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The Insectan Apes

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Abstract

I present evidence that humans have evolved convergently to social insects with regard to a large suite of social, ecological, and reproductive phenotypes. Convergences between humans and social insects include: (1) groups with genetically and environmentally defined structures; (2) extensive divisions of labor; (3) specialization of a relatively restricted set of females for reproduction, with enhanced fertility; (4) extensive extramaternal care; (5) within-group food sharing; (6) generalized diets composed of high-nutrient-density food; (7) solicitous juveniles, but high rates of infanticide; (8) ecological dominance; (9) enhanced colonizing abilities; and (10) collective, cooperative decision-making. Most of these convergent phenotypic adaptations stem from reorganization of key life-history trade-offs due to behavioral, physiological, and life-historical specializations. Despite their extensive socioreproductive overlap with social insects, humans differ with regard to the central aspect of eusociality: reproductive division of labor. This difference may be underpinned by the high energetic costs of producing offspring with large brains.

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References

  • Alexander, R. D., Noonan, K. M., & Crespi, B. J. (1991). The evolution of eusociality. In P. W. Sherman, J. U. M. Jarvis, & R. D. Alexander (Eds.), The biology of the naked mole rat (pp. 3–44). Princeton: Princeton University Press.

    Google Scholar 

  • Barrett, R., Kuzawa, C. W., McDade, T., & Armelagos, G. J. (1998). Emerging and re-emerging infectious diseases: the third epidemiologic transition. Annual Review of Anthropology, 27, 247–271.

    Article  Google Scholar 

  • Bell, M. B., Nichols, H. J., Gilchrist, J. S., Cant, M. A., & Hodge, S. J. (2012). The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses. Proceedings of the Royal Society, Series B: Biological Sciences, 279(1728), 619–624.

    Google Scholar 

  • Berletch, J. B., Yang, F., Xu, J., Carrel, L., & Disteche, C. M. (2011). Genes that escape from X inactivation. Human Genetics, 130(2), 237–245.

    Article  Google Scholar 

  • Bignell, D. E., Roisin, Y., & Lo, N. (2011). Biology of termites: A modern synthesis. Dordrecht: Springer.

    Book  Google Scholar 

  • Boomsma, J. J. (2009). Lifetime monogamy and the evolution of eusociality. Philosophical Transactions of the Royal Society, Series B: Biological Sciences, 364(1533), 3191–3207.

    Google Scholar 

  • Boomsma, J. J., & Ratnieks, F. L. W. (1996). Paternity in eusocial Hymenoptera. Philosophical Transactions of the Royal Society, Series B: Biological Sciences, 351(1342), 947–975.

    Google Scholar 

  • Bourke, A. F. G. (1999). Colony size, social complexity and reproductive conflict in social insects. Journal of Evolutionary Biology, 12(2), 245–257.

    Article  Google Scholar 

  • Bowles, S. (2006). Group competition, reproductive leveling, and the evolution of human altruism. Science, 314(5805), 1569–1572.

    Article  Google Scholar 

  • Bowles, S. (2009). Did warfare among ancestral hunter-gatherers affect the evolution of human social behaviors? Science, 324(5932), 1293–1298.

    Article  Google Scholar 

  • Bowles, S. (2012). Warriors, levelers, and the role of conflict in human social evolution. Science, 336(6083), 876–879.

    Article  Google Scholar 

  • Boyd, R., & Richerson, P. J. (1987). The evolution of ethnic markers. Cultural Anthropology, 2, 65–79.

    Article  Google Scholar 

  • Cant, M. A., & Johnstone, R. A. (1999). Costly young and reproductive skew in animal societies. Behavioral Ecology, 10, 178–184.

    Article  Google Scholar 

  • Cant, M. A., & Johnstone, R. A. (2008). Reproductive conflict and the separation of reproductive generations in humans. Proceedings of the National Academy of Sciences of the United States of America, 105(14), 5332–5336.

    Article  Google Scholar 

  • Cant, M. A., Johnstone, R. A., & Russell, A. F. (2009). Reproductive conflict and the evolution of menopause. In R. Hager & C. B. Jones (Eds.), Reproductive skew in vertebrates: Proximate and ultimate causes (pp. 24–50). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Chagnon, N. A. (1988). Life histories, blood revenge, and warfare in a tribal population. Science, 239(4843), 985–992.

    Article  Google Scholar 

  • Clutton-Brock, T. H. (2009). Structure and function in mammalian societies. Philosophical Transactions of the Royal Society, Series B: Biological Sciences, 364(1533), 3229–3242.

    Google Scholar 

  • Clutton-Brock, T. H., Hodge, S. J., Flower, T. P., Spong, G. F., & Young, A. J. (2010). Adaptive suppression of subordinate reproduction in cooperative mammals. American Naturalist, 176(5), 664–673.

