Primate brain size is predicted by diet but not sociality

Abstract

The social brain hypothesis posits that social complexity is the primary driver of primate cognitive complexity, and that social pressures ultimately led to the evolution of the large human brain. Although this idea has been supported by studies indicating positive relationships between relative brain and/or neocortex size and group size, reported effects of different social and mating systems are highly conflicting. Here, we use a much larger sample of primates, more recent phylogenies, and updated statistical techniques, to show that brain size is predicted by diet, rather than multiple measures of sociality, after controlling for body size and phylogeny. Specifically, frugivores exhibit larger brains than folivores. Our results call into question the current emphasis on social rather than ecological explanations for the evolution of large brains in primates and evoke a range of ecological and developmental hypotheses centred on frugivory, including spatial information storage, extractive foraging and overcoming metabolic constraints.

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Figure 1: Ancestral reconstructions of primate EQ (left) and mean group size (right).

References

  1. 1

    Healy, S. D. & Rowe, C. A critique of comparative studies of brain size. Proc. R. Soc. B 274, 453–464 (2007).

    Article  PubMed  Google Scholar 

  2. 2

    Barton, R. A. Neocortex size and behavioural ecology in primates. Proc. R. Soc. Lond. B 263, 173–177 (1996).

    Article  CAS  Google Scholar 

  3. 3

    Clutton-Brock, T. H. & Harvey, P. H. Primates, brains and ecology. J. Zool. 190, 309–323 (1980).

    Article  Google Scholar 

  4. 4

    Harvey, P. H. & Krebs, J. R. Comparing brains. Science 249, 140–146 (1990).

    Article  CAS  PubMed  Google Scholar 

  5. 5

    Gibson, K. R. in Primate Ontogeny, Cognition and Social Behaviour (eds Lee, P. C. & Lee, J. G. ) 93–104 (Cambridge Univ. Press, 1986).

    Google Scholar 

  6. 6

    Wrangham, R. & Carmody, R. Human adaptation to the control of fire. Evol. Anthropol. 19, 187–199 (2010).

    Article  Google Scholar 

  7. 7

    Zink, K. D. & Lieberman, D. E. Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans. Nature 531, 500–503 (2016).

    Article  CAS  PubMed  Google Scholar 

  8. 8

    Martin, R. D. Human brain evolution in an ecological context. Fifty-Second James Arthur Lecture on “The Evolution of the Human Brain,” (American Museum of Natural History 1983).

  9. 9

    Armstrong, E. Relative brain size in monkeys and prosimians. Am. J. Phys. Anthropol. 66, 263–273 (1985).

    Article  CAS  PubMed  Google Scholar 

  10. 10

    Pontzer, H. et al. Metabolic acceleration and the evolution of human brain size and life history. Nature 533, 390–392 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Isler, K. & van Schaik, C. P. The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57, 392–400 (2009).

    Article  PubMed  Google Scholar 

  12. 12

    Humphrey, N. K. in Growing Points in Ethology (eds Bateson, P. P. G. & Hinde, R. A. ) 303–317 (Cambridge Univ. Press, 1976).

    Google Scholar 

  13. 13

    Jolly, A. Lemur social behavior and primate intelligence. Science 153, 501–506 (1966).

    Article  CAS  PubMed  Google Scholar 

  14. 14

    Dunbar, R. I. M. Neocortex size as a constraint on group size in primates. J. Hum. Evol. 22, 469–493 (1992).

    Article  Google Scholar 

  15. 15

    Dunbar, R. I. M. The social brain hypothesis. Evol. Anthropol. 6, 178–190 (1998).

    Article  Google Scholar 

  16. 16

    Sandel, A. A. et al. Assessing sources of error in comparative analyses of primate behavior: intraspecific variation in group size and the social brain hypothesis. J. Hum. Evol. 94, 126–133 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17

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

    Article  PubMed  Google Scholar 

  18. 18

    Schillaci, M. A. Sexual selection and the evolution of brain size in primates. PLoS ONE 1, e62 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19

    Freckleton, R. P. The seven deadly sins of comparative analysis. J. Evol. Biol. 22, 1367–1375 (2009).

    Article  CAS  PubMed  Google Scholar 

  20. 20

    Purvis, A. A. A composite estimate of primate phylogeny. Phil. Trans. R. Soc. Lond. B 348, 405–421 (1995).

    Article  CAS  Google Scholar 

  21. 21

    Barton, R. A. & Harvey, P. H. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058 (2000).

