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The social and cultural roots of whale and dolphin brains

An Author Correction to this article was published on 05 December 2017

This article has been updated

Abstract

Encephalization, or brain expansion, underpins humans’ sophisticated social cognition, including language, joint attention, shared goals, teaching, consensus decision-making and empathy. These abilities promote and stabilize cooperative social interactions, and have allowed us to create a ‘cognitive’ or ‘cultural’ niche and colonize almost every terrestrial ecosystem. Cetaceans (whales and dolphins) also have exceptionally large and anatomically sophisticated brains. Here, by evaluating a comprehensive database of brain size, social structures and cultural behaviours across cetacean species, we ask whether cetacean brains are similarly associated with a marine cultural niche. We show that cetacean encephalization is predicted by both social structure and by a quadratic relationship with group size. Moreover, brain size predicts the breadth of social and cultural behaviours, as well as ecological factors (diversity of prey types and to a lesser extent latitudinal range). The apparent coevolution of brains, social structure and behavioural richness of marine mammals provides a unique and striking parallel to the large brains and hyper-sociality of humans and other primates. Our results suggest that cetacean social cognition might similarly have arisen to provide the capacity to learn and use a diverse set of behavioural strategies in response to the challenges of social living.

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Fig. 1: Distribution of residual brain size and social repertoire scores.
Fig. 2: Mid-sized social groups are associated with larger brain size and higher social repertoire scores.
Fig. 3: Model of likely relationships between brain size, behaviour and ecology in cetaceans. Paths were determined via a model selection approach using AIC.

Change history

  • 05 December 2017

    In Table 1 of the Supplementary Information, the data presented in the column ‘Corrected social repertoire’ were incorrect. This error does not affect the analyses, statistics or conclusions of the study, which employed the correct values. The data have now been corrected in the Supplementary file.

References

  1. 1.

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

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

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

    Article  Google Scholar 

  3. 3.

    Pinker, S. The cognitive niche: coevolution of intelligence, sociality, and language. Proc. Natl Acad. Sci. USA 107, 8993–8999 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Boyd, R., Richerson, P. J. & Henrich, J. The cultural niche: why social learning is essential for human adaptation. Proc. Natl Acad. Sci. USA 108, 10918–10925 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Marino, L. et al. Cetaceans have complex brains for complex cognition. PLoS Biol. 5, e139 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Whitehead, H. & Rendell, L. The Cultural Lives of Whales and Dolphins (Univ. Chicago Press, Chicago, 2014).

  7. 7.

    Connor, R. C. Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Phil. Trans. R. Soc. Lond. B 362, 587–602 (2007).

    Article  Google Scholar 

  8. 8.

    Allen, J., Weinrich, M., Hoppitt, W. & Rendell, L. Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science 340, 485–488 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Jurasz, C. & Jurasz, V. Feeding modes of the humpback whale, Megaptera novaeangliae, in southeast Alaska. Scientific Reports of the Whales Research Institute (1979).

  10. 10.

    Ford, J. K. Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can. J. Zool. 69, 1454–1483 (1991).

    Article  Google Scholar 

  11. 11.

    Ridgway, S., Carder, D., Jeffries, M. & Todd, M. Spontaneous human speech mimicry by a cetacean. Curr. Biol. 22, R860–R861 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Janik, V. M. & Slater, P. J. The different roles of social learning in vocal communication. Anim. Behav. 60, 1–11 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Pryor, K. & Lindbergh, J. A dolphin–human fishing cooperative in Brazil. Mar. Mamm. Sci. 6, 77–82 (1990).

    Article  Google Scholar 

  14. 14.

    Zaeschmar, J. R., Dwyer, S. L. & Stockin, K. A. Rare observations of false killer whales (Pseudorca crassidens) cooperatively feeding with common bottlenose dolphins (Tursiops truncatus) in the Hauraki Gulf, New Zealand. Mar. Mamm. Sci. 29, 555–562 (2013).

    Article  Google Scholar 

  15. 15.

    Leung, E. S., Vergara, V. & Barrett‐Lennard, L. G. Allonursing in captive belugas (Delphinapterus leucas). Zoo Biol. 29, 633–637 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Guinet, C. Intentional stranding apprenticeship and social play in killer whales (Orcinus orca). Can. J. Zool. 69, 2712–2716 (1991).

    Article  Google Scholar 

  17. 17.

    Lefebvre, L., Reader, S. M. & Sol, D. Brains, innovations and evolution in birds and primates. Brain Behav. Evol. 63, 233–246 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Lefebvre, L. Brains, innovations, tools and cultural transmission in birds, non-human primates, and fossil hominins. Front. Hum. Neurosci. 7, 245 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Nicolakakis, N. & Lefebvre, L. Forebrain size and innovation rate in European birds: feeding, nesting and confounding variables. Behaviour 137, 1415–1429 (2000).