    Article  Google Scholar 

  • Cordts, E. B., Christofolini, D. M., Dos Santos, A. A., Bianco, B., & Barbosa, C. P. (2011). Genetic aspects of premature ovarian failure: a literature review. Archives of Gynecology and Obstetrics, 283(3), 635–643.

    Article  Google Scholar 

  • Crespi, B. J. (1992). Cannibalism and trophic eggs in subsocial and eusocial insects. In M. A. Elgar & B. J. Crespi (Eds.), Cannibalism: Ecology and evolution among diverse taxa (pp. 177–213). Oxford: Oxford University Press.

    Google Scholar 

  • Crespi, B. J. (1994). Three conditions for the evolutions of eusociality: are they sufficient? Insectes Sociaux, 41, 395–400.

    Article  Google Scholar 

  • Crespi, B. J. (2008). Turner syndrome and the evolution of human sexual dimorphism. Evolutionary Applications, 1, 449–461.

    Article  Google Scholar 

  • Crespi, B. J. (2009). Social conflict resolution, life history, and the reconstruction of skew. In R. Hager & C. B. Jones (Eds.), Reproductive skew in vertebrates: Proximate and ultimate causes (pp. 480–507). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Crespi, B. J. (2011). The evolutionary biology of child health. Proceedings of the Royal Society, Series B: Biological Sciences, 278(1711), 1441–1449.

  • Crespi, B. J., & Yanega, D. (1995). The definition of eusociality. Behavioral Ecology, 6, 109–115.

    Article  Google Scholar 

  • Crespi, B. J., Morris, D. C., & Mound, L. A. (2004). Evolution of ecological and behavioural diversity: Australian acacia thrips as model organisms. Canberra: Australian Biological Resources Study & CSIRO Entomology.

    Google Scholar 

  • Crespi, B. J., Summers, K., & Dorus, S. (2009). Genomic sister-disorders of neurodevelopment: an evolutionary approach. Evolutionary Applications, 2, 81–100.

    Article  Google Scholar 

  • Cronin, A. L., Molet, M., Doums, C., Monnin, T., & Peeters, C. (2013). Recurrent evolution of dependent colony foundation across eusocial insects. Annual Review of Entomology, 58, 37–55.

    Article  Google Scholar 

  • Cronk, L. (2007). Boy or girl: gender preferences from a Darwinian point of view. Reproductive BioMedicine Online, 15(Supplement 2), 23–32.

    Article  Google Scholar 

  • Crozier, R. H., & Pamilo, P. (1996). Evolution of social insect colonies: Sex allocation and kin-selection. Oxford: Oxford University Press.

    Google Scholar 

  • Curtis, V. A. (2007). Dirt, disgust and disease: a natural history of hygiene. Journal of Epidemiology and Community Health, 61(8), 660–664.

    Article  Google Scholar 

  • Dennen, J.M.G. van der. (2005). Nonhuman intergroup agonistic behavior and ‘warfare’. University of Groningen. Faculty of Law, http://irs.ub.rug.nl/ppn/280031254, urn:nbn:nl:ui:11-dbi/4357a9830ee93.

  • Diamond, J. (2005). Collapse: How societies choose to fail or succeed. New York: Penguin.

    Google Scholar 

  • Dobata, S., Sasaki, T., Mori, H., Hasegawa, E., Shimada, M., & Tsuji, K. (2009). Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus. Proceedings of the Royal Society, Series B: Biological Sciences, 276(1656), 567–574.

    Google Scholar 

  • Ellison, P. T. (2003). On fertile ground: A natural history of human reproduction. Cambridge: Harvard University Press.

    Google Scholar 

  • Fefferman, N. H., Traniello, J. F. A., Rosengaus, R. B., & Calleri, D. V., II. (2007). Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behavioral Ecology and Sociobiology, 61, 565–577.

    Article  Google Scholar 

  • Foster, K. R., & Ratnieks, F. L. W. (2005). A new eusocial vertebrate? Trends in Ecology and Evolution, 20(7), 363–364.

    Article  Google Scholar 

  • Fox, M., Sear, R., Beise, J., Ragsdale, G., Voland, E., & Knapp, L. A. (2010). Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality. Proceedings of the Royal Society, Series B: Biological Sciences, 277(1681), 567–573.

    Google Scholar 

  • Frank, S. A. (2003). Repression of competition and the evolution of cooperation. Evolution, 57, 693–705.

    Google Scholar 

  • Frank, S. A., & Crespi, B. J. (2011). Pathology from evolutionary conflict, with a theory of X chromosome versus autosome conflict over sexually antagonistic traits. Proceedings of the National Academy of Sciences of the United States of America, 108(Supplement 2), 10886–10893.

    Article  Google Scholar 

  • Fromhage, L., & Kokko, H. (2011). Monogamy and haplodiploidy act in synergy to promote the evolution of eusociality. Nature Communications, 2(397), doi:10.1038/ncomms/1410.

  • Gadagkar, R. (1991). Demographic predisposition to the evolution of eusociality: a hierarchy of models. Proceedings of the National Academy of Sciences of the United States of America, 88, 10993–10997.

