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Stepwise evolution of stable sociality in primates

Nature volume 479, pages 219–222 (2011)Cite this article

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Abstract

Although much attention has been focused on explaining and describing the diversity of social grouping patterns among primates1,2,3, less effort has been devoted to understanding the evolutionary history of social living4. This is partly because social behaviours do not fossilize, making it difficult to infer changes over evolutionary time. However, primate social behaviour shows strong evidence for phylogenetic inertia, permitting the use of Bayesian comparative methods to infer changes in social behaviour through time, thereby allowing us to evaluate alternative models of social evolution. Here we present a model of primate social evolution, whereby sociality progresses from solitary foraging individuals directly to large multi-male/multi-female aggregations (approximately 52 million years (Myr) ago), with pair-living (approximately 16 Myr ago) or single-male harem systems (approximately 16 Myr ago) derivative from this second stage. This model fits the data significantly better than the two widely accepted alternatives (an unstructured model implied by the socioecological hypothesis or a model that allows linear stepwise changes in social complexity through time). We also find strong support for the co-evolution of social living with a change from nocturnal to diurnal activity patterns, but not with sex-biased dispersal. This supports suggestions that social living may arise because of increased predation risk associated with diurnal activity. Sociality based on loose aggregation is followed by a second shift to stable or bonded groups. This structuring facilitates the evolution of cooperative behaviours5 and may provide the scaffold for other distinctive anthropoid traits including coalition formation, cooperative resource defence and large brains.

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Figure 1: Primate phylogeny showing ancestral state reconstructions for sociality under the reversible-jump Markov chain Monte Carlo-derived model of evolution.
Figure 2: Alternative evolutionary models of primate social evolution.
Figure 3: Estimated transition rates for co-evolution of social living.
Figure 4: Alternative evolutionary models for the evolution of stable grouping patterns.

References

  1. van Schaik, C. P. Why are diurnal primates living in groups? Behaviour 87, 120–144 (1983)

    Article  Google Scholar 

  2. Terborgh, J. & Janson, C. H. The socioecology of primate groups. Annu. Rev. Ecol. Syst. 17, 111–135 (1986)

    Article  Google Scholar 

  3. Sterck, H. M., Watts, D. P. & van Schaik, C. P. The evolution of female social relationships in nonhuman primates. Behav. Ecol. Sociobiol. 41, 291–309 (1997)

    Article  Google Scholar 

  4. Di Fiore, A. & Rendall, D. Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc. Natl Acad. Sci. USA 91, 9941–9945 (1994)

    Article  CAS  ADS  Google Scholar 

  5. Nowak, M. A., Tarnita, C. E. & Wilson, E. O. The evolution of eusociality. Nature 466, 1057–1062 (2010)

    Article  CAS  ADS  Google Scholar 

  6. Shultz, S. & Dunbar, R. I. M. The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc. R. Soc. Lond. B 274, 2429–2436 (2007)

    Article  Google Scholar 

  7. Elton, S. Forty years on and still going strong: the use of hominin-cercopithecid comparisons in palaeoanthropology. J. R. Anthropol. Inst. 12, 19–38 (2006)

    Article  Google Scholar 

  8. Jarman, P. J. The social organisation of antelope in relation to their ecology. Behaviour 48, 215–268 (1974)

    Article  Google Scholar 

  9. Kappeler, P. M. & van Schaik, C. P. Evolution of primate social systems. Int. J. Primatol. 23, 707–740 (2002)

    Article  Google Scholar 

  10. Gould, S. J. & Lewontin, R. C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205, 581–598 (1979)

    Article  CAS  ADS  Google Scholar 

  11. Stirling, D. G., Réale, D. & Roff, D. A. Selection, structure and the heritability of behaviour. J. Evol. Biol. 15, 277–289 (2002)

    Article  Google Scholar 

  12. Arnold, C., Matthews, L. J. & Nunn, C. L. The 10kTrees website: a new online resource for primate phylogeny Evol. Anthropol. 19, 114–118 (2010)

    Google Scholar 

  13. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)

    Article  CAS  ADS  Google Scholar 

  14. Dunbar, R. I. M. in Primate Males: Causes and Consequences of Variation in Group Composition (ed. Kappeler, P. M. ) 259–268 (Cambridge Univ. Press, 2000)

    Google Scholar 

  15. Nunn, C. L. & van Schaik, C. P. in Reconstructing Behavior in the Primate Fossil Record (eds Plavcan, J. M., Kay, R. F., Jungers, W. L. & van Schaik, C. P. ) 159–216 (Plenum, 2001)

    Google Scholar 

  16. Müller, A. E. & Thalmann, U. Origin and evolution of primate social organisation: a reconstruction. Biol. Rev. Camb. Philos. Soc. 75, 405–435 (2000)