    Article  Google Scholar 

  20. 20.

    Timmermans, S., Lefebvre, L., Boire, D. & Basu, P. Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav. Evol. 56, 196–203 (2000).

    Article  CAS  Google Scholar 

  21. 21.

    Sol, D., Timmermans, S. & Lefebvre, L. Behavioural flexibility and invasion success in birds. Anim. Behav. 63, 495–502 (2002).

    Article  Google Scholar 

  22. 22.

    Navarrete, A. F., Reader, S. M., Street, S. E., Whalen, A. & Laland, K. N. The coevolution of innovation and technical intelligence in primates. Phil. Trans. R. Soc. B  371, 20150186 (2016).

    Article  Google Scholar 

  23. 23.

    Reader, S. M., Hager, Y. & Laland, K. N. The evolution of primate general and cultural intelligence. Phil. Trans. R. Soc. B 366, 1017–1027 (2011).

    Article  Google Scholar 

  24. 24.

    Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2002).

    Article  CAS  Google Scholar 

  25. 25.

    Reader, S. M. & MacDonald, K. in Animal Innovation (eds Reader, S. M. & Laland, K. N.) (Oxford Univ. Press, Oxford, 2003).

  26. 26.

    Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. nlme: linear and nonlinear mixed effects models. R package v.3.1-117 http://CRAN.R-project.org/package=nlme (R Core Team, 2014).

  27. 27.

    Mazerolle, M. J. AICcmodavg: model selection and multimodel inference based on (Q) AIC (c). R package version 1, 35 (2013).

  28. 28.

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

    Article  CAS  Google Scholar 

  29. 29.

    Montgomery, S. H. et al. The evolutionary history of cetacean brain and body size. Evolution 67, 3339–3353 (2013).

    Article  Google Scholar 

  30. 30.

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

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

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

    Article  Google Scholar 

  32. 32.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    DeCasien, A. R., Williams, S. A. & Higham, J. P. Primate brain size is predicted by diet but not sociality. Nat. Ecol. Evol. 1, 0112 (2017).

    Article  Google Scholar 

  34. 34.

    Marino, L., McShea, D. W. & Uhen, M. D. Origin and evolution of large brains in toothed whales. Anat. Rec. 281, 1247–1255 (2004).

    Article  Google Scholar 

  35. 35.

    Marino, L. et al. Endocranial volume of mid-late Eocene archaeocetes (Order: Cetacea) revealed by computed tomography: implications for cetacean brain evolution. J. Mamm. Evol. 7, 81–94 (2000).

    Article  Google Scholar 

  36. 36.

    Dunbar, R. I. M. & Shultz, S. Why are there so many explanations for primate brain evolution? Phil. Trans. R. Soc. B 372, 2016–0244 (2017).

  37. 37.

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

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

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

    Article  Google Scholar 

  39. 39.

    Dunbar, R. I. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Dunbar, R. I. Neocortex size and group size in primates: a test of the hypothesis. J. Hum. Evol. 28, 287–296 (1995).

    Article  Google Scholar 

  41. 41.

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

    Article  Google Scholar 

  42. 42.

    Muthukrishna, M. & Henrich, J. Innovation in the collective brain. Phil. Trans. R. Soc. Lond. B 371, 20150192 (2016).

  43. 43.

    Marino, L. What can dolphins tell us about primate evolution? Evol. Anthropol. I 5, 81–86 (1996).

    Article  Google Scholar 

  44. 44.

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

    Article  Google Scholar 

  45. 45.

    May-Collado, L. J., Agnarsson, I. & Wartzok, D. Phylogenetic review of tonal sound production in whales in relation to sociality. BMC Evol. Biol. 7, 136 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Ridgway, S. H. in The Bottlenose Dolphin (eds Leatherwood, S. & Reeves, R. R.) 69–97 (Academic Press, San Diego, 1990).

  47. 47.

    Freeberg, T. M., Dunbar, R. I. M. & Ord, T. J. Social complexity as a proximate and ultimate factor in communicative complexity. Phil. Trans. R. Soc. Lond. B 367, 1785–1801 (2012).

    Article  Google Scholar 

  48. 48.

    Hof, P. R., Chanis, R. & Marino, L. Cortical complexity in cetacean brains. Anat. Rec. 287, 1142–1152 (2005).

    Article  Google Scholar 

  49. 49.

    Allman, J. M., Watson, K. K., Tetreault, N. A. & Hakeem, A. Y. Intuition and autism: a possible role for Von Economo neurons. Trends Cogn. Sci. 9, 367–373 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Kesarev, V. The inferior brain of the dolphin. Soviet Sci. Rev. 1, 52–58 (1971).

    Google Scholar 

  51. 51.

    Patzke, N. et al. In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct. Funct. 220, 361–383 (2015).