    Article  Google Scholar 

  • Gardner, A., & West, S. A. (2004). Cooperation and punishment, especially in humans. American Naturalist, 164(6), 753–764.

    Article  Google Scholar 

  • Gardner, A., Alpedrinha, J., & West, S. A. (2012). Haplodiploidy and the evolution of eusociality: split sex ratios. American Naturalist, 179(2), 240–256.

    Article  Google Scholar 

  • Gautrais, J., Theraulaz, G., Deneubourgz, J. L., & Anderson, C. (2002). Emergent polyethism as a consequence of increased colony size in insect societies. Journal of Theoretical Biology, 215, 363–373.

    Article  Google Scholar 

  • Gibson, M. A., & Gurmu, E. (2011). Land inheritance establishes sibling competition for marriage and reproduction in rural Ethiopia. Proceedings of the National Academy of Sciences of the United States of America, 108(6), 2200–2204.

    Article  Google Scholar 

  • Gotwald, W. H., Jr. (1995). Army ants: The biology of social predation. Ithaca: Cornell University Press.

    Google Scholar 

  • Graves, J. A. M., Koina, E., & Sankovic, N. (2006). How the gene content of human sex chromosomes evolved. Current Opinion in Genetics & Development, 16(3), 219–224.

    Article  Google Scholar 

  • Grüter, C., Menezes, C., Imperatriz-Fonseca, V. L., & Ratnieks, F. L. (2012). A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee. Proceedings of the National Academy of Sciences of the United States of America, 109(4), 1182–1186.

    Article  Google Scholar 

  • Gurven, M. (2004). To give and to give not: the behavioral ecology of human food transfers. Behavioral and Brain Sciences, 27(4), 543–583.

    Google Scholar 

  • Gurven, M., & Hill, K. (2009). Why do men hunt? A reevaluation of “man the hunter” and the sexual division of labor. Current Anthropology, 50, 51–74.

    Article  Google Scholar 

  • Hagen, E. H., & Barrett, H. C. (2009). Cooperative breeding and adolescent siblings: evidence for the ecological constraints model? Current Anthropology, 50, 727–737.

    Article  Google Scholar 

  • Haig, D. (2006). Intragenomic politics. Cytogenetic and Genome Research, 113, 68–74.

    Article  Google Scholar 

  • Haig, D. (2010). Transfers and transitions: parent-offspring conflict, genomic imprinting, and the evolution of human life history. Proceedings of the National Academy of Sciences of the United States of America, 107(Supplement 1), 1731–1735.

    Article  Google Scholar 

  • Haig, D., & Wharton, R. (2003). Prader-Willi syndrome and the evolution of human childhood. American Journal of Human Biology, 15(3), 320–329.

    Article  Google Scholar 

  • Hamilton, W. D. (1966). The moulding of senescence by natural selection. Journal of Theoretical Biology, 12(1), 12–45.

    Article  Google Scholar 

  • Harpending, H. (2002). Kinship and population subdivision. Population and Environment, 24(2), 141–147.

    Article  Google Scholar 

  • Hausfater, G., & Hrdy, S. B. (Eds.). (1984). Infanticide: Comparative and evolutionary perspectives. New York: Aldine.

    Google Scholar 

  • He, C., Kraft, P., Chasman, D. I., Buring, J. E., Chen, C., Hankinson, S. E., et al. (2010). A large-scale candidate gene association study of age at menarche and age at natural menopause. Human Genetics, 128(5), 515–527.

    Article  Google Scholar 

  • Heinze, J. (2004). Reproductive conflict in insect societies. In P. J. B. Slater, J. S. Rosenblatt, T. J. Roper, et al. (Eds.), Advances in the study of behavior (Vol. 34, pp. 1–57). New York: Academic.

    Google Scholar 

  • Heinze, J., & Weber, M. (2011). Lethal sibling rivalry for nest inheritance among virgin ant queens. Journal of Ethology, 29(1), 197–201.

    Article  Google Scholar 

  • Henrich, J., & Boyd, R. (2008). Division of labor, economic specialization and the evolution of social stratification. Current Anthropology, 49, 715–724.

    Article  Google Scholar 

  • Henrich, J., Boyd, R., Bowles, S., Camerer, C., Fehr, E., Gintis, H., et al. (2001). Cooperation, reciprocity and punishment in fifteen small-scale societies. American Economic Review, 91(2), 73–78.

    Article  Google Scholar 

  • Henrich, J., Boyd, R., & Richerson, P. J. (2012). The puzzle of monogamous marriage. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 367(1589), 657–669.

    Article  Google Scholar 

  • Hill, K., & Hurtado, A. M. (2009). Cooperative breeding in South American hunter-gatherers. Proceedings of the Royal Society, Series B: Biological Sciences, 276(1674), 3863–3870.

    Google Scholar 

  • Hill, K., & Hurtado, A. M. (2012). Human reproductive assistance. Nature, 483, 160–162.

