EVIDENCE FOR COEVOLUTION OF SOCIALITY AND RELATIVE BRAIN SIZE IN THREE ORDERS OF MAMMALS
Abstract
As the brain is responsible for managing an individual's behavioral response to its environment, we should expect that large relative brain size is an evolutionary response to cognitively challenging behaviors. The "social brain hypothesis" argues that maintaining group cohesion is cognitively demanding as individuals living in groups need to be able to resolve conflicts that impact on their ability to meet resource requirements. If sociality does impose cognitive demands, we expect changes in relative brain size and sociality to be coupled over evolutionary time. In this study, we analyze data on sociality and relative brain size for 206 species of ungulates, carnivores, and primates and provide, for the first time, evidence that changes in sociality and relative brain size are closely correlated over evolutionary time for all three mammalian orders. This suggests a process of coevolution and provides support for the social brain theory. However, differences between taxonomic orders in the stability of the transition between small-brained/nonsocial and large-brained/social imply that, although sociality is cognitively demanding, sociality and relative brain size can become decoupled in some cases. Carnivores seem to have been especially prone to this.
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According to the social brain hypothesis, the high degree of encephalization reached by the neocortex of social mammals, especially Homo sapiens, may be a direct consequence of the cognitive demands required for the stable management of complex relationships within social groups.
“the high degree of encephalization reached by the neocortex of social mammals, especially by Homo sapiens, may be a direct consequence of the cognitive demands required for the stable management of complex relationships that occur within social groups”
From Internet use and access, behavior, cyberbullying, and grooming: Results of an investigative whole city survey of adolescents (2017) · cites this paper as [40]
Dunbar has identified an approximate number of 150 friends or social relationships that the individual human subject is actually able to maintain.
“Dunbar has come to identify an approximate number of 150 friends or social relationships that the individual human subject is actually able to maintain”
From Internet use and access, behavior, cyberbullying, and grooming: Results of an investigative whole city survey of adolescents (2017) · cites this paper as [40]
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BackgroundSocial Information Transmission in Animals: Lessons from Studies of Diffusion
Duboscq, J., Romano, V., MacIntosh, A. J. J., & Sueur, C. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01147 · Cited by 72 · see citing works
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Multiple Determinants of Whole and Regional Brain Volume among Terrestrial Carnivorans
Swanson, E. M., Holekamp, K. E., Lundrigan, B. L., Arsznov, B. M., & Sakai, S. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038447 · Cited by 68 · see citing works
“[17,18,53]).”
Brain Size and Social Complexity: A Computed Tomography Study in Hyaenidae
Sakai, S. T., Arsznov, B. M., Lundrigan, B. L., & Holekamp, K. E. (2011) · Brain Behavior and Evolution · doi:10.1159/000323849 · Cited by 66 · see citing works
“Researchers have reported a relationship between total brain volume and social complexity in carnivores and insectivores [Dunbar and Bever, 1998; Pérez-Barberia et al., 2007], ungulates [Shultz and Dunbar, 2006; Pérez-Barberia et al., 2007], odontocete cetaceans [Marino, 1996], and primates…”
BackgroundHabits of the heart: Life history and the developmental neuroendocrinology of emotion
Worthman, C. M. (2009) · American Journal of Human Biology · doi:10.1002/ajhb.20966 · Cited by 65 · see citing works
“Indeed, these pressures alone have been proposed as prime movers for evolution of expanded cranial capacity (Perez-Barberia et al. 2007), and as determinants of social network configurations and sustainable group sizes in humans (Dunbar 2008).”
BackgroundThe comparative approach and brain–behaviour relationships: A tool for understanding tool use.
