The present study investigated whether increased relative brain size, including regional brain volumes, is related to differing behavioral specializations exhibited by three member species of the family Procyonidae. Procyonid species exhibit continuums of behaviors related to social and physical environmental complexities: the mostly solitary, semiarboreal and highly dexterous raccoons (Procyon lotor); the exclusively arboreal kinkajous (Potos flavus), which live either alone or in small polyandrous family groups, and the social, terrestrial coatimundi (Nasua nasua, N. narica). Computed tomographic (CT) scans of 45 adult skulls including 17 coatimundis (9 male, 8 female), 14 raccoons (7 male, 7 female), and 14 kinkajous (7 male, 7 female) were used to create three-dimensional virtual endocasts. Endocranial volume was positively correlated with two separate measures of body size: skull basal length (r = 0.78, p < 0.01) and basicranial axis length (r = 0.45, p = 0.002). However, relative brain size (total endocranial volume as a function of body size) varied by species depending on which body size measurement (skull basal length or basicranial axis length) was used. Comparisons of relative regional brain volumes revealed that the anterior cerebrum volume consisting mainly of frontal cortex and surface area was significantly larger in the social coatimundi compared to kinkajous and raccoons. The dexterous raccoon had the largest relative posterior cerebrum volume, which includes the somatosensory cortex, in comparison to the other procyonid species studied. The exclusively arboreal kinkajou had the largest relative cerebellum and brain stem volume in comparison to the semi arboreal raccoon and the terrestrial coatimundi. Finally, intraspecific comparisons failed to reveal any sex differences, except in the social coatimundi. Female coatimundis possessed a larger relative frontal cortical volume than males. Social life histories differ in male and female coatimundis but not in either kinkajous or raccoons. This difference may reflect the differing social life histories experienced by females who reside in their natal bands, and forage and engage in antipredator behavior as a group, while males disperse upon reaching adulthood and are usually solitary thereafter. This analysis in the three procyonid species supports the comparative neurology principle that behavioral specializations correspond to an expansion of neural tissue involved in that function.

Keywords:
Endocast, Coatimundi, Kinkajou, Raccoon, Computed tomography
1.
Adolphs R (2001): The neurobiology of social cognition. Curr Opin Neurobiol 11:231-239.
2.
Allen, TB (1987): Wild Animals of North America. Washington, National Geographic Society, pp 246-247.
3.
Amodio DM, Frith CD (2006): Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268-277.
4.
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.
5.
Arsznov BM, Sakai ST (2012): Pride diaries: sex, brain size and sociality in the African lion (Panthera leo) and cougar (Puma concolor). Brain Behav Evol 79:275-89.
6.
Baron GH, Stephan H, Frahm HD (1996): Comparative Neurobiology in Chiroptera. Basel, Birkhäuser.
7.
Barton (1998): Visual specialization and brain evolution in primates. Proc Biol Sci 265:1933-1937.
8.
Bekoff M, Daniels TJ, Gittleman JL (1984): Life history patterns and the comparative social ecology of carnivores. Annu Rev Ecol Syst 15:191-232.
9.
Brodmann K (1909): Localisation in the Cerebral Cortex (Garey LJ transl. 1999). London, Imperial College Press.
10.
Brutkowski S (1965): Functions of prefrontal cortex in animals. Physiol Rev 45:721-746.
11.
Budeau DA, Verts BJ (1986): Relative brain size and structural complexity of habitats of chipmunks. J Mammal 67:579-581.
12.
Byrne RW (1994): The evolution of intelligence; in Slater PJB, Halliday TR (eds): Behaviour and Evolution. Cambridge, Cambridge University Press, pp 223-265.
13.
Byrne R, Corp N (2004): Neocortex size predicts deception rate in primates. Proc Biol Sci 271:1693-1699.
14.
Byrne R, Whiten A (1988): Machiavellian Intelligence. Oxford, Clarendon.
15.
Changizi MA (2003): The Brain from 25,000 Feet: High Level Explorations of Brain Complexity, Perception, Induction and Vagueness. Dordrecht, Kluwer Academic.
16.
Clark DA, Mitra PP, Wang SS (2001): Scalable architecture in mammalian brains. Nature 10;411:189-193.
17.
Clutton-Brock T, Harvey P (1980): Primates, brains and behavior. J Zool (1987) 190:309-323.
18.
Dechmann DK, Safi K (2009): Comparative studies of brain evolution: a critical insight from the Chiroptera. Biol Rev 84:161-172.
19.
Dunbar R (1992): Neocortex size as a constraint on group size in primates. J Hum Evol 20:469-493.
20.
Dunbar RIM (1998): The social brain hypothesis. Evol Anthropol 6:178-190.
21.
Dunbar RIM (2003): Why are apes so smart? In Kappeler P, Pereira M (eds): Primate Life Histories and Socioecology. Chicago, Chicago University Press, pp 285-298.