    Article  Google Scholar 

  17. Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010)

    Article  CAS  ADS  Google Scholar 

  18. Shultz, S. & Dunbar, R. I. M. Life-history, social bonding and adaptive peak shifts in avian brain evolution. Biol. J. Linn. Soc. 100, 111–123 (2010)

    Article  Google Scholar 

  19. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008)

    Article  CAS  ADS  Google Scholar 

  20. Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006)

    PubMed  Google Scholar 

  21. Rambaut, A. & Drummond, A. J. Tracer v1.4. Tracer 〈http://beast.bio.ed.ac.uk/Tracer〉 (2007)

  22. Kass, R. E. & Raftery, A. E. Bayes Factors. J. Am. Stat. Assoc. 90, 773–795 (1995)

    Article  MathSciNet  Google Scholar 

  23. Barton, R. A. Visual specialization and brain evolution in primates. Proc. R. Soc. Lond. B 265, 1933–1937 (1998)

    Article  CAS  Google Scholar 

  24. Greenwood, P. J. Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28, 1140–1162 (1980)

    Article  Google Scholar 

  25. Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, 1998)

    Google Scholar 

  26. Hamilton, W. D. The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17–52 (1964)

    Article  CAS  Google Scholar 

  27. Gompper, M. E., Gittleman, J. L. & Wayne, R. K. Genetic relatedness, coalitions and social behaviour of white-nosed coatis, Nasua narica. Anim. Behav. 53, 781–797 (1997)

    Article  Google Scholar 

  28. Broad, K. D., Curley, J. P. & Keverne, E. B. Mother–infant bonding and the evolution of mammalian social relationships. Phil. Trans. R. Soc. B 361, 2199–2214 (2006)

    Article  CAS  Google Scholar 

  29. Shultz, S. & Dunbar, R. I. M. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl Acad. Sci. USA 107, 21582–21586 (2010)

    Article  CAS  ADS  Google Scholar 

  30. Drummond, A. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007)

    Article  Google Scholar 

  31. Campbell, C. J., Fuentes, A., MacKinnon, K. C., Panger, M. & Bearder, S. K. Primates in Perspective (Oxford Univ. Press, 2007)

    Google Scholar 

  32. Dixson, A. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings (Oxford Univ. Press, 1998)

    Google Scholar 

  33. Dunbar, R. I. M. Primate Social Systems (Chapman & Hall, 1988)

    Book  Google Scholar 

  34. Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R. & Struhsaker, T. Primate Societies (Univ. Chicago Press, 1987)

    Google Scholar 

  35. Isbell, L. A. & van Vuren, D. Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133, 1–36 (1996)

    Article  Google Scholar 

  36. Jack, K. M. & Isbell, L. A. Dispersal in primates: advancing an individualized approach. Behaviour 146, 429–436 (2009)

    Article  Google Scholar 

  37. Schulke, O. & Ostner, J. Big times for dwarfs: social organization, sexual selection, and cooperation in the Cheirogaleidae. Evol. Anthropol. 14, 170–185 (2005)

    Article  Google Scholar 

  38. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008)

    Article  CAS  Google Scholar 

  39. Pagel, M. D. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37–45 (1994)

    Article  ADS  Google Scholar 

  40. Freckleton, R. P., Harvey, P. H. & Pagel, M. D. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002)

    Article  CAS  Google Scholar 

  41. Pagel, M. D., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004)

    Article  Google Scholar 

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Acknowledgements

S.S. is supported by a Royal Society Dorothy Hodgkin Fellowship. We thank R.I.M. Dunbar for comments on the manuscript.

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Authors and Affiliations

  1. Institute of Cognitive and Evolutionary Anthropology, 64 Banbury Road, University of Oxford, Oxford OX2 6PN, UK,

    Susanne Shultz, Christopher Opie & Quentin D. Atkinson

  2. Department of Psychology, University of Auckland, Private Bag 92019, Auckland, New Zealand,

    Quentin D. Atkinson

Authors
  1. Susanne Shultz
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  2. Christopher Opie
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  3. Quentin D. Atkinson
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Contributions

S.S. designed the study, compiled the data and executed analyses. C.O. executed analyses. Q.A. was involved in study design and advised on statistical analyses. All authors contributed to the manuscript.

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Correspondence to Susanne Shultz.

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The authors declare no competing financial interests.

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This file contains Supplementary Tables 1-6, Supplementary Figures 1-3 with legends and Supplementary References for Supplementary Table 6. (PDF 994 kb)

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Shultz, S., Opie, C. & Atkinson, Q. Stepwise evolution of stable sociality in primates. Nature 479, 219–222 (2011). https://doi.org/10.1038/nature10601

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