    Article  Google Scholar 

  • Hirsh, A. E., & Gordon, D. M. (2001). Distributed problem solving in social insects. Annals of Mathematics and Artificial Intelligence, 31(1–4), 199–221.

    Article  Google Scholar 

  • Holden, C. J., Sear, R., & Mace, R. (2003). Matriliny as daughter-biased investment. Evolution and Human Behavior, 24(2), 99–112.

    Article  Google Scholar 

  • Hölldobler, B. (2010). Territories of the African weaver ant (Oecophylla longinoda [Latreille]): a field study. Zeitschrift für Tierpsychologie, 51(2), 201–213.

    Google Scholar 

  • Hou, C., Kaspari, M., Vander Zanden, H. B., & Gillooly, J. F. (2010). Energetic basis of colonial living in social insects. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3634–3638.

    Article  Google Scholar 

  • Hrdy, S. B. (1999). Mother Nature: A history of mothers, infants and natural selection. New York: Pantheon.

    Google Scholar 

  • Hrdy, S. B. (2005). Evolutionary context of human development: The cooperative breeding hypothesis. In C. S. Carter, L. Ahnert, K. E. Grossmann, S. B. Hrdy, M. E. Lamb, S. W. Porges, & N. Sachser (Eds.), Attachment and bonding: A new synthesis (92nd Dahlem Workshop, pp. 9–32). Cambridge: MIT Press.

  • Hrdy, S. B. (2009). Mothers and others: The evolutionary origins of mutual understanding. Cambridge: Harvard University Press.

    Google Scholar 

  • Hunt, J. H., & Nalepa, C. A. (Eds.). (1994). Nourishment & evolution in insect societies. Boulder: Westview Press.

    Google Scholar 

  • Hvilsom, C., Qian, Y., Bataillon, T., Li, Y., Mailund, T., Sallé, B., et al. (2012). Extensive X-linked adaptive evolution in central chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 109(6), 2054–2059.

    Article  Google Scholar 

  • Isler, K., & van Schaik, C. P. (2012). Allomaternal care, life history and brain size evolution in mammals. Journal of Human Evolution, 63(1), 52–63.

    Article  Google Scholar 

  • Jablonka, E. (2004). The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view. BioEssays, 26(12), 1327–1332.

    Article  Google Scholar 

  • Jamison, C. S., Cornell, L. L., Jamison, P. L., & Nakazato, H. (2002). Are all grandmothers equal? A review and a preliminary test of the “grandmother hypothesis” in Tokugawa Japan. American Journal of Physical Anthropology, 119(1), 67–76.

    Article  Google Scholar 

  • Jiao, X., Qin, C., Li, J., Qin, Y., Gao, X., Zhang, B., et al. (2012). Cytogenetic analysis of 531 Chinese women with premature ovarian failure. Human Reproduction, 27(7), 2201–2207.

    Article  Google Scholar 

  • Johnstone, R. A., & Cant, M. A. (2010). The evolution of menopause in cetaceans and humans: the role of demography. Proceedings of the Royal Society, Series B: Biological Sciences, 277(1701), 3765–3771.

    Google Scholar 

  • Jones, D. (2011). The matrilocal tribe: an organization of demic expansion. Human Nature, 22(1–2), 177–200.

    Article  Google Scholar 

  • Kachel, A. F., & Premo, L. S. (2012). Disentangling the evolution of early and late life history traits in humans. Evolutionary Biology. doi:10.1007/s11692-012-9169-4.

    Google Scholar 

  • Kaplan, H. S., & Gurven, M. (2005). The natural history of human food sharing and cooperation: A review and a new multi-individual approach to the negotiation of norms. In H. Gintis, S. Bowles, R. Boyd, & E. Fehr (Eds.), Moral sentiments and material interests: The foundations of cooperation in economic life (pp. 75–114). Cambridge: MIT Press.

    Google Scholar 

  • Kaplan, H. S., & Robson, A. J. (2002). The emergence of humans: the coevolution of intelligence and longevity with intergenerational transfers. Proceedings of the National Academy of Sciences of the United States of America, 99(15), 10221–10226.

    Article  Google Scholar 

  • Kaptein, N., Billen, J., & Gobin, B. (2005). Larval begging for food enhances reproductive options in the ponerine ant Gnamptogenys striatula. Animal Behaviour, 69, 293–299.

    Article  Google Scholar 

  • Keeley, L. H. (1996). War before civilization. USA: Oxford University Press.

    Google Scholar 

  • Keller, L., & Genoud, M. (1997). Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature, 389, 958–960.

    Article  Google Scholar 

  • Kelly, R. L. (1983). Hunter-gatherer mobility strategies. Journal of Anthropological Research, 39(3), 277–306.

    Google Scholar 

  • Kesebir, S. (2012). The superorganism account of human sociality: how and when human groups are like beehives. Personality and Social Psychology Review, 16(3), 233–261.

