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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. Current Biology Vol 17 No 16 R674 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 Special Issue R675 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 n tio Current Biology 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 Current Biology Vol 17 No 16 R676 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 Special Issue R677 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 Current Biology 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 Current Biology Vol 17 No 16 R678 2 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) Current Biology 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 Special Issue R679 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]. 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