessity for helpers to discriminate according to degree of kin is expected to be directly related to the turnover of breeders after death or usurpation and the extent of promiscuity of the breeding
female (Figure 2). A closer comparative look at the mating systems of cooperatively breeding birds and mammals is therefore worthwhile, in order to evaluate how
kin selection and sexual selection may interact in systems that are not constrained to be monogamous and
that have helpers that can disperse to reproduce
independently.
A recent study by Griffith et al. [87] reviewed the
available data on extra pair paternity across 129 species of birds and categorised them in five mutually exclusive breeding systems. A simple analysis of the
data shows that 61% (11/18) of the cooperatively
breeding species show some degree of extra-pair
paternity, whereas this proportion is 75% (83/111) for
all other, non-cooperative breeding systems. Though
non-significant (c2 = 1.46; P = 0.227), this difference
is in the expected direction of cooperative breeders
having fewer offspring with extra-pair paternity, analogous with the evolution of permanent helper castes relying on strict monogamy. A more specific evaluation
of the ranked proportions of offspring with extra-pair
paternity in cooperative versus non-cooperative
breeders gave a marginally significant result (t =
1.5463; one tailed P = 0.0624; Wilcoxon two-sample
Current Biology Vol 17 No 16
R680
Cooperative breeders
Other breeding systems
0.30
0.25
0.20
0.15
0.10
0.05
0
35
51
43
–EPP
+EPP(<10%)
+EPP(>10%)
Current Biology
Figure 4. Cooperative breeding and promiscuity in birds.
The frequency of no extra-pair paternity (-EPP), some extra-pair
paternity (0% <+EPP<10%), and ample extra-pair paternity
(+EPP>10%) among cooperative breeding birds, relative to
birds with other breeding systems. Data are from Griffith et al.
[87]. The separation of the +EPP data at 10% is arbitrary, but
has the merit of achieving roughly equal sample sizes among
the three categories (written in the bars). The horizontal line is
the average ratio of cooperative breeders versus other breeding
systems in the 129 species for which data on % offspring with
EPP were available and deemed reliable enough to be used
for comparative analysis by Griffith et al. [87].
test; Figure 4). As it appears, the category of below
10% extra-pair paternity is equally common in cooperative and non-cooperative breeders, but genetically
documented monogamy is overrepresented and
more excessive promiscuity underrepresented among
the cooperative breeders. This analysis is obviously
very crude as phylogenetic effects have not been
taken into account, but some of the deviations from
the overall trend suggest that more detailed and better
controlled future studies might actually produce more
significant effects.
One of the four cooperative breeders in the highest
extra-pair paternity class, the white-browed scrubwren, is just above the 10% cut-off point with 12.4% offspring with extra-pair paternity, but the other three
species have much higher percentages and were
part of the comparative data set analysed by Griffin
and West [86]. One of these, the superb fairy wren
(with 71.6% offspring with extra-pair paternity) is in
the very bottom left corner of their regression plot
(see Figure 2 in [86]; see also Figure 5 in [88]), indicating that it neither obtains kin-selected inclusive fitness
benefits from helping, nor directs its helping efforts
preferentially towards kin. When the Wilcoxon rank
score test is repeated without this outlier, the result
is actually significant (t = 1.987; one tailed P = 0.025).
The other two highly promiscuous species (western
bluebird and Seychelles warbler) are further towards
the right in Griffin and West’s plot [86], indicating that
they obtain, respectively, some and substantial inclusive fitness benefits from helping. Interestingly, these
two species also have the two highest positive residuals for kin discrimination. This implies that they are
considerably better in directing their help towards
close kin than predicted from the overall regression,
which seems an appropriate way to partially eliminate
the negative inclusive fitness consequences of parental promiscuity.
The cooperatively breeding mammal data included in
Griffin and West’s analysis [86] are too few to evaluate
systematically, but it is interesting to note that the two
mongoose species (dwarf mongoose and meerkat)
show moderate inclusive fitness benefits of helping
and intermediate tendencies to preferentially direct
helping towards close kin. Some promiscuity has been
reported for both species [85,89,90], which contrasts
with the naked and Damaraland molerats, where most
individuals are lifetime helpers raising only very close
kin. The negative correlation between sexual selection
and kin selection that made monogamy a requirement
for the evolution of sterile castes in insects, thus, seems
to occur also in cooperative breeding birds and mammals where options for re-mating promiscuity are present. This suggests that kin selection and sexual selection also work in opposite directions in cooperatively
breeding vertebrates, but that becoming strictly monogamous is a much more difficult transition to make
than in insects. This is consistent with only two species
of mole rats having come close to being eusocial, although their helper castes are not irreversible as, for example, in ants, honeybees or higher termites.
As it turns out, the two species of mole rats are
interesting cases to evaluate the general validity of
the monogamy criterion for eusociality (Table 1). Their
colonies have a single breeding female and one to
three dominant males that sire offspring [91]. As far
as it is strictly monogamous, this breeding system is
comparable with termites where a single live king is
lifetime committed to a single queen and where inbreeding cycles may occur after colony establishment
by an outbreeding pair to prolong colony life span.
However, naked mole rat colonies with multiple male
breeders seem functionally more comparable to
army ants — having multiple males lifetime committed
as stored sperm [59] — where colonies multiply by
fission and by sending out drones to mate with unrelated queens [92].