22.
Dunbar RIM, Bever J (1998): Neocortex size predicts group size in carnivores and some insectivores. Ethology 104:695-708.
23.
Dunbar RIM, Shultz S (2007): Evolution in the social brain. Science 317:1344-1347.
24.
Eisenberg JF (1981): The Mammalian Radiations - An Analysis of Trends in Evolution, Adaptation, and Behavior. Chicago, University of Chicago Press.
25.
Eisenberg JF, Wilson DE (1978): Relative brain size and feeding strategies in the Chiroptera. Evolution 32:740-751.
26.
Finarelli JA (2006): Estimation of endocranial volume through the use of external skull measures in the Carnivora (Mammalia). J Mammal 87:1027-1036.
27.
Finarelli JA, Flynn JJ (2009): Brain-size evolution and sociality in Carnivora. Proc Natl Acad Sci USA 106:9345-9349.
28.
Gittleman JL (1986): Carnivore brain size, behavioral ecology, and phylogeny. J Mammal 67:23-36.
29.
Gompper ME (1995): Nasua narica. Mamm Species 487:1-10.
30.
Gompper ME (1996): Foraging costs and benefits of coati (Nasua narica) sociality and asociality. Behav Ecol 7:254-263.
31.
Gompper ME, Decker D (1998): Nasua nasua. Mamm Species 580:1-9.
32.
Gorska T (1974): Functional organization of cortical motor areas in adult dogs and puppies. Acta Neurobiol Exp (Wars) 34:171-203.
33.
Hager R, Lu L, Rosen GD, Williams RW (2012): Genetic architecture supports mosaic brain evolution and independent brain-body size regulation. Nat Commun 3:1079.
34.
Hardin Jr WB, Arumugasamy N, Jameson HD (1968): Pattern of localization in ‘precentral' motor cortex of raccoon. Brain Res 11:611-617.
35.
Hassler R, Muhs-Clement K (1964): Architectonic construction of the sensomotor and parietal cortex in the cat (in German). J Hirnforsch 20:377-420.
36.
Hauver SA, Gehrt SD, Prange S, Dubach J (2010): Behavioral and genetic aspects of the raccoon mating system. J Mammal 91:749-757.
37.
Hirsch BT (2011): Within-group spatial position in ring-tailed coatis: balancing predation, feeding competition, and social competition. Behav Ecol Sociobiol 65:391-399.
38.
Hirsch BT, Stanton MA, Maldonado JE (2012): Kinship shapes affiliative social networks but not aggression in ring-tailed coatis. PLoS One 7:e37301.
39.
Humphrey NK (1976): The social formation of intellect; in Bateson PPG, Hinde RA (eds): Growing Points in Ethology. Cambridge, Cambridge University Press, pp 303-317.
40.
Iwaniuk AN (2010): Comparative brain collections are an indispensable resource for evolutionary neurobiology. Brain Behav Evol 76:87-88.
41.
Iwaniuk AN, Pellis SM, Whishaw IQ (1999): Brain size is not correlated with forelimb dexterity in fissiped carnivores (Carnivora): a comparative test of the principle of proper mass. Brain Behav Evol 54:167-180.
42.
Janis C (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.
43.
Jerison H (1973): Evolution of the Brain and Intelligence. London, Academic Press.
44.
Jerison HJ (2007): What fossils tell us about the evolution of the neocortex; in Kaas JH, Krubizer LA (eds): Evolution of Nervous System. New York, Elsevier.
45.
Joffe TH, Dunbar RIM (1997): Visual and socio-cognitive information processing in primate brain evolution. Proc Biol Sci 264:1303-1307.
46.
Jolly A (1969): Lemur social behavior and primate intelligence. Science 153:501-506.
47.
Kaufmann JH (1962): Ecology and the social behavior of the coati, Nasua narica, on Barro Colorado Island, Panama. Univ Calif Publ Zool 60:95-222.
48.
Kaufmann JH (1982): Raccoon and allies; in Chapman JA, Feldhamer GA (eds): Wild Mammals of North America: Biology, Management, and Economics. Baltimore, The Johns Hopkins University Press, pp 567-585.
49.
Kawamura J (1971): Variations of the cerebral sulci in the cat. Acta Anat 80:204-221.
50.
Kays RW, Gittleman JL (1995): Home-range size and social behavior of kinkajous (Potosflavus) in the Republic of Panama. Biotropica 27:530-534.
51.
Kays RW, Gittleman J (2001): The social organization of the kinkajou Potos flavus (Procyonidae). J Zool (1987) 253:491-504.
52.
Lemen C (1980): Relationship between relative brain size and climbing ability in Peromyscus. J Mammal 61:360-364.
53.
Marino L (1996): What can dolphins tell us about primate evolution? Evol Anthropol 5:81-86.