    Article  Google Scholar 

  • Kim, P. S., Coxworth, J. E., & Hawkes, K. (2012). Increased longevity evolves from grandmothering. Proceedings of the Royal Society, Series B: Biological Sciences, 279(1749), 4880–4884.

    Google Scholar 

  • Kokko, H., Johnstone, R. A., & Clutton-Brock, T. H. (2001). The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society, Series B: Biological Sciences, 268(1463), 187–196.

    Google Scholar 

  • Kong, A., Frigge, M. L., Masson, G., Besenbacher, S., Sulem, P., Magnusson, G., et al. (2012). Rate of de novo mutations and the importance of father’s age to disease risk. Nature, 488(7412), 471–475.

    Article  Google Scholar 

  • Kramer, K. L. (2005). Children’s help and the pace of reproduction: cooperative breeding in humans. Evolutionary Anthropology, 14, 224–237.

    Article  Google Scholar 

  • Kramer, K. L. (2007). Application of an integrated cooperation approach to human cooperative breeders. Behavioural Processes, 76(2), 167–169.

    Article  Google Scholar 

  • Kramer, K. L. (2010). Cooperative breeding and its significance to the demographic success of humans. Annual Review of Anthropology, 39, 417–436.

    Article  Google Scholar 

  • Kramer, K. L. (2011). The evolution of human parental care and recruitment of juvenile help. Trends in Ecology & Evolution, 26(10), 533–540.

    Article  Google Scholar 

  • Kramer, K. L., & Ellison, P. T. (2010). Pooled energy budgets: resituating human energy allocation trade-offs. Evolutionary Anthropology, 19, 136–147.

    Article  Google Scholar 

  • Lahdenperä, M., Russell, A. F., Tremblay, M., & Lummaa, V. (2011). Selection on menopause in two premodern human populations: no evidence for the Mother Hypothesis. Evolution, 65(2), 476–489.

    Article  Google Scholar 

  • Lahdenperä, M., Gillespie, D. O. S., Lummaa, V., & Russell, A. F. (2012). Severe intergenerational reproductive conflict and the evolution of menopause. Ecology Letters, 15(11), 1283–1290.

    Article  Google Scholar 

  • Lassek, W. D., & Gaulin, S. J. (2007). Menarche is related to fat distribution. American Journal of Physical Anthropology, 133(4), 1147–1151.

    Article  Google Scholar 

  • Le Bourg, E. (2007). Does reproduction decrease longevity in human beings? Ageing Research Reviews, 6, 141–149.

    Article  Google Scholar 

  • Leadbeater, E., Carruthers, J. M., Green, J. P., et al. (2011). Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science, 333(6044), 874–876.

    Article  Google Scholar 

  • Leonetti, D. L., & Chabot-Hanowell, B. (2011). The foundations of kinship: households. Human Nature, 22(1–2), 16–40.

    Article  Google Scholar 

  • Loat, C. S., Asbury, K., Galsworthy, M. J., Plomin, R., & Craig, I. W. (2004). X inactivation as a source of behavioural differences in monozygotic female twins. Twin Research, 7(1), 54–61.

    Article  Google Scholar 

  • Loope, K. J., & Jeanne, R. L. (2008). A test of adaptive hypotheses for rapid nest construction in a swarm-founding wasp. Insectes Sociaux, 55(3), 274–282.

    Article  Google Scholar 

  • Lukas, D., & Clutton-Brock, T. (2012). Life histories and the evolution of cooperative breeding in mammals. Proceedings of the Royal Society, Series B: Biological Sciences, 279(1744), 4065–4070.

  • Mace, R., & Alvergne, A. (2012). Female reproductive competition within families in rural Gambia. Proceedings of the Royal Society, Series B: Biological Sciences, 279(1736), 2219–2227.

  • Marlowe, F. W. (1998). The nobility hypothesis: the human breast as an honest signal of residual reproductive value. Human Nature, 9(3), 263–271.

    Google Scholar 

  • Mas, F., & Kölliker, M. (2008). Maternal care and offspring begging in social insects: chemical signalling, hormonal regulation and evolution. Animal Behaviour, 76, 1121–1131.

    Article  Google Scholar 

  • Mathew, S., & Boyd, R. (2011). Punishment sustains large-scale cooperation in prestate warfare. Proceedings of the National Academy of Sciences, 108(28), 11375–11380.

    Article  Google Scholar 

  • Miles, J. H., McCathren, R. B., Stichter, J., & Shinawi, M. (2003). Autism spectrum disorders. In R. A. Pagon, T. D. Bird, C. R. Dolan, et al. (Eds.), GeneReviews™ . Seattle: University of Washington. Available from http://www.ncbi.nlm.nih.gov/books/NBK1442/.

  • Mitteldorf, J. (2010). Female fertility and longevity. Age (Dordrecht), 32(1), 79–84.