Iwaniuk, A. N., Lefebvre, L., & WYLIE, D. R. W. (2009) · Canadian Journal of Experimental Psychology/Revue canadienne de psychologie expérimentale · doi:10.1037/a0015678 · Cited by 63 · see citing works
Comparative studies of brain evolution: a critical insight from the Chiroptera
Dechmann, D. K. N., & Safi, K. (2009) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2008.00067.x · Cited by 63 · see citing works
Whiten, A. (2018) · Journal of comparative psychology · doi:10.1037/com0000135 · Cited by 62 · see citing works
Integrating brain, behavior, and phylogeny to understand the evolution of sensory systems in birds
WYLIE, D. R. W., Gutiérrez‐Ibáñez, C., & Iwaniuk, A. N. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00281 · Cited by 60 · see citing works
Social carnivores outperform asocial carnivores on an innovative problem
Borrego, N., & Gaines, M. S. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.013 · Cited by 60 · see citing works
Brain size as a driver of avian escape strategy
Samia, D. S. M., Møller, A. P., & Blumstein, D. T. (2015) · Scientific Reports · doi:10.1038/srep11913 · Cited by 58 · see citing works
Lombard, M., & Högberg, A. (2021) · Journal of Archaeological Method and Theory · doi:10.1007/s10816-020-09502-6 · Cited by 57 · see citing works
“Whereas an increase in brain size probably played a role in early hominin evolution in terms of the social brain hypothesis (e.g. Dunbar 1998; Pérez-Barbería et al. 2007), amongst other things, it is clear from the data presented in the Galway-Witham et al. (2019) graph that by the MSA/MP, this…”
BackgroundFluctuations in Evolutionary Integration Allow for Big Brains and Disparate Faces
Evans, K. M., Waltz, B. T., Tagliacollo., V. A., Sidlauskas, B. L., & Albert, J. S. (2017) · Scientific Reports · doi:10.1038/srep40431 · Cited by 58 · see citing works
Embracing covariation in brain evolution
Charvet, C. J., & Finlay, B. L. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00004-0 · Cited by 55 · see citing works
“In a series of studies beginning in the early 1990s, Dunbar and his colleagues showed that the relative size of the isocortex or brain size and residuals derived from a linear regression of brain and body size positively correlate with group size or related measures of group size in primates (Dunbar, 1992, 2009; Dunba…”
InfluentialSociality does not drive the evolution of large brains in eusocial African mole-rats
Kverková, K., Bělíková, T., Olkowicz, S., Pavelková, Z., O'Riain, M., Šumbera, R., Burda, H., Bennett, N., & Němec, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-26062-8 · Cited by 51 · see citing works
Bite force and encephalization in the C anidae ( M ammalia: C arnivora)
Damasceno, E. M., Hingst‐Zaher, E., & Astúa, D. (2013) · Journal of Zoology · doi:10.1111/jzo.12030 · Cited by 54 · see citing works
Finlay, B. L., Hinz, F. I., & Darlington, R. B. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0344 · Cited by 54 · see citing works
Lombard, M. (2021) · Quaternary Science Reviews · doi:10.1016/j.quascirev.2021.107021 · Cited by 54 · see citing works
Markov, A. V., & Markov, M. A. (2020) · Ecology and Evolution · doi:10.1002/ece3.6350 · Cited by 50 · see citing works
Evolutionary dynamics of recent selection on cognitive abilities
Miller, S., Legan, A. W., Henshaw, M. T., Ostevik, K. L., Samuk, K., Uy, F. M. K., Reeve, H. K., & Sheehan, M. J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918592117 · Cited by 50 · see citing works
Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks
Samuk, K., Iritani, D., & Schluter, D. (2014) · Ecology and Evolution · doi:10.1002/ece3.1175 · Cited by 48 · see citing works
Collective personalities: present knowledge and new frontiers
Wright, C. M., Lichtenstein, J. L. L., Doering, G. N., Pretorius, J., Meunier, J., & Pruitt, J. N. (2019) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-019-2639-2 · Cited by 46 · see citing works
Linking ecology and cognition: does ecological specialisation predict cognitive test performance?
