Brain Size and Social Complexity: A Computed Tomography Study in HyaenidaeSakai S.T.a, b · Arsznov B.M.a · Lundrigan B.L.c, d · Holekamp K.E.c
aDepartment of Psychology, bNeuroscience Program, cDepartment of Zoology, and dMichigan State University Museum, Michigan State University, East Lansing, Mich., USA
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Article / Publication Details
The social brain hypothesis posits that the demands of living in complex social groups require increased neural processing, and that this underlies the expansion of brain areas involved in mediation of complex social behavior. However, much of the support for the social brain hypothesis is derived from comparative studies in primates. If large brains evolved as a result of selection pressures imposed by life within complex societies, as the social brain hypothesis predicts, then gregarious nonprimate species should possess large brains and exhibit comparable expansion of brain areas mediating social behavior. Our purpose here was to test a prediction of the social brain hypothesis – that increased brain size is related to social complexity – by examining species in the carnivore family Hyaenidae. Hyaenidae contains 4 extant species that span a spectrum of social complexity: the aardwolf (Proteles cristata) is solitary during the nonbreeding season, and forms monogamous pairs during the breeding season; the striped hyena (Hyaena hyaena) lives solitarily or in small groups; the brown hyena (Parahyaena brunnea) lives in groups of up to 14 individuals; and the spotted hyena (Crocuta crocuta) lives in complex hierarchically organized groups containing up to 90 animals. Computed tomography was used to create three-dimensional endocasts based on serial analysis of coronal sections of the adult endocranium. The largest brain volume, relative to body size, is found in the spotted hyena. We found no significant variation in relative brain volume among striped hyenas, brown hyenas, and aardwolves. The spotted hyena also possesses a larger anterior cerebrum volume relative to total brain volume than is found in the other hyena species; this region is composed primarily of frontal cortex. These data are consistent with the idea that expansion of the frontal cortex is driven by the demands of processing cognitive information associated with complex social lives, but other factors may drive the evolution of large brains in hyaenids.
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- Adolphs R (2001): The neurobiology of social cognition. Curr Opin Neurobiol 11:231–239.
- Amici F, Aureli F, Call J (2008): Fission-fusion dynamics, behavioral flexibility and inhibitory control in primates. Curr Biol 18:1415–1419.
- Amodio DM, Frith CD (2006): Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277.
- Arsznov BM, Lundrigan BL, Holekamp KE, Sakai ST (2010): Sex and the frontal cortex: a developmental CT study in the spotted hyena. Brain Behav Evol 76:185–197.
- Aureli F, Schafner CM, Boesch C, Bearder SK, Call J, Chapman CA, Conner R, Difiore A, Dunbar RIM, Henzi SP, Holekamp KE, Korstjens AH, Layton RH, Lee P, Leymann J, Manson JH, Ramos-Fernandez G, Strier KB, Van Schaik CP (2008): Fission-fusion dynamics: new research frameworks. Curr Anthropol 48:627–654.
Barton RA, Dunbar RIM (1997): Evolution of the social brain; in Whiten A, Byrne R (eds): Machiavellian Intelligence II. Cambridge, Cambridge University Press, pp 240–263.
- Brutkowski S (1965): Functions of prefrontal cortex in animals. Physiol Rev 45:721.
- Brutkowski S, Dabrowska J (1963): Disinhibition after prefrontal lesions as a function of duration of intertrial intervals. Science 139:505–506.
- Bush EC, Allman JM (2004): The scaling of frontal cortex in primates and carnivores. Proc Natl Acad Sci USA 101:3962–3966.
Byrne RW (1994): The evolution of intelligence; in Slater PJB, Halliday TR (eds): Behaviour and Evolution. Cambridge, Cambridge University Press, pp 223–265.
Byrne RW, Whiten A (1988): Machiavellian Intelligence. Oxford, Clarendon Press.
Cheney DL, Seyfarth RM (1990): How Monkeys See the World. Chicago, University of Chicago Press.
- Dunbar RIM (1995): Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28:287–296.
- Dunbar RIM (1998): The social brain hypothesis. Evol Anthrop 6:178–190.