    Article  Google Scholar 

  • Monget, P., Bobe, J., Gougeon, A., Fabre, S., Monniaux, D., & Dalbies-Tran, R. (2012). The ovarian reserve in mammals: a functional and evolutionary perspective. Molecular and Cellular Endocrinology, 356(1–2), 2–12.

    Article  Google Scholar 

  • Monnin, T. (2006). Chemical recognition of reproductive status in social insects. Annales Zoologici Fennici, 43, 515–530.

    Google Scholar 

  • Moreau, C., Bhérer, C., Vézina, H., Jomphe, M., Labuda, D., & Excoffier, L. (2011). Deep human genealogies reveal a selective advantage to be on an expanding wave front. Science, 334(6059), 1148–1150.

    Article  Google Scholar 

  • Mueller, U. G., Rehner, S. A., & Schultz, T. R. (1998). The evolution of agriculture in ants. Science, 281(5385), 2034–2038.

    Article  Google Scholar 

  • Myrskylä, M., & Fenelon, A. (2012). Maternal age and offspring adult health: evidence from the health and retirement study. Demography. doi:10.1007/s13524-012-0132-x.

    Google Scholar 

  • Nettle, D., & Dunbar, R. I. M. (1997). Social markers and the evolution of reciprocal exchange. Current Anthropology, 38(1), 93–99.

    Article  Google Scholar 

  • Nguyen, D. K., & Disteche, C. M. (2006). High expression of the mammalian X chromosome in brain. Brain Research, 1126(1), 46–49.

    Article  Google Scholar 

  • Nichols, H. J., Bell, M. B. V., Hodge, S. J., & Cant, M. A. (2012). Resource limitation moderates the adaptive suppression of subordinate breeding in a cooperatively breeding mongoose. Behavioral Ecology, 23(3), 635–642.

    Article  Google Scholar 

  • Oster, G. F., & Wilson, E. O. (1978). Caste and ecology in the social insects. Monographs in population biology (Vol. 12). Princeton: Princeton University Press.

    Google Scholar 

  • Parker, J. D. (2010). What are social insects telling us about aging? Myrmecological News, 13, 103–110.

    Google Scholar 

  • Persani, L., Rossetti, R., & Cacciatore, C. (2010). Genes involved in human premature ovarian failure. Journal of Molecular Endocrinology, 45(5), 257–279.

    Article  Google Scholar 

  • Powell, S. (2011). How much do army ants eat? On the prey intake of a neotropical top-predator. Insectes Sociaux, 58(3), 317–324.

    Article  Google Scholar 

  • Qin, Y., Sun, M., You, L., Wei, D., Sun, J., Liang, X., et al. (2012). ESR1, HK3 and BRSK1 gene variants are associated with both age at natural menopause and premature ovarian failure. Orphanet Journal of Rare Diseases, 7(5), 1–6.

    Google Scholar 

  • Queller, D. C. (1989). The evolution of eusociality: reproductive head starts of workers. Proceedings of the National Academy of Sciences of the United States of America, 86(9), 3224–3226.

    Article  Google Scholar 

  • Queller, D. C. (1994). Extended parental care and the origin of eusociality. Proceedings of the Royal Society of London Series B, 256, 105–111.

    Article  Google Scholar 

  • Quinlan, R. J., & Flinn, M. V. (2005). Kinship and reproduction in a Caribbean community. Human Nature, 16(1), 32–57.

    Google Scholar 

  • Quinlan, R. J., & Quinlan, M. B. (2008). Human lactation, pair-bonds, and alloparents: a cross-cultural analysis. Human Nature, 19(1), 87–102.

    Google Scholar 

  • Ragsdale, J. E. (1999). Reproductive skew theory extended: the effect of resource inheritance on social organization. Evolutionary Ecology Research, 1, 859–874.

    Google Scholar 

  • Ratnieks, F. L. W., & Anderson, C. (1999). Task partitioning in insect societies. Insectes Sociaux, 47(2), 95–108.

    Article  Google Scholar 

  • Ratnieks, F. L., & Wenseleers, T. (2005). Policing insect societies. Science, 307(5706), 54–56.

    Article  Google Scholar 

  • Reddy, P., Adhikari, D., Zheng, W., Liang, S., Hämäläinen, T., Tohonen, V., et al. (2009). PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Human Molecular Genetics, 18(15), 2813–2824.

    Article  Google Scholar 

  • Reeve, H. K., & Shellman-Reeve, J. S. (1997). The general protected invasion theory: sex biases in parental and alloparental care. Evolutionary Ecology, 11, 357–370.

    Article  Google Scholar 

  • Reiches, M. W., Ellison, P. T., Lipson, S. F., Sharrock, K. C., Gardiner, E., & Duncan, L. G. (2009). Pooled energy budget and human life history. American Journal of Human Biology, 21(4), 421–429.

    Article  Google Scholar 

  • Rice, W. R., Gavrilets, S., & Friberg, U. (2010). The evolution of sex-specific grandparental harm. Proceedings of the Royal Society, Series B: Biological Sciences, 277(1694), 2727–2735.