der Malsburg, J. H., Kappeler, P. M., & Fichtel, C. (2020) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-020-02923-z · Cited by 48 · see citing works
Both Diet and Sociality Affect Primate Brain-Size Evolution
Grabowski, M. W., Kopperud, B. T., Tsuboi, M., & Hansen, T. F. (2022) · Systematic Biology · doi:10.1093/sysbio/syac075 · Cited by 44 · see citing works
Big Cat Coalitions: A Comparative Analysis of Regional Brain Volumes in Felidae
Sakai, S. T., Arsznov, B. M., Hristova, A. E., Yoon, E. J., & Lundrigan, B. L. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00099 · Cited by 49 · see citing works
“…for the social brain hypothesis was provided by three subsequent studies which found positive correlations between sociality in carnivores and relative brain size (Perez-Barberia et al., 2007), relative cerebrum volume (Swanson et al., 2012), and relative neocortex size (Dunbar and Bever, 1998).”
BackgroundA framework for conceptualizing dimensions of social organization in mammals
Prox, L., & Farine, D. R. (2019) · Ecology and Evolution · doi:10.1002/ece3.5936 · Cited by 43 · see citing works
The lemur baseline: how lemurs compare to monkeys and apes in the Primate Cognition Test Battery
Fichtel, C., Dinter, K., & Kappeler, P. M. (2020) · PeerJ · doi:10.7717/peerj.10025 · Cited by 42 · see citing works
Vogt, C. C., Zipple, M. N., Sprockett, D. D., Miller, C. H., Hardy, S. X., Arthur, M. K., Greenstein, A. M., Colvin, M. S., Michel, L. M., Moeller, A. H., et al. (2024) · BMC Biology · doi:10.1186/s12915-024-01809-0 · Cited by 39 · see citing works
“The organization of mammal societies is influenced by ecological [100–102], demographic [103– 106], and phylogenetic factors [107–109], each of which were controlled for in our trials.”
BackgroundEcological Determinants of Social Systems
Chaverri, G., & Kunz, T. (2010) · Advances in the study of behavior · doi:10.1016/s0065-3454(10)42009-4 · Cited by 40 · see citing works
The Infertility Trap: The Fertility Costs of Group-Living in Mammalian Social Evolution
Dunbar, R., & Shultz, S. (2021) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2021.634664 · Cited by 41 · see citing works
Self-citationReser, J. E. (2011) · Evolutionary Psychology · doi:10.1177/147470491100900209 · Cited by 41 · see citing works
“It is clear that there are costs and benefits to living in groups and that the pressures from the social environment can change abruptly (Perez-Barberia, Shultz, and Dunbar, 2007).”
BackgroundBrain size, ecology and sociality: a reptilian perspective
Meester, G. D., Huyghe, K., & Damme, R. V. (2018) · Biological Journal of the Linnean Society · doi:10.1093/biolinnean/bly206 · Cited by 39 · see citing works
Levels and mechanisms of behavioural variability
Kappeler, P. M., & Kraus, C. (2010) · Springer eBooks · doi:10.1007/978-3-642-02624-9_21 · Cited by 39 · see citing works
The social brain hypothesis – thirty years on
Dunbar, R. (2024) · Annals of Human Biology · doi:10.1080/03014460.2024.2359920 · Cited by 37 · see citing works
“…derivative of selection for specialised cognition required for group-living in primates, ungulates, carnivores, bats, cetaceans, and birds (Pérez-Barbería et al. 2007; Shultz and Dunbar 2007, 2010a, 2010b, 2022; Dunbar and Shultz 2017, 2021; Fox et al. 2017), (2) this relationship…”
Self-citationO’Donnell, S., Clifford, M. R., & Molina, Y. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017566108 · Cited by 37 · see citing works
Population densities predict forebrain size variation in the cleaner fish Labroides dimidiatus
Triki, Z., Levorato, E., McNeely, W., Marshall, N. J., & Bshary, R. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.2108 · Cited by 34 · see citing works
“Despite its initial success, the SBH is now viewed with more scepticism for two main reasons: on a more technical level, various studies found supporting evidence only if group size and neocortex ratio were replaced with other measures [19,31,63,78,88,89] thus introducing arbitrary factors in the analyses.”