Following the logic of the monogamy hypothesis,
a key criterion for classifying the naked and Damaraland mole rats as eusocial would be that dispersing
males — a special morph predicted by Dawkins [3]
and found in the naked mole rat by Braude [93] —
should not breed with an already established dominant
female but only found new colonies with unrelated females that have not bred before. If this were the case
the two mole rat species would fulfil the same non-remating promiscuity criterion that characterizes eusocial insects. It would make their breeding systems fully
analogous to those of honeybees, stingless bees, and
army ants, where colonies that lose their queen may
raise a virgin replacement queen that will mate with unrelated males from other colonies, or to those of termites where a replacement or additional queen mates
incestuously with a brother. It is interesting to note
that, while the naked mole rat has secondarily evolved
inbreeding cycles reminiscent of termites, the Damaraland mole rat has retained the ancestral state of avoiding inbreeding and having colony fission after the
Special Issue
R681
death of a reproductive, reminiscent of army ants [92].
Naked mole rats have much larger colonies than Damaraland mole rats, which may imply that selection for
accepting a permanent helper role in order to maintain
already established colonies has been more pronounced [91]. Similarly, increasing colony size has
been an important factor during the elaboration of eusocial organization in insect societies [94].
Conclusions
The relative impact of sexual selection among females
and males is determined by their parental investments.
In this review, I have extended this fundamental insight
by Trivers [6] by arguing that lifetime bi-parental commitment to a single family characterizes all eusocial
breeding systems with permanent castes such that
sexual selection is greatly constrained. My central argument has been that re-mating promiscuity, in spite
of all the direct fitness benefits that it may bring to parents, is a form of social cheating from the perspective
of offspring when they care for younger siblings without being able to discriminate between full and half
siblings. Permanent helper castes that rely mostly or
exclusively on indirect (inclusive) fitness benefits will,
therefore, not evolve unless lifetime monogamy secures these benefits. Cooperative breeders do not
have this ancestral monogamy constraint, but the extent to which helpers in birds and mammals obtain inclusive fitness benefits appears to be similarly affected
by parental promiscuity.
Although supported by a fair amount of evidence,
monogamy as a general prerequisite for the evolution
of permanent eusocial castes is a hypothesis that
awaits further testing. Its generality would be refuted
if cases came to light where non-monogamous clades
have produced species with permanently sterile
castes. This issue, and other predictions derived
from the monogamy hypothesis (Table 1) should be
further tested both in the eusocial Hymenoptera and
termites, and in the presumed eusocial ambrosia beetles, gall-forming thrips with soldiers, snapping
shrimps and mole rats. Focused comparative studies
in cooperative breeders and even human societies
could further shed important light on the generality of
the negative correlation between inclusive fitness benefits and re-mating promiscuity.
The monogamy hypothesis implies that eusocial and
cooperative breeding are distinct social systems because the three variables of Hamilton’s rule [1,2] tend
to combine into different strategy sets. This is easiest
to illustrate when using life-time relatedness and benefit-cost ratios, as in Figure 3. This also makes it
straightforward to use Wilsonian group selection terminology to describe the same phenomena [95–97].
All cases of strong altruism where worker and soldier
castes rely on indirect fitness benefits are concentrated in the grey area of Figure 3. In contrast, cases
of weak altruism that are driven by direct benefits
may occur throughout the diagram, i.e., both in the
white area in the Figure referring to independent or cooperative breeders and in the grey area when multiple
eusocial queens breed in the same colony. Parents
making life-time commitments to their partner(s)
when founding colonies are, therefore, also a condition
Table 1. Testable predictions that follow from the Monogamy
Hypothesis.
1. Clades with eusocial species are characterized by strict
lifetime monogamy as ancestral state.
2. Clades where dominant breeders have retained the
option to change sexual partner(s) do not have lifetime
committed worker/soldier morphs (castes) of irreversibly
reduced fertility.
3. Established queens of eusocial Hymenoptera do not
naturally re-mate later in life in ways that allow them to
store significant amounts of new sperm from unrelated
males so that their tenure as breeder is prolonged.
4. Polygamy of, or promiscuity among, unrelated
reproductives in termites is rare or absent, or merely
happens in accidentally merged senescent colonies that
have no reproductive future.
5. Cooperative breeders in which helpers obtain larger
indirect fitness benefits should be less promiscuous.
6. Manipulative traits of ejaculates that harm the
reproductive fitness of multiply mating eusocial queens
are uncommon and have relatively mild effects.
for strong reproductive altruism [95]. This underlines
that recent challenges to kin selection as the crucial
mechanism for the evolution of eusociality (for example, [53]) are unsustainable not only because of conceptual problems [49,96,97], but also because they
would require the monogamy hypothesis to be falsified
for every extant eusocial clade.
The hypothesized high (0.5) relatedness and low
(just >1) b/c ratio conditions for the early evolution of
eusociality contrast with the low relatedness and
high b/c ratios (relative to ancestors that made the
transition towards eusociality) that often characterize
derived eusocial systems with multiple mating or multiple queens. This underlines the need to distinguish
between scenarios for the early evolution and later
elaboration of social behaviour. Additional variables
such as coercion and punishment are now known to
be important as secondary developments both in
cooperatively breeding and eusocial clades [98,99].
However, although these mechanisms help to stabilize
societies, their establishment rarely implied that
relatedness became unimportant.
Acknowledgements
I thank Boris Baer, Trine Bilde, Tim Clutton-Brock, Sylvia
Cremer, Bernie Crespi, Patrizia D’Ettorre, Alan Grafen, David
Hughes, Laurent Keller, David Nash, Gösta Nachman, Jes
Pedersen, Joan Strassmann and Stu West for discussion and
comments, David Nash for editing the figures and the Danish
National Research Foundation for support.
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