    Article  CAS  Google Scholar 

  22. 22

    Pérez-Barbería, F. J., Shultz, S. & Dunbar, R. I. M. Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61, 2811–2821 (2007).

    Article  PubMed  Google Scholar 

  23. 23

    Barton, R. A. Embodied cognitive evolution and the cerebellum. Phil. Trans. R. Soc. B 367, 2097–2107 (2012).

    Article  PubMed  Google Scholar 

  24. 24

    Shultz, S. & Dunbar, R. I. M. Species differences in executive function correlate with hippocampus volume and neocortex ratio across nonhuman primates. J. Comp. Psychol. 124, 252–260 (2010).

    Article  PubMed  Google Scholar 

  25. 25

    Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2011).

    Article  CAS  Google Scholar 

  26. 26

    Deaner, R. O., Isler, K., Burkart & J. & van Schaik, C. P. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 70, 115–124 (2007).

    Article  PubMed  Google Scholar 

  27. 27

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

    Article  Google Scholar 

  28. 28

    Perelman, P. et al. A molecular phylogeny of living primates. PLoS Genet. 7, e1001342 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Raftery, A. E. Bayesian model selection in social research. Sociol. Methodol. 25, 111–164 (1995).

    Article  Google Scholar 

  30. 30

    Herculano-Houzel, S. & Kaas, J. H. Gorilla and orangutan brains conform to the primate cellular scaling rules: implications for human evolution. Brain Behav. Evol. 77, 33–44 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Jerison, H. J. Evolution of the Brain and Intelligence (Academic, 1973).

    Google Scholar 

  32. 32

    Montgomery, S. H., Capellini, I., Barton, R. A. & Mundy, N. I. Reconstructing the ups and downs of primate brain evolution: implications for adaptive hypotheses and Homo floresiensis. BMC Biol. 8, 9 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33

    Fedigan, L. M. Vertebrate predation in Cebus capucinus: meat eating in a neotropical monkey. Folia Primatol. 54, 196–205 (1990).

    Article  CAS  PubMed  Google Scholar 

  34. 34

    Navarrete, A., van Schaik, C. P. & Isler, K. Energetics and the evolution of human brain size. Nature 480, 91–93 (2011).

    Article  CAS  PubMed  Google Scholar 

  35. 35

    MacLean, E. L., Barrickman, N. L., Johnson, E. M. & Wall, C. E. Sociality, ecology, and relative brain size in lemurs. J. Hum. Evol. 56, 471–478 (2009).

    Article  PubMed  Google Scholar 

  36. 36

    Manger, P. R. An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol. Rev. 81, 293–338 (2006).

    Article  PubMed  Google Scholar 

  37. 37

    Gittleman, J. L. Carnivore brain size, behavioral ecology, and phylogeny. J. Mammal. 67, 23–36 (1986).

    Article  Google Scholar 

  38. 38

    Beauchamp, G & Fernández-Juricic, E. Is there a relationship between forebrain size and group size in birds? Evol. Ecol. Res. 6, 833–842 (2004).

    Google Scholar 

  39. 39

    Holekamp, K. E., Sakai, S. T. & Lundrigan, B. L. The spotted hyena (Crocuta crocuta) as a model system for study of the evolution of intelligence. J. Mammal. 88, 545–554 (2007).

    Article  Google Scholar 

  40. 40

    Barrett, L., Henzi, P. & Rendall, D. Social brains, simple minds: does social complexity really require cognitive complexity? Phil. Trans. R. Soc. B 362, 561–575 (2007).

    Article  PubMed  Google Scholar 

  41. 41

    Bshary, R., Di Lascio, F., Pinto, A. & van de Waal, E. in Animal Thinking: Contemporary Issues in Comparative Cognition (eds Menzel, R. & Fischer, J. ) 209–221 (MIT Press, 2011).

    Google Scholar 

  42. 42

    Sol, D., Bacher, S., Reader, S. M. & Lefebvre, L. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172, S63–S71 (2008).

    Article  PubMed  Google Scholar 

  43. 43

    Dunbar, R. I. M. & Shultz, S. Understanding primate brain evolution. Phil. Trans. R. Soc. B 362, 649–658 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. 44

    Bergman, T. J. & Beehner, J. C. Measuring social complexity. Anim. Behav. 103, 203–209 (2015).

    Article  Google Scholar 

  45. 45

    Barton, R. A. & Venditti, C. Rapid evolution of the cerebellum in humans and other great apes. Curr. Biol. 24, 2440–2444 (2014).

    Article  CAS  PubMed  Google Scholar 

  46. 46

    Stout, D. & Chaminade, T. Stone tools, language and the brain in human evolution. Phil. Trans. R. Soc. B 367, 75–87 (2012).