    Google Scholar 

  • Rodriguez-Serrano, E., Inostroza-Michael, O., Avaria-Llautureo, J., & Hernandez, C. E. (2012). Colony size evolution and the origin of eusociality in corbiculate bees (Hymenoptera: Apinae). PLoS One, 7(7), e40838.

    Article  Google Scholar 

  • Schmid-Hempel, P. (1998). Parasites in social insects. Princeton: Princeton University Press.

    Google Scholar 

  • Schoenstadt, A. (2006). Children with Klinefelter Syndrome. Resource document. Genetics Health Channel by eMedTV. http://genetics.emedtv.com/klinefelter-syndrome/children-with-klinefelter-syndrome.html. Accessed 9 November 2012.

  • Schrempf, A., Cremer, S., & Heinze, J. (2011). Social influence on age and reproduction: reduced lifespan and fecundity in multi-queen ant colonies. Journal of Evolutionary Biology, 24(7), 1455–1461.

    Article  Google Scholar 

  • Schultz, T. R., & Brady, S. G. (2008). Major evolutionary transitions in ant agriculture. Proceedings of the National Academy of Sciences of the United States of America, 105(14), 5435–5440.

    Article  Google Scholar 

  • Sear, R., & Mace, R. (2008). Who keeps children alive? A review of the effects of kin on child survival. Evolution and Human Behavior, 29(1), 1–18.

    Article  Google Scholar 

  • Seeley, T. D. (2010). Honeybee democracy. Princeton: Princeton University Press.

    Google Scholar 

  • Sellen, D. W. (2007). Evolution of infant and young child feeding: implications for contemporary public health. Annual Review of Nutrition, 27, 123–148.

    Article  Google Scholar 

  • Semeiks, J., & Grishin, N. V. (2012). A method to find longevity-selected positions in the mammalian proteome. PLoS One, 7(6), e38595.

    Article  Google Scholar 

  • Service, E. R. (1975). Origins of the state and civilization: The process of cultural evolution. New York: Norton.

    Google Scholar 

  • Singh, D., Dixson, B. J., Jessop, T. S., Morgan, B., & Dixson, A. F. (2010). Cross-cultural consensus for waist-hip ratio and women’s attractiveness. Evolution and Human Behavior, 31(3), 176–181.

    Article  Google Scholar 

  • Skillern, A., & Rajkovic, A. (2008). Recent developments in identifying genetic determinants of premature ovarian failure. Sexual Development, 2(4–5), 228–243.

    Article  Google Scholar 

  • Skuse, D. H. (2006a). Genetic influences on the neural basis of social cognition. Philosophical Transactions of the Royal Society, Series B: Biological Sciences, 361(1476), 2129–2141.

    Article  Google Scholar 

  • Skuse, D. H. (2006b). Sexual dimorphism in cognition and behaviour: the role of X-linked genes. European Journal of Endocrinology, 155, S99–S106. doi:10.1530/eje.1.02263.

    Article  Google Scholar 

  • Solomon, N. G., & French, J. A. (Eds.). (1997). Cooperative breeding in mammals. New York: Cambridge University Press.

    Google Scholar 

  • Stacey, P. B., & Koenig, W. D. (Eds.). (1990). Cooperative breeding in birds: Long term studies of ecology and behaviour. Cambridge: Cambridge University Press.

    Google Scholar 

  • Strassmann, B. I. (2011). Cooperation and competition in a cliff-dwelling people. Proceedings of the National Academy of Sciences of the United States of America, 108(Supplement 2), 10894–10901.

    Article  Google Scholar 

  • Strassmann, B. I., & Garrard, W. M. (2011). Alternatives to the grandmother hypothesis: a meta-analysis of the association between grandparental and grandchild survival in patrilineal populations. Human Nature, 22(1–2), 201–222.

    Article  Google Scholar 

  • Strassmann, B. I., & Clarke, A. L. (1998). Ecological constraints on marriage in rural Ireland. Evolution and Human Behavior, 19(1), 33–55.

    Article  Google Scholar 

  • Strassmann, B. I., & Kurapati, N. T. (2010). Are humans cooperative breeders? Most studies of natural fertility populations do not support the grandmother hypothesis. Behavioral and Brain Sciences, 33(1), 35–39.

    Google Scholar 

  • Strassmann, J. E., & Queller, D. C. (2010). The social organism: congresses, parties, and committees. Evolution, 63(3), 605–616.

    Article  Google Scholar 

  • Strassmann, B. I., & Warner, J. H. (1998). Predictors of fecundability and conception waits among the Dogon of Mali. American Journal of Physical Anthropology, 105(2), 167–184.

    Article  Google Scholar 

  • Sullivan, S. D., Welt, C., & Sherman, S. (2011). FMR1 and the continuum of primary ovarian insufficiency. Seminars in Reproductive Medicine, 29(4), 299–307.

