Endocranial volume is variable and heritable, but not related to fitness, in a free-ranging primate
1.
Healy, S. D. & Rowe, C. A critique of comparative studies of brain size. Proc. R. Soc. B Biol. Sci. 274, 453–464 (2007).
Article Google Scholar
2.
Roth, G. & Dicke, U. Evolution of the brain and intelligence. Trends Cogn. Sci. 9, 250–257 (2005).
PubMed Article Google Scholar
3.
Logan, C. J., Kruuk, L. E. B., Stanley, R., Thompson, A. M. & Clutton-Brock, T. H. Endocranial volume is heritable and is associated with longevity and fitness in a wild mammal. R. Soc. Open Sci. 3, 160622 (2016).
ADS CAS PubMed PubMed Central Article Google Scholar
4.
Dunbar, R. I. M. Neocortex size as a constraint on group size in primates. J. Hum. Evol. 22, 469–493 (1992).
Article Google Scholar
5.
Innocenti, G. M. & Kaas, J. H. The cortex. Trends Neurosci. 18, 371–372 (1995).
CAS Article Google Scholar
6.
Kaas, J. H. The evolution of isocortex. Brain. Behav. Evol. 46, 187–196 (1995).
CAS PubMed Article Google Scholar
7.
Barton, R. A. & Harvey, P. H. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058 (2000).
ADS CAS PubMed Article Google Scholar
8.
Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl. Acad. Sci. 99, 4436–4441 (2002).
ADS CAS PubMed Article Google Scholar
9.
Sol, D., Székely, T., Liker, A. & Lefebvre, L. Big-brained birds survive better in nature. Proc. R. Soc. B Biol. Sci. 274, 763–769 (2007).
Article Google Scholar
10.
Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E. M. & Holekamp, K. E. Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl. Acad. Sci. USA 113, 2532–2537 (2016).
ADS CAS PubMed Article Google Scholar
11.
Cartmill, M. New views on primate origins. Evol. Anthropol. Issues News Rev. 1, 105–111 (2005).
Article Google Scholar
12.
Allman, J., McLaughlin, T. & Hakeem, A. Brain weight and life-span in primate species. Proc. Natl. Acad. Sci. 90, 118–122 (1993).
ADS CAS PubMed Article Google Scholar
13.
González-Lagos, C., Sol, D. & Reader, S. M. Large-brained mammals live longer. J. Evol. Biol. 23, 1064–1074 (2010).
PubMed Article Google Scholar
14.
Harvey, P. H. & Bennett, P. M. Evolutionary biology: Brain size, energetics, ecology and life history patterns. Nature 306, 314–315 (1983).
ADS CAS PubMed Article Google Scholar
15.
Aiello, L. C. & Wheeler, P. The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199–221 (1995).
Article Google Scholar
16.
Kudo, H. & Dunbar, R. I. M. Neocortex size and social network size in primates. Anim. Behav. 62, 711–722 (2001).
Article Google Scholar
17.
Schillaci, M. A. Sexual selection and the evolution of brain size in primates. PLoS ONE 1, e62 (2006).
ADS PubMed PubMed Central Article Google Scholar
18.
Shultz, S. & Dunbar, R. I. M. The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc. R. Soc. B Biol. Sci. 274, 2429–2436 (2007).
Article Google Scholar
19.
King, B. J. Extractive foraging and the evolution of primate intelligence. Hum. Evol. 1, 361–372 (1986).
Article Google Scholar
20.
Barton, R. A. Neocortex size and behavioural ecology in primates. Proc. R. Soc. Lond. B 263, 173–177 (1996).
ADS CAS Article Google Scholar
21.
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
22.
Powell, L. E., Isler, K. & Barton, R. A. Re-evaluating the link between brain size and behavioural ecology in primates. Proc. R. Soc. B Biol. Sci. 284, 20171765 (2017).
Article Google Scholar
23.
Dunbar, R. I. M. & Shultz, S. Why are there so many explanations for primate brain evolution?. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160244 (2017).
Article Google Scholar
24.
Van Schaik, C. P. Why are diurnal primates living in groups?. Behaviour 87, 120–144 (1983).
Article Google Scholar
25.
Van Schaik, C. P. & Van Hooff, J. A. R. A. M. On the ultimate causes of primate social systems. Behaviour 85, 91–117 (1983).
Article Google Scholar
26.
Wrangham, R. W. An ecological model of female-bonded primate groups. Behaviour 75, 262–300 (1980).
Article Google Scholar
27.
Atchley, W. R., Riska, B., Kohn, L. A. P., Plummer, A. A. & Rutledge, J. J. A quantitative genetic analysis of brain and body size associations, their origin and ontogeny: Data from mice. Evolution 38, 1165 (1984).
