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• W1977528892 abstract "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 non-social 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. 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 non-social 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 speciesH. Cronin (1991), The Ant and the PeacockSex is an antisocial force in evolutionE.O. Wilson (1975), Sociobiology, The New Synthesis The second half of the 20th century saw major advances in our understanding of evolutionary conflicts. Hamilton's [1Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Scopus (8957) Google Scholar, 2Hamilton W.D. Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 1972; 3: 193-232Crossref Google Scholar] ‘gene-centered’ view of evolution made reproductive altruism and reproductive conflict understandable [3Dawkins R. The Selfish Gene.Second Edition. Oxford University Press, Oxford, UK1976Google Scholar, 4Dawkins R. The Extended Phenotype: The Gene as the Unit of Selection. Oxford University Press, Oxford, UK1982Google Scholar] and allowed the fundamental intergenerational conflicts between parents and offspring to be formulated [5Trivers R.L. Parent-offspring conflict.Amer. Zool. 1974; 14: 249-264Google Scholar]. Likewise the study of sexually selected conflicts was firmly reinstated in Darwin's original adaptive framework [6Trivers R.L. Parental investment and sexual selection.in: Campbell B. Sexual Selection and the Descent of Man, 1871-1971. Aldine-Atherton, Chicago, USA1972: 136-172Google Scholar, 7Cronin H. The Ant and the Peacock. Cambridge University Press, Cambridge, UK1991Google Scholar, 8Andersson M. Sexual Selection. Princeton University Press, Princeton, New Jersey1994Crossref Google Scholar], while also the Fisherian runaway null-model of sexual selection was greatly refined [9Lande R. Models of speciation by sexual selection on polygenic traits.Proc. Natl. Acad. Sci. USA. 1981; 78: 3721-3725Crossref PubMed Scopus (1546) Google Scholar]. More recently, Haig [10Haig D. The social gene.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Fourth Edition. Blackwell Scientific Publications, Oxford, UK1997: 284-304Google Scholar] 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 [11Burt A. Trivers R. Genes in Conflict: The Biology of Selfish Genetic Elements. Harvard University Press, Cambridge, Massachusetts2006Crossref Google Scholar]. 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 [12Stearns S.C. Evolution in Health and Disease. Oxford University Press, Oxford, UK1999Google Scholar, 13Denison R.F. Kiers E.T. West S.A. Darwinian agriculture: When can humans find solutions beyond the reach of natural selection?.Q. Rev. Biol. 2003; 78: 145-168Crossref PubMed Scopus (128) Google Scholar]. An interesting paradox is that selfish-gene approaches have allowed us to make progress in understanding the true general nature of cooperation, 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 [14Chapman T. Arnqvist G. Bangham J. Rowe L. Sexual conflict.Trends Ecol. Evol. 2003; 18: 41-47Abstract Full Text Full Text PDF Scopus (820) Google Scholar, 15Bernasconi G. Ashman T.-L. Birkhead T.R. Bishop J.D.D. Grossniklaus U. Kubli E. Marshall D.L. Schmid B. Skogsmyr I. Snook R.R. et al.Evolutionary ecology of the prezygoric stage.Science. 2004; 303: 971-975Crossref PubMed Scopus (135) Google Scholar]. 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 [16Barash D.P. Lipton J.E. The Myth of Monogamy: Fidelity and Infidelity in Animals and People. W.H. Freeman, Oxford, UK2001Google Scholar]. 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 [17Boomsma J.J. Ratnieks F.L.W. Paternity in eusocial Hymenoptera.Philos. Trans. R. Soc. London Ser. B. 1996; 351: 947-975Crossref Scopus (392) Google Scholar, 18Strassmann J. The rarity of multiple mating by females in the social Hymenoptera.Insectes Soc. 2001; 48: 1-13Crossref Google Scholar, 19Boomsma J.J. Kronauer D.J.C. Pedersen J.S. The evolution of social insect mating systems.in: Gadau J. Fewell J. Organization of Insect Societies – Integrated Research Projects. Harvard University Press, Cambridge, Massachusetts2008Google Scholar]. 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).Box 1Glossary.Caste: A social phenotype that becomes permanently specialized for reproduction (queen, king), defence (soldier) or labour (worker), before reaching maturity [55Crespi B.J. Yanega D. The definition of eusociality.Behav. Ecol. 1995; 6: 109-115Crossref Scopus (223) Google Scholar].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) [55Crespi B.J. Yanega D. The definition of eusociality.Behav. Ecol. 1995; 6: 109-115Crossref Scopus (223) Google Scholar].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 [100Grafen A. Natural selection, kin selection and group selection.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 62-84Google Scholar].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 [88West S.A. Griffin A.S. Gardner A. Evolutionary explanations for cooperation.Curr. Biol. 2007; 17: R661-R672Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar].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. Caste: A social phenotype that becomes permanently specialized for reproduction (queen, king), defence (soldier) or labour (worker), before reaching maturity [55Crespi B.J. Yanega D. The definition of eusociality.Behav. Ecol. 1995; 6: 109-115Crossref Scopus (223) Google Scholar].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) [55Crespi B.J. Yanega D. The definition of eusociality.Behav. Ecol. 1995; 6: 109-115Crossref Scopus (223) Google Scholar].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 [100Grafen A. Natural selection, kin selection and group selection.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 62-84Google Scholar].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 [88West S.A. Griffin A.S. Gardner A. Evolutionary explanations for cooperation.Curr. Biol. 2007; 17: R661-R672Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar].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. As the quotes above illustrate, the conceptual interface between sexual selection and social evolution has been confusing (but see [20Queller D.C. Male-female conflict and parent-offspring conflict.Am. Nat. 1994; 144: S84-S99Crossref Scopus (55) Google Scholar]). 