    Article  Google Scholar 

  52. 52.

    Butti, C. et al. The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Brain Struct. Funct. 220, 3339–3368 (2015).

    Article  Google Scholar 

  53. 53.

    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  Google Scholar 

  54. 54.

    Marino, L. et al. A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure. Biol. Rev. 83, 417–440 (2008).

    PubMed  Google Scholar 

  55. 55.

    Maximino, C. A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods. Mar. Freshwater Behav. Physiol. 42, 1–17 (2009).

    Article  Google Scholar 

  56. 56.

    Gygax, L. Evolution of group size in the superfamily Delphinoidea (Delphinidae, Phocoenidae and Monodontidae): a quantitative comparative analysis. Mamm. Rev. 32, 295–314 (2002).

    Article  Google Scholar 

  57. 57.

    Perrin, W. F. & Wursig, B. Encyclopedia of Marine Mammals (Academic Press, San Diego, 2009).

  58. 58.

    Nowak, R. M. Walker’s Marine Mammals of the World (Johns Hopkins Univ. Press, Baltimore, 2003).

  59. 59.

    Jefferson, T. A., Webber, M. A. & Pitman, R. L. Marine Mammals of the World: A Comprehensive Guide to Their Identification (Academic Press, San Diego, 2011).

  60. 60.

    Charrad, M., Ghazzali, N., Boiteau, V., Niknafs, A. & Charrad, M. M. Package ‘NbClust’. J. Stat. Softw. 61, 1–36 (2014).

    Article  Google Scholar 

  61. 61.

    Paulos, R. D., Trone, M., Kuczaj, I. & Stan, A. Play in wild and captive cetaceans. Int. J. Comp. Psychol. 23, 701–722 (2010).

  62. 62.

    Rendell, L. & Whitehead, H. Culture in whales and dolphins. Behav. Brain Sci. 24, 309–324 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

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

    Article  CAS  Google Scholar 

  64. 64.

    MacLean, E. L. et al. The evolution of self-control. Proc. Natl Acad. Sci. USA 111, E2140–E2148 (2014).

    Article  CAS  Google Scholar 

  65. 65.

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

    Google Scholar 

  66. 66.

    Kolenikov, S. & Angeles, G. Socioeconomic status measurement with discrete proxy variables: is principal component analysis a reliable answer? Rev. Income Wealth 55, 128–165 (2009).

    Article  Google Scholar 

  67. 67.

    Revelle, W. psych: Procedures for Personality and Psychological Research v.1.7.8  https://CRAN.R-project.org/package=psych (Northwestern University, Evanston, 2017).

  68. 68.

    Freckleton, R. P. On the misuse of residuals in ecology: regression of residuals vs. multiple regression. J. Anim. Ecol. 71, 542–545 (2002).

    Article  Google Scholar 

  69. 69.

    Jerison, H. Evolution of the Brain and Intelligence (Academic Press, San Diego, 1973).

  70. 70.

    Shipley, B. Cause and Correlation in Biology: A User’s Guide to Path Analysis, Structural Equations and Causal Inference with R (Cambridge Univ. Press, Cambridge, UK, 2016).

  71. 71.

    Hardenberg, Av & Gonzalez‐Voyer, A. Disentangling evolutionary cause–effect relationships with phylogenetic confirmatory path analysis. Evolution 67, 378–387 (2013).

    Article  Google Scholar 

  72. 72.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach (Springer Science & Business Media, New York, 2002).

  73. 73.

    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  PubMed  PubMed Central  Google Scholar 

  74. 74.

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

    Article  CAS  Google Scholar 

  75. 75.

    Pagel, M. 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  Google Scholar 

  76. 76.

    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 

  77. 77.

    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 

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Acknowledgements

We thank R. Sears of the Mingan Island Cetacean Study for early encouragement of this work. K.C.R.F. is supported by a postdoctoral fellowship from the Natural Sciences and Engineering Research Council of Canada; S.S. is supported by a Royal Society University Research Fellowship (UF110641).

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K.C.R.F., M.M. and S.S. conceived the project and wrote the manuscript. K.C.R.F. and M.M. collated the data, with some assistance from S.S. S.S. primarily conducted statistical analyses, with some assistance from M.M. and K.C.R.F.

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Correspondence to Susanne Shultz.

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Supplementary Information

Supplementary Figures 1–7; Supplementary Tables 3–8.

Supplementary Table 1

Main database of basic cetacean physical and social data.

Supplementary Table 2

Database of cetacean social and prosocial behaviour.

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Fox, K.C.R., Muthukrishna, M. & Shultz, S. The social and cultural roots of whale and dolphin brains. Nat Ecol Evol 1, 1699–1705 (2017). https://doi.org/10.1038/s41559-017-0336-y

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