PubMed Article Google Scholar
28.
Riska, B. & Atchley, W. R. Genetics of growth predict patterns of brain-size evolution. Science 229, 668–671 (1985).
ADS CAS PubMed Article Google Scholar
29.
Rogers, J. et al. Heritability of brain volume, surface area and shape: An MRI study in an extended pedigree of baboons. Hum. Brain Mapp. 28, 576–583 (2007).
PubMed PubMed Central Article Google Scholar
30.
Gómez-Robles, A., Hopkins, W. D., Schapiro, S. J. & Sherwood, C. C. Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proc. Natl. Acad. Sci. 112, 14799–14804 (2015).
ADS PubMed Article CAS Google Scholar
31.
DeCasien, A. R., Sherwood, C. C., Schapiro, S. J. & Higham, J. P. Greater variability in chimpanzee (Pan troglodytes) brain structure among males. Proc. R. Soc. B 287, 20192858 (2020).
PubMed Article Google Scholar
32.
Fears, S. C. et al. Identifying heritable brain phenotypes in an extended pedigree of vervet monkeys. J. Neurosci. 29, 2867–2875 (2009).
CAS PubMed PubMed Central Article Google Scholar
33.
Noreikiene, K. et al. Quantitative genetic analysis of brain size variation in sticklebacks: Support for the mosaic model of brain evolution. Proc. R. Soc. B Biol. Sci. 282, 20151008 (2015).
Article Google Scholar
34.
Kotrschal, A. et al. Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23, 168–171 (2013).
CAS PubMed PubMed Central Article Google Scholar
35.
Cheverud, J. M. et al. Heritability of brain size and surface features in rhesus macaques (Macaca mulatta). J. Hered. 81, 51–57 (1990).
CAS PubMed Article Google Scholar
36.
de Villemereuil, P. Tutorial estimation of a biological trait heritability using the animal model How to use the MCMCglmm R package. (2012).
37.
Axelrod, C. J., Laberge, F. & Robinson, B. W. Intraspecific brain size variation between coexisting sunfish ecotypes. Proc. R. Soc. B Biol. Sci. 285, 20181971 (2018).
Article Google Scholar
38.
Blomquist, G. E. Fitness-related patterns of genetic variation in rhesus macaques. Genetica 135, 209–219 (2009).
PubMed Article Google Scholar
39.
Brent, L. J. N. et al. Personality traits in rhesus macaques (Macaca mulatta) are heritable but do not predict reproductive output. Int. J. Primatol. 35, 188–209 (2014).
PubMed Article Google Scholar
40.
Dubuc, C. et al. Sexually selected skin colour is heritable and related to fecundity in a non-human primate. Proc. R. Soc. B Biol. Sci. 281, 20141602 (2014).
Article Google Scholar
41.
Kimock, C. M., Dubuc, C., Brent, L. J. N. & Higham, J. P. Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate. Sci. Rep. 9, 19794 (2019).
ADS CAS PubMed PubMed Central Article Google Scholar
42.
Kruuk, L. E. B. Estimating genetic parameters in natural populations using the ‘animal model’. Philos. Trans. R. Soc. B 359, 873–890 (2004).
Article Google Scholar
43.
Falk, D., Froese, N., Sade, D. S. & Dudek, B. C. Sex differences in brain/body relationships of Rhesus monkeys and humans. J. Hum. Evol. 36, 233–238 (1999).
CAS PubMed Article Google Scholar
44.
Herndon, J. G., Tigges, J., Anderson, D. C., Klumpp, S. A. & McClure, H. M. Brain weight throughout the life span of the chimpanzee. J. Comp. Neurol. 409, 567–572 (1999).
CAS PubMed Article Google Scholar
45.
Iwaniuk, A. N. Interspecific variation in sexual dimorphism in brain size in Nearctic ground squirrels (Spermophilus spp.). Can. J. Zool. 79, 759–765 (2001).
Article Google Scholar
46.
Towe, A. L. & Mann, M. D. Habitat-related variations in brain and body size of pocket gophers. J. Hirnforsch. 36, 195–201 (1995).
CAS PubMed Google Scholar
47.
Kotrschal, A., Räsänen, K., Kristjánsson, B. K., Senn, M. & Kolm, N. Extreme sexual brain size dimorphism in sticklebacks: A consequence of the cognitive challenges of sex and parenting?. PLoS ONE 7, e30055 (2012).
ADS CAS PubMed PubMed Central Article Google Scholar
48.
Ritchie, S. J. et al. Sex differences in the adult human brain: Evidence from 5216 uk biobank participants. Cereb. Cortex 28, 2959–2975 (2018).