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 [7Cronin H. The Ant and the Peacock. Cambridge University Press, Cambridge, UK1991Google Scholar] 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 [6Trivers R.L. Parental investment and sexual selection.in: Campbell B. Sexual Selection and the Descent of Man, 1871-1971. Aldine-Atherton, Chicago, USA1972: 136-172Google Scholar]. 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.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. 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 [21Bourke A.F.G. Sociality and kin selection in insects.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Fourth Edition. Blackwell Scientific Publications, Oxford, UK1997: 203-227Google Scholar, 22Shellman-Reeve J.S. The spectrum of eusociality in termites.in: Choe J.C. Crespi B.J. Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge, UK1997: 52-93Google Scholar, 23Thorne B.L. Evolution of eusociality in termites.Annu. Rev. Ecol. Syst. 1997; 28: 27-54Crossref Scopus (203) Google Scholar]. 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 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 [24Nalepa C.A. Jones S.C. Evolution of monogamy in termites.Biol. Rev. 1991; 66: 83-97Crossref Google Scholar]. 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 [22Shellman-Reeve J.S. The spectrum of eusociality in termites.in: Choe J.C. Crespi B.J. Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge, UK1997: 52-93Google Scholar, 23Thorne B.L. Evolution of eusociality in termites.Annu. Rev. Ecol. Syst. 1997; 28: 27-54Crossref Scopus (203) Google Scholar, 24Nalepa C.A. Jones S.C. Evolution of monogamy in termites.Biol. Rev. 1991; 66: 83-97Crossref Google Scholar, 25Wilson E.O. The Insect Societies. Belknap Press of Harvard University Press, Cambridge, Massachusetts1971Google Scholar, 26Wilson E.O. Sociobiology, the New Synthesis. Belknap Press of Harvard University Press, Cambridge, Massachusetts1975Google Scholar, 27Nalepa C.A. Bell W.J. Postovulation parental investment and parental care in cockroaches.in: Choe J.C. Crespi B.J. Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge, UK1997: 26-51Google Scholar, 28Roisin Y. Philopatric reproduction, a prime mover in the evolution of termite sociality?.Insectes Soc. 1999; 46: 297-305Crossref Scopus (47) Google Scholar, 29Inward D. Beccaloni G. Eggleton P. Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches.Biol. Lett. 2007; (published on line)https://doi.org/10.1098/rsbl.2007.0102Crossref PubMed Scopus (332) Google Scholar]. 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 haplo-diploid, but this fact is less widely appreciated. By the time inclusive fitness theory [1Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Scopus (8957) Google Scholar, 2Hamilton W.D. Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 1972; 3: 193-232Crossref Google Scholar] 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 [26Wilson E.O. Sociobiology, the New Synthesis. Belknap Press of Harvard University Press, Cambridge, Massachusetts1975Google Scholar, 30Brockmann H.J. The evolution of social behaviour in insects.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 340-361Google Scholar]), even though Hamilton [1Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Scopus (8957) Google Scholar, 2Hamilton W.D. Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 1972; 3: 193-232Crossref Google Scholar], Wilson [25Wilson E.O. The Insect Societies. Belknap Press of Harvard University Press, Cambridge, Massachusetts1971Google Scholar] and Andersson [31Andersson M. The evolution of eusociality.Ann. Rev. Ecol. Syst. 1984; 15: 165-189Crossref Scopus (175) Google Scholar] 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 [17Boomsma J.J. Ratnieks F.L.W. Paternity in eusocial Hymenoptera.Philos. Trans. R. Soc. London Ser. B. 1996; 351: 947-975Crossref Scopus (392) Google Scholar, 18Strassmann J. The rarity of multiple mating by females in the social Hymenoptera.Insectes Soc. 2001; 48: 1-13Crossref Google Scholar, 19Boomsma J.J. Kronauer D.J.C. Pedersen J.S. The evolution of social insect mating systems.in: Gadau J. Fewell J. Organization of Insect Societies – Integrated Research Projects. Harvard University Press, Cambridge, Massachusetts2008Google Scholar]. This implies 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 [21Bourke A.F.G. Sociality and kin selection in insects.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Fourth Edition. Blackwell Scientific Publications, Oxford, UK1997: 203-227Google Scholar]. The current empirical evidence for monogamy as an ancestral trait of eusocial taxa can be summarized as follows: The vespid wasps [32Foster K.R. Ratnieks F.L.W. Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions.Behav. Ecol. 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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 [35Matthews R.W. Evolution of social behavior in sphecid wasps.in: Ross K.G. Matthews R.W. The Social Biology of Wasps. Cornell University Press, Ithaca, New York1991Google Scholar], the thrips with soldiers [36Crespi B.J. Mound L.A. Ecology and evolution of social behavior among Australian gall thrips and their allies.in: Choe J.C. Crespi B.J. Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge, UK1997: 166-180Google Scholar], the social ambrosia beetles [37Kirkendall L.R. Kent D.S. Raffa K.A. Interactions among males, females and offspring in bark and ambrosia beetles: the significance of living in tunnels for the evolution of social behavior.in: Choe J.C. Crespi B.J. Social Behavior in Insects and Arachnids. 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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 [41Stern D.L. Foster W.A. The evolution of sociality in aphids: a clone" @default.
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• W1977528892 date "2007-08-01" @default.
• W1977528892 modified "2023-10-14" @default.
• W1977528892 title "Kin Selection versus Sexual Selection: Why the Ends Do Not Meet" @default.
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