54.
McClearn D (1992): Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. J Mammal 73:245-261.
55.
McComb JG, Withers GJ, Davis RL (1981): Cortical damage from Zenker's solution applied to the dura mater. Neurosurgery 8:68-71.
56.
Mishkin M (1964): Perseveration of central sets after frontal lesions in monkeys; in Warren J, Akert K (eds): The Frontal Granular Cortex and Behavior. New York, McGraw Hill, pp 219-241.
57.
Myasnikov AA, Dykes RW, Leclerc SS (1997): Correlating cytoarchitecture and function in cat primary somatosensory cortex: the challenge of individual differences. Brain Res 750:95-108.
58.
Packer C, Pusey A (1987): Intrasexual cooperation and the sex ratio in African lions. Am Nat 130:636-642.
59.
Parker ST, Gibson KR (1977): Object manipulation, tool use, and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J Hum Evol 6:623-641.
60.
Perez-Barberia FJ, Shultz S, Dunbar RIM (2007): Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evol 61:2811-2821.
61.
Powell J, Lewis PA, Dunbar RIM, García-Fiñana M, Roberts N (2010): Orbital prefrontal cortex volume correlates with social cognitive competence. Neuropsychologia 48:3554-3562.
62.
Pubols BH, Welker WI, Johnson JI (1965): Somatic sensory representation of fore-limb in dorsal root fibers of raccoon, coatimundi, and cat. J Neurophysiol 28:312-341.
63.
Radinsky L (1969): Outlines of canid and felid brain evolution. Ann NY Acad Sci 167:277-288.
64.
Radinsky L (1984): Basicranial axis length v. skull length in analysis of carnivore skull shape. Biol J Linn Soc Lond 22:31-41.
65.
Radinsky L (1985): Approaches in evolutionary morphology: a search for patterns. Ann Rev Ecol Syst 16:1-14.
66.
Reader S, Laland K (2002): Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci USA 99:4436-4441.
67.
Rilling JK, Insel TR (1998): Evolution of the cerebellum in primates: differences in relative volume among monkeys, apes and humans. Brain Behav Evol 52:308-314.
68.
Romero T, Aureli F (2007): Spatial association and social behaviour in zoo-living female ring-tailed coatis (Nasua nasua). Behaviour 144:179-193.
69.
Russell JK (1981): Exclusion of adult male coatis from social groups: protection from predation. J Mammal 62:206-208.
70.
Sakai ST (1982): The thalamic connectivity of the primary motor cortex (MI) in the raccoon. J Comp Neurol 204:238-252.
71.
Sakai ST (1990): Corticospinal projections from areas 4 and 6 in the raccoon. Exp Brain Res 79:240-248.
72.
Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011a): Brain size and social complexity: a computed tomography study in hyaenidae. Brain Behav Evol 77:91-104.
73.
Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011b): Virtual endocasts: an application of computed tomography in the study of brain variation among hyenas. Ann NY Acad Sci 1225(suppl 1):E160-E170.
74.
Sakai ST, Stanton GB, Isaacson LG (1993): Thalamic afferents of area 4 and 6 in the dog: a multiple retrograde fluorescent dye study. Anat Embryol (Berl) 188:551-559.
75.
Shultz S, Dunbar R (2006): Both social and ecological factors predict ungulate brain size. Proc Roy Soc Lond B 273:207-215.
76.
Smale L, Nunes S, Holekamp KE (1997): Sexually dimorphic dispersal in mammals: patterns, causes, and consequences; in Slater P, Rosenblatt J, Snowden C, Milinski M (eds): Advances in the Study of Behavior. San Diego, Academic Press, vol 26, pp 181-250.
77.
Stanton GB, Tanaka D, Jr., 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.
78.
Striedter GF (2005): Principles of brain evolution. Sunderland, Sinauer.
79.
Swanson EM, Holekamp KE, Lundrigan BL, Arsznov BM, Sakai ST (2012): Multiple determinants of whole and regional brain volume among terrestrial carnivorans. PLoS One 7:e38447.
80.
Tanaka D Jr (1987): Neostriatal projections from cytoarchitectonically defined gyri in the prefrontal cortex of the dog. J Comp Neurol 261:48-73.
81.
Van Valkenburgh B (1990): Skeletal and dental predictors of body mass in carnivores; in Damuth J, MacFadden B (eds): Body Size in Mammalian Paleobiology: Estimations and Biological Implications. Cambridge, Cambridge University Press, pp 181-206.
82.
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.
83.
Welker WI, Johnson JI (1965): Correlation between nuclear morphology and somatotopic organization in ventrobasal complex of the raccoon's thalamus. J Anat 99:761-790.
84.
Welker WI, Seidenstein S (1959): Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469-501.
85.
Whishaw IQ, Sarna JR, Pellis SM (1998): Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res 96:79-91.
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