- Dunbar RIM (2003): The social brain: mind, language, and society in evolutionary perspective. Annu Rev Anthropol 32:163–181.
- Dunbar RIM, Bever J (1998): Neocortex size predicts group size in carnivores and some insectivores. Ethology 104:695–708.
- Dunbar RIM, Shultz S (2007): Evolution in the social brain. Science 317:1344–1347.
- Finarelli JA, Flynn JJ (2009): Brain-size evolution and sociality in Carnivora. Proc Natl Acad Sci USA 106:345–349.
- Ghosh S (1997): Cytoarchitecture of sensorimotor areas in the cat cerebral cortex. J Comp Neurol 388:354–370.
- Gittleman JL (1986): Carnivore brain size, behavioral ecology, and phylogeny. J Mamm 67:23–36.
- Gorska T (1974): Functional organization of cortical motor areas in adult dogs and puppies. Acta Neurobiol Exp 34:171–203.
Harcourt AH, de Waal FBM (1992): Coalitions and Alliances in Humans and Other Animals. Oxford, Oxford Science Publications.
- Hardin WB Jr, Arumugasamy N, Jameson HD (1968): Pattern of localization in ‘precentral’ motor cortex of raccoon. Brain Res 11:611–617.
Holekamp KE, Kolowski JM (2009): Hyaenidae; in Wilson D, Mittermeier R, Fonseca G (eds): Handbook of Mammals of the World. Madrid, Lynx Edicions, pp 234–260.
- Holekamp KE, Sakai ST, Lundrigan BL (2007): Social intelligence in the spotted hyena. Phil Trans R Soc B 362:523–538.
Holloway RL, Broadfield DC, Yuan MS (2004): The Human Fossil Record; in Brain Endocasts – The Paleoneurological Evidence. New York, Wiley, vol 3.
Humphrey NK (1976): The social function of intellect; in Bateson PPG, Hinde RA (eds): Growing Points in Ethology. Cambridge, Cambridge University Press, pp 303–317.
- Isler K, Kirk EC, Miller JMA, Albrecht GA, Gelvin BR, Martin RD (2008): Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J Human Evol 55:967–978.
Janis CM (1990): Correlation of cranial and dental variables with body size in ungulates and macropodoids; in Damuth J, MacFadden BJ (eds): Body Size in Mammalian Paleobiology, Estimations and Biological Implications. Cambridge, Cambridge University Press, pp 255–300.
Jerison HJ (1973): Evolution of the Brain and Intelligence. London, Academic Press.
Jerison HJ (2007): What fossils tell us about the evolution of the neocortex; in Kaas JH, Krubitzer LA (eds): Evolution of Nervous System. New York, Elsevier.
- Jolly A (1966): Lemur social behavior and primate intelligence. Science 153:501–506.
Kamil AC (1987): A synthetic approach to the study of animal intelligence. Nebr Symp Motiv 7:257–308.
- Koepfli KP, Jenks SM, Eizirik E, Zahirpour T, Van Valkenburgh B, Wayne RK (2006): Molecular systematics of the Hyaenidae: relationships of a relictual lineage resolved by a molecular supermatrix. Mol Phylogenet Evol 38:603–620.
Kruuk H (1972): The Spotted Hyena: A Study of Predation and Social Behavior. Chicago, University of Chicago Press.
- Kubo D, Kono RT, Saso, A, Mizushima S, Suwa G (2008): Accuracy and precision of CT-based endocranial capacity estimations: a comparison with the conventional millet seed method and application to the Minatogawa 1 skull. Anthropol Sci 11:77–85.
- Kudo H, Dunbar RIM (2001): Neocortex size and social network size in primates. Anim Behav 62:711–722.
- Lewis K (2001): A comparative study of primate play behaviour: implications for the study of cognition. Folia Primatol 71:417–421.
- Lyras GA, Van der Geer AAE (2003): External brain anatomy in relation to the phylogeny of Caninae (Carnivora: Canidae). Zoo J Linn Soc 138:505–522.
- Macrini TE, Rowe T, Vandeberg JL (2007): Cranial endocasts from a growth series of Monodelphis domestica (Didelphidae, Marsupialia): a study of individual and ontogenetic variation. J Morphol 268:844.