The evolution of capture myopathy in hooved mammals: a model for human stress cardiomyopathy?
Blumstein, D. T., Buckner, J. C., Shah, S., Patel, S., Alfaro, M. E., & Natterson-Horowitz, B. (2015) · Evolution Medicine and Public Health · doi:10.1093/emph/eov015 · Cited by 36 · see citing works
“Indeed, more social species, including ungulates, may have larger brains [51].”
BackgroundAbsolute, not relative brain size correlates with sociality in ground squirrels
Matějů, J., Kratochvíl, L., Pavelková, Z., Řičánková, V. P., Vohralík, V., & Němec, P. (2016) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.2725 · Cited by 36 · see citing works
Why direct effects of predation complicate the social brain hypothesis
van der Bijl, W., & Kolm, N. (2016) · BioEssays · doi:10.1002/bies.201500166 · Cited by 36 · see citing works
“Some evidence for larger brains in social carnivores has been presented [10], but the observed link between brain size and sociality was later shown to stem from dogs alone ([18], but see [19]).”
BackgroundIlieş, I., Muscedere, M. L., & Traniello, J. F. A. (2015) · Brain Behavior and Evolution · doi:10.1159/000370100 · Cited by 35 · see citing works
“…Dunbar and Shultz, 2007; Eberhard and Wcislo, 2012; Farris and Roberts, 2005; GómezRobles et al., 2014; Herculano-Houzel, 2012; HerculanoHouzel et al., 2014; Kotrschal et al., 2013; Lefebvre and Sol, 2008; Muscedere et al., 2014; Pérez-Barbería et al., 2007; Reichert, 2009; Swanson et al., 2012].”
BackgroundBrain and Behaviour in Primate Evolution
Dunbar, R. (2009) · Springer eBooks · doi:10.1007/978-3-642-02725-3_15 · Cited by 33 · see citing works
Self-citationYamaguchi, N., Kitchener, A. C., Gilissen, E., & Macdonald, D. W. (2009) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2009.01249.x · Cited by 33 · see citing works
Attacked ravens flexibly adjust signalling behaviour according to audience composition
Szipl, G., Ringler, E., & Bugnyar, T. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0375 · Cited by 32 · see citing works
“Sociality is thought to have driven the evolution of cognitive abilities in primates [1–4] and other mammals (e.g. cetaceans [5], carnivores and ungulates [6]), and possibly also in birds like parrots and corvids [7] (but see [8,9] for an argument against this notion in hyenas).”
Individual memory and the emergence of cooperation
Moreira, J. A. G., Vukov, J., Sousa, C., Santos, F. C., d'Almeida, A. F., Santos, M. D., & Pacheco, J. M. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.10.030 · Cited by 31 · see citing works
“Indeed, N can vary between 2 and 30 in accord with average maximum population sizes described in several species of primates (Kudo & Dunbar 2001; Dunbar & Shultz 2007a, b; Pérez-Barbería et al. 2007; Shultz & Dunbar 2010).”
BackgroundDeCasien, A. R., González, N. T., Williams, S. A., & Shattuck, M. R. (2018) · Evolution · doi:10.1111/evo.13633 · Cited by 28 · see citing works
Why big brains? A comparison of models for both primate and carnivore brain size evolution
Chambers, H., Heldstab, S. A., & O’Hara, S. J. (2021) · PLoS ONE · doi:10.1371/journal.pone.0261185 · Cited by 33 · see citing works
“This became the method of choice when brain and body size were found to be tightly coupled allometrically across vertebrates; therefore, accounting for this allometric relationship became of great importance [35, 58].”