    Article  PubMed  Google Scholar 

  47. 47

    Hopkins, W. D., Russell, J. L. & Cantalupo, C. Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes). Implication for theories on the evolution of language. Psychol. Sci. 18, 971–977 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48

    Boddy, A. M. et al. Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling. J. Evol. Biol. 25, 981–994 (2012a).

    Article  CAS  PubMed  Google Scholar 

  49. 49

    Isler, K. et al. Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J. Hum. Evol. 55, 967–978 (2008).

    Article  PubMed  Google Scholar 

  50. 50

    Stephan, H., Frahm, H. & Baron, G. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. 35, 1–29 (1981).

    Article  CAS  PubMed  Google Scholar 

  51. 51

    Harvey, P. H., Martin, R. D. & Clutton-Brock, T. H. in Primate Societies (eds Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wragham, R. W. & Struhsaker, T. T. ) 181–196 (Univ. Chicago Press, 1987).

    Google Scholar 

  52. 52

    Silva, M. & Downing, J. A. CRC Handbook of Mammalian Body Masses (CRC, 1995).

    Google Scholar 

  53. 53

    Tacutu, R. et al. Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res. 41, D1027–D1033 (2013).

    Article  CAS  PubMed  Google Scholar 

  54. 54

    Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648–2648 (2009).

    Article  Google Scholar 

  55. 55

    Plavcan, J. M. & van Schaik, C. P. Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 103, 37–68 (1997).

    Article  CAS  PubMed  Google Scholar 

  56. 56

    Smith, R. J. & Jungers, W. L. Body mass in comparative primatology. J. Hum. Evol. 32, 523–559 (1997).

    Article  CAS  PubMed  Google Scholar 

  57. 57

    Kappeler, P. M. & Heymann, E. W. Nonconvergence in the evolution of primate life history and socio-ecology. Biol. J. Linn. Soc. 59, 297–326 (1996).

    Article  Google Scholar 

  58. 58

    Fox, E. A., van Schaik, C. P., Sitompul, A. & Wright, D. N. Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use. Am. J. Phys. Anthropol. 125, 162–174 (2004).

    Article  PubMed  Google Scholar 

  59. 59

    Shah, N. F. Foraging Strategies in the Two Sympatric Mangabey Species (Cercocebus agilis and Lophocebus albigena) PhD thesis, Stony Brook Univ. (2003).

    Google Scholar 

  60. 60

    Horn, A. D. The socioecology of the black mangabey (Cercocebus aterrimus) near Lake Tumba, Zaire. Am. J. Primatol. 12, 165–180 (2007).

    Article  Google Scholar 

  61. 61

    Rothman, J. M., Plumptre, A. J., Dierenfeld, E. S. & Pell, A. N. Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. J. Trop. Ecol. 23, 673–682 (2007).

    Article  Google Scholar 

  62. 62

    Kaplan, H. S. et al. in Guts and Brains: An Integrative Approach to the Hominin Record (ed. Roebroeks, W. ) 47–90 (Leiden Univ. Press, 2007).

    Google Scholar 

  63. 63

    Sawaguchi, T. & Kudo, H. Neocortical development and social structure in primates. Primates 31, 283–289 (1990).

    Article  Google Scholar 

  64. 64

    Thorén, S., Lindenfors, P. & Kappeler, P. M. Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size. Am. J. Phys. Anthropol. 130, 50–59 (2006).

    Article  PubMed  Google Scholar 

  65. 65

    Plavcan, J. M. in Comparative Primate Socioecology (ed. Lee, P. C. ) 241–269 (Cambridge Univ. Press, 1999).

    Google Scholar 

  66. 66

    Shultz, S., Opie, C. & Atkinson, Q. D. Stepwise evolution of stable sociality in primates. Nature 479, 219–222 (2011).

    Article  CAS  PubMed  Google Scholar 

  67. 67

    Smuts, B. B., Cheney, D. L., Seyfarth, R. M. & Wrangham, R. W. Primate Societies (Univ. Chicago Press, 1987).

    Google Scholar 

  68. 68

    Rowe, N. The Pictoral Guide to the Living Primates (Pogonias, 1996).

    Google Scholar 

  69. 69

    Patterson, S. K., Sandel, A. A., Miller, J. A. & Mitani, J. C. Data quality and the comparative method: the case of primate group size. Int. J. Primatol. 35, 990–1003 (2014).