- Marino L (1996): What can dolphins tell us about primate evolution? Evol Anthrop 5:81–85.
- Mills MGL (1983): Behavioural mechanisms in territory and group maintenance of the brown hyenas, Hyaena brunnea, in the southern Kalahari. Anim Behav 31:503–510.
- Murray EA, O’Doherty JP, Schoenbaum G (2007): What we know and do not know about the functions of the orbitofrontal cortex after 20 years of cross-species studies. J Neurosci 27:8166–8169.
- Perez-Barberia FJ, Shultz S, Dunbar RIM (2007): Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61:2811–2821.
- Petrides M (2005): Lateral prefrontal cortex: architectonics and functional organization. Philos Trans R Soc Lond B 360:781–795.
- Preuss T (1995): Do rats have prefrontal cortex? The Rose-Woolsey-Akert program revisited. J Cogn Neurosci 7:1–24.
Preuss T (2007): Primate brain evolution in phylogenetic context; in Kaas JH, Preuss TM (eds): Evolution of Nervous Systems. A Comprehensive Reference, vol 4: Primates. Amsterdam, Elsevier, pp 1–35.
- Radinsky LB (1969): Outlines of canid and felid brain evolution. Ann NY Acad Sci 167:277–288.
- Radinsky LB (1973): Evolution of the canid brain. Brain Behav Evol 7:169–202.
- Radinsky LB (1975): Evolution of the felid brain. Brain Behav Evol 11:214–254.
Richardson PRK, Coetzee M (1988): Mate desertion in response to female promiscuity in the socially monogamous aardwolf. S Afr J Zool 23:306–308.
- Sakai ST (1982): The thalamic connectivity of the primary motor cortex (MI) in the raccoon. J Comp Neurol 204:238–252.
- Schoenbaum G, Setlow B (2001): Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions. Learn Mem 8:134–147.
- Shultz S, Dunbar RIM (2006): Both social and ecological factors predict brain size in ungulates. Proc R Soc Lond B 273:207–215.
- Shultz S, Dunbar RIM (2007): The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc R Soc Lond B 274:2429–2436.
- Smith JE, Kolowski JM, Graham KE, Dawes SE, Holekamp KE (2008): Social and ecological determinants of fission-fusion dynamics in the spotted hyaena. Anim Behav 76:619–636.
- Springer MS, Murphy WJ, Eizirik E, O’Brien S (2003): Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc Natl Acad Sci USA 100:1056–1061.
Springer MS, Murphy WJ, Eizirik E, O’Brien S (2005): Molecular evidence for major placental clades; in Rose KD and Archibald JD (eds): The Rise of Placental Mammals. Baltimore, The Johns Hopkins University Press, pp 37–49.
- Stanton GB, Tanaka D, Sakai ST, Weeks OI (1986): Thalamic afferents to cytoarchitectonic subdivisions of area 6 on the anterior sigmoid gyrus of the dog – a retrograde and anterograde tracing study. J Comp Neurol 252:446–467.
- Stephan H, Frahm H, Baron G (1981): New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol 35:1–29.
- Tanaka D Jr, Gorska T, Dutkiewicz (1981): Corticostriate projections from the primary motor cortex in the dog. Brain Res 209:287–303.
Van Valkenburgh BV (1990): Skeletal and dental predictors of body mass in carnivores; in Damuth J, MacFadden BJ (eds): Body Size in Mammalian Paleobiology, Estimations and Biological Implications. Cambridge, Cambridge University Press, pp 181–206.
- Wagner AP, Frank LG, Creel S (2008): Spatial grouping in behaviourally solitary striped hyaenas, Hyaena hyaena. Anim Behav 75:1131–1142.
- Watts HE, Holekamp KE (2007): Hyena societies. Curr Biol 17:R657–R660.
- Welker WI, Campos GB (1963): Physiological significance of sulci in somatic sensory cerebral cortex in mammals of the family Procyonidae. J Comp Neurol 120:19–36.
- Welker WI, Seidenstein S (1959): Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469–501.
Werdelin L, Solounias N (1991): The Hyaenidae: taxonomy, systematics and evolution. Fossils Strata 30:1–104.
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