Four errors and a fallacy: pitfalls for the unwary in comparative brain analyses
Dunbar, R., & Shultz, S. (2023) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12953 · Cited by 28 · see citing works
Self-citationMorphometric Study of Phylogenetic and Ecologic Signals in Procyonid (Mammalia: Carnivora) Endocasts
Ahrens, H. E. (2014) · The Anatomical Record · doi:10.1002/ar.22996 · Cited by 30 · see citing works
Silk, J. B., & Kappeler, P. M. (2017) · Cambridge University Press eBooks · doi:10.1017/9781107338319.010 · Cited by 28 · see citing works
Hooper, R., Brett, B., & Thornton, A. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270771 · Cited by 28 · see citing works
Spatial learning and memory in African mole-rats: The role of sociality and sex
Costanzo, M. S., Bennett, N. C., & Lutermann, H. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.09.008 · Cited by 28 · see citing works
“group size, [43–46]).”
Sociality and communicative complexity: insights from the other insect societies
Nehring, V., & Steiger, S. (2018) · Current Opinion in Insect Science · doi:10.1016/j.cois.2018.04.002 · Cited by 27 · see citing works
Muscedere, M. L., Gronenberg, W., Moreau, C. S., & Traniello, J. F. A. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0217 · Cited by 27 · see citing works
Morrison, R. E., Eckardt, W., Stoinski, T. S., & Brent, L. J. N. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.1026 · Cited by 26 · see citing works
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Fuentes-González, J. A., Housworth, E. A., Weber, A., & Martins, E. P. (2016) · The American Naturalist · doi:10.1086/688917 · Cited by 25 · see citing works
Page, R. A., von Merten, S., & Siemers, B. M. (2012) · Animal Cognition · doi:10.1007/s10071-012-0474-1 · Cited by 25 · see citing works
“Sociality has been connected with cognitive abilities in a variety of taxa (Pérez-Barbería et al. 2007).”
BackgroundLongevity in Bovids Is Promoted by Sociality, But Reduced by Sexual Selection
Bro‐Jørgensen, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045769 · Cited by 22 · see citing works
“and dilution benefits of group living, it is conceivable that the positive link between sociality and longevity is promoted also by a general link between large brain size and sociality [1], which has been reported specifically in ungulates [41,42].”
BackgroundA model for brain life history evolution
González-Forero, M., Faulwasser, T., & Lehmann, L. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005380 · Cited by 21 · see citing works
Individual Recognition and the Evolution of Learning and Memory in Polistes Paper Wasps
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Sayol, F., Collado, M. Á., Garcia‐Porta, J., Seid, M. A., Gibbs, J., Agorreta, A., Mauro, D. S., Raemakers, I., Sol, D., & Bartomeus, Í. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.0762 · Cited by 21 · see citing works
- Authors
- Pérez-Barbería, F. J., Shultz, S., & Dunbar, R. I. M.
- Affiliations
- University of Liverpool (GB)
- Corresponding author
- Pérez-Barbería, F. Javier
- Shultz, Susanne
- Dunbar, Robin I. M.
- Venue
- Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-12
- Volume
- 61
- Issue
- 12
- Pages
- 2811-2821
- ISSN
- 0014-3820 (ISSN-L)
- 1558-5646
- OpenAlex
- W2105254791
- Cited by
- 241
- References
- 58
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 14 · 2023: 8 · 2022: 10 · 2021: 27 · 2020: 12 · 2019: 9 · 2018: 16 · 2017: 17 · 2016: 15 · 2015: 11 · 2014: 8 · 2013: 12 · 2012: 18
- FWCI
- 16.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Evolution (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- British Academy
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- social brain hypothesis, sociality, relative brain size, coevolution, ungulates, carnivores, primates, group cohesion, cognitive demand, brain evolution, evolution of social behavior
- MeSH terms
- Animals, Behavior, Animal, Brain, Carnivora, Mammals, Organ Size, Phylogeny, Primates, Social Behavior
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