    Article  Google Scholar 

  70. 70

    Kudo, H. & Dunbar, R. I. M. Neocortex size and social network size in primates. Anim. Behav. 62, 711–722 (2001).

    Article  Google Scholar 

  71. 71

    Wrangham, R. W., Gittleman, J. L. & Chapman, C. A. Constraints on group size in primates and carnivores: population density and day-range as assays of exploitation competition. Behav. Ecol. Sociobiol. 32, 199–209 (1993).

    Article  Google Scholar 

  72. 72

    Dunbar, R. I. M. Functional significance of social grooming in primates. Folia Primatol. 57, 121–131 (1991).

    Article  Google Scholar 

  73. 73

    Clutton-Brock, T. H. & Harvey, P. H. Primate ecology and social organization. J. Zool. 183, 1–39 (1977).

    Article  Google Scholar 

  74. 74

    Eisenberg, J. F. & Redford, K. H. Mammals of the Neotropics, Volume 2: The Southern Cone: Chile, Argentina, Uruguay, Paraguay (Univ. Chicago Press, 1992).

    Google Scholar 

  75. 75

    Garamszegi, L. Z. Modern Phylogenetic Comparative Methods and their Application in Evolutionary Biology (Springer, 2014).

    Google Scholar 

  76. 76

    Lehmann, J. & Dunbar, R. I. M. Network cohesion, group size and neocortex size in female-bonded Old World primates. Proc. R. Soc. B 276, 4417–4422 (2009).

    Article  PubMed  Google Scholar 

  77. 77

    Janson, C. H. & Chapman, C. A. in Primate Communities (eds Fleagle, J. G., Janson, C. H. & Reed, K. ) 237–267 (Cambridge Univ. Press, 1999).

    Google Scholar 

  78. 78

    Pettang, C. Decision Support for Construction Cost Control in Developing Countries (IGI Global, 2016).

    Google Scholar 

  79. 79

    Garamszegi, L. Z. & Møller, A. P. Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol. Rev. 85, 797–805 (2010).

    PubMed  Google Scholar 

  80. 80

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. 81

    Pagel, M. & Meade, A. BayesTraits V1 Manual (Univ. Reading, 2013).

    Google Scholar 

  82. 82

    Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).

    Google Scholar 

  83. 83

    Meade, A. & Pagel, M. BayesTraits V2 Manual (Univ. Reading, 2014).

    Google Scholar 

  84. 84

    Hadfield, J. D. MCMC methods for multiresponse generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  85. 85

    Healy, K. et al. Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. R. Soc. B. 281, 20140298 (2014).

    Article  PubMed  Google Scholar 

  86. 86

    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).

    Article  Google Scholar 

  87. 87

    Mönkkönen, M. & Martin, T. E. Sensitivity of comparative analyses to population variation in trait values: clutch size and cavity excavation tendencies. J. Avian Biol. 31, 576–579 (2000).

    Article  Google Scholar 

  88. 88

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 89

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  90. 90

    Jerison, H. J. Evolution of the Brain and Intelligence (Elsevier, 2012).

    Google Scholar 

  91. 91

    Ramdarshan, A. & Orliac, M. J. Endocranial morphology of Microchoerus erinaceus (Euprimates, Tarsiiformes) and early evolution of the Euprimates brain. Am. J. Phys. Anthropol. 159, 5–16 (2016).

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank M. Shattuck for help with data compilation, H. Kaplan for providing access to additional data, R. Raaum for statistical advice, and R. Peterson and M. Petersdorf for encouragement and feedback on previous versions of the manuscript. For training in phylogenetic comparative methods, J.P.H. thanks the AnthroTree Workshop, which is supported by the National Science Foundation (NSF; BCS-0923791) and the National Evolutionary Synthesis Center (NSF grant EF-0905606). This material is based on work supported by the NSF Graduate Research Fellowship (grant DGE1342536).

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A.R.D. designed the project and performed the analyses with input from J.P.H. and S.A.W. A.R.D. and S.A.W. collected the data. All three authors wrote the manuscript.

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Correspondence to Alex R. DeCasien.

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Supplementary Information

Supplementary Figures 1–3, Supplementary Tables 1–107, Supplementary Text, Supplementary References. (PDF 990 kb)

Supplementary Data 1

Full dataset on brain size, body size, diet, social/mating systems, group size and estimates of early Eocene fossil primate brain volumes, complied from published literature sources. (XLS 930 kb)

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DeCasien, A., Williams, S. & Higham, J. Primate brain size is predicted by diet but not sociality. Nat Ecol Evol 1, 0112 (2017). https://doi.org/10.1038/s41559-017-0112

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