    Article  Google Scholar 

  • Tanskanen, A. O., Rotkirch, A., & Danielsbacka, M. (2011). Do grandparents favor granddaughters? Biased grandparental investment in UK. Evolution and Human Behavior, 32(6), 407–415.

    Article  Google Scholar 

  • te Velde, E. R., & Pearson, P. L. (2002). The variability of female reproductive ageing. Human Reproduction Update, 8(2), 141–154.

    Article  Google Scholar 

  • Úbeda, F., & Duéñez-Guzmá, E. A. (2011). Power and corruption. Evolution, 65(4), 1127–1139.

    Article  Google Scholar 

  • Uematsu, K., Kutsukake, M., Fukatsu, T., Shimada, M., & Shibao, H. (2010). Altruistic colony defense by menopausal female insects. Current Biology, 20(13), 1182–1186.

    Article  Google Scholar 

  • Valeggia, C. R. (2009). Flexible caretakers: Responses of Toba families in transition. In G. Bentley & R. Mace (Eds.), Substitute parents: Biological and social perspectives on alloparenting in human societies. Studies in biosocial science series (pp. 100–115). Oxford/New York: Berghahn Press.

    Google Scholar 

  • Vallender, E. J., & Lahn, B. T. (2004). How mammalian sex chromosomes acquired their peculiar gene content. BioEssays, 26(2), 159–169.

    Article  Google Scholar 

  • Vallender, E. J., Pearson, N. M., & Lahn, B. T. (2005). The X chromosome: not just her brother’s keeper. Nature Genetics, 37, 343–345.

    Article  Google Scholar 

  • van Schaik, C. P., & Burkart, J. M. (2009). Mind the gap: Cooperative breeding and the evolution of our unique features. In P. M. Kappeler & J. Silk (Eds.), Mind the gap: Tracing the origins of human universals (pp. 477–496). Heidelberg: Springer.

    Google Scholar 

  • van Zweden, J. S., & d’Ettorre, P. (2010). Nestmate recognition in social insects and the role of hydrocarbons. In G. J. Blomquist & A.-G. Bagnères (Eds.), Insect hydrocarbons: Biology, biochemistry, and chemical ecology (pp. 222–243). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Vicoso, B., & Charlesworth, B. (2009). Effective population size and the faster-X effect: an extended model. Evolution, 63(9), 2413–2426.

    Article  Google Scholar 

  • Walker, R., Hill, K., Kaplan, H., & McMillan, G. (2002). Age dependency of hunting ability among the Ache of eastern Paraguay. Journal of Human Evolution, 42, 639–657.

    Article  Google Scholar 

  • Wells, J. C. (2003). Parent-offspring conflict theory, signaling of need, and weight gain in early life. Quarterly Review of Biology, 78(2), 169–202.

    Article  Google Scholar 

  • Wells, J. C., & Stock, J. T. (2007). The biology of the colonizing ape. Yearbook of Physical Anthropology, 50, 191–222.

    Article  Google Scholar 

  • Wenzel, J. W., & Pickering, J. (1991). Cooperative foraging, productivity, and the central limit theorem. Proceedings of the National Academy of Sciences of the United States of America, 88, 36–38.

    Article  Google Scholar 

  • Whiten, A., & Erdal, D. (2012). The human socio-cognitive niche and its evolutionary origins. Philosophical Transactions of the Royal Society, B: Biological Sciences, 367(1599, Special Issue: SI), 2119–2129.

    Article  Google Scholar 

  • Wilder, J. A. (2010). Do grandmothers who play favorites sow seeds of genomic conflict? BioEssays, 32(6), 457–460.

    Article  Google Scholar 

  • Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11(4), 398–411.

    Article  Google Scholar 

  • Wilson, D. S., Timmel, J. J., & Miller, R. R. (2004). Cognitive cooperation – When the going gets tough, think as a group. Human Nature, 15(3), 225–250.

    Article  Google Scholar 

  • Wilson, E. O. (1971). The insect societies. Cambridge: Belknap.

    Google Scholar 

  • Wilson, E. O. (2012). The social conquest of earth. New York: Liveright Press.

    Google Scholar 

  • Zechner, U., Wilda, M., Kehrer-Sawatzki, H., Vogel, W., Fundele, R., & Hameister, H. (2001). A high density of X-linked genes for general cognitive ability: a run-away process shaping human evolution? Trends in Genetics, 17(12), 697–701.

    Article  Google Scholar 

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Acknowledgments

I am grateful to L. Betzig, A. Bourke, F. de Ubeda, P. Ellison, S. Frank, E. Hagen, K. Hill, A. Mooers, P. Nepomnaschy, T. Schwander, B. Strassmann, and P. Turke for helpful comments, and to L. Betzig and J. Lancaster for inviting me to contribute this article. I thank the Natural Sciences and Engineering Research Council of Canada for financial support and S. Read for technical assistance.

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    Bernard Crespi

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Crespi, B. The Insectan Apes. Hum Nat 25, 6–27 (2014). https://doi.org/10.1007/s12110-013-9185-9

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