PubMed PubMed Central Article Google Scholar
49.
Whitten, P. L. Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am. J. Primatol. 5, 139–159 (1983).
PubMed Article Google Scholar
50.
Mori, A. Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20, 371–397 (1979).
Article Google Scholar
51.
Small, M. F. Body fat, rank, and nutritional status in a captive group of Rhesus Macaques. Int. J. Primatol. 2, 91–95 (1981).
Article Google Scholar
52.
Sade, D. S. Population dynamics in relation to social structure on Cayo Santiago. Ybk. Phys. Anthr. 20, 253–262 (1976).
Google Scholar
53.
Silk, J. B., Clark-Wheatley, C. B., Rodman, P. S. & Samuels, A. Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Anim. Behav. 29, 1106–1120 (1981).
Article Google Scholar
54.
Rawlins, R. G. & Kessler, M. J. The Cayo Santiago macaques: History, behavior, and biology (SUNY Series Primatology, Suny, 1986).
Google Scholar
55.
Kessler, M. J. & Rawlins, R. G. A 75-year pictorial history of the Cayo Santiago rhesus monkey colony. Am. J. Primatol. 78, 6–43 (2016).
PubMed Article Google Scholar
56.
Widdig, A. et al. Genetic studies on the Cayo Santiago rhesus macaques: A review of 40 years of research. Am. J. Primatol. 78, 44–62 (2016).
PubMed Article Google Scholar
57.
Widdig, A. et al. Low incidence of inbreeding in a long-lived primate population isolated for 75 years. Behav. Ecol. Sociobiol. 71, 18 (2017).
PubMed Article Google Scholar
58.
Cheverud, J. M. Epiphyseal union and dental eruption in Macaca mulatta. Am. J. Phys. Anthropol. 56, 157–167 (1981).
CAS PubMed Article Google Scholar
59.
Turnquist, J. E. & Kessler, M. J. Free-ranging Cayo Santiago rhesus monkeys (Macaca mulatta): I. Body size, proportion, and allometry. Am. J. Primatol. 19, 1–13 (1989).
PubMed Article Google Scholar
60.
Havill, L. M. Osteon remodeling dynamics in macaca mulatta: Normal variation with regard to age, sex, and skeletal maturity. Calcif. Tissue Int. 74, 95–102 (2004).
CAS PubMed Article Google Scholar
61.
Konigsberg, L. et al. External brain morphology in rhesus macaques (Macaca mulatta). J. Hum. Evol. 19, 269–284 (1990).
Article Google Scholar
62.
Logan, C. J. & Clutton-Brock, T. H. Validating methods for estimating endocranial volume in individual red deer (Cervus elaphus). Behav. Process. 92, 143–146 (2013).
Article Google Scholar
63.
Jolly, C. The classification and natural history of Theropithecus (Simopithecus) (Andrew, 1916) baboons of the African Plio-Pleistocene. (Bull. Brit. Mus. Nat. Hist., 1972).
64.
Delson, E. et al. Body mass in Cercopithecidae (Primates, mammalia): Estimation and scaling in extinct and extant taxa. (American Museum of Natural History, 2000).
65.
Hadfield, J. D., Richardson, D. S. & Burke, T. Towards unbiased parentage assignment: Combining genetic, behavioural and spatial data in a Bayesian framework. Mol. Ecol. 15, 3715–3730 (2006).
CAS PubMed Article Google Scholar
66.
Hadfield, J. D. MCMCglmm Course Notes. (2016).
67.
Morrissey, M. B. & Wilson, A. J. pedantics: An r package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing: Computer program article. Mol. Ecol. Resour. 10, 711–719 (2009).
PubMed Article Google Scholar
68.
Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
Article Google Scholar
69.
Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010).
CAS PubMed Article Google Scholar
70.
Wilson, A. J. et al. An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13–26 (2010).
PubMed Article Google Scholar
71.
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 13 (2017).
Article Google Scholar
72.
Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).
PubMed Article Google Scholar
73.
Morrissey, M. B. & Sakrejda, K. Unification of regression-based methods for the analysis of natural selection. Evolution 67, 2094–2100 (2013).
PubMed Article Google Scholar
74.
Stinchcombe, J., Agrawal, A., Hohenlohe, P., Arnold, S. & Blows, M. Estimating nonlinear selection gradients using quadratic regression coefficients: Double or nothing?. Evolution 62, 2435–2440 (2008).
PubMed Article Google Scholar
75.
Matsumura, S., Arlinghaus, R. & Dieckmann, U. Standardizing selection strengths to study selection in the wild: A critical comparison and suggestions for the future. Bioscience 62, 1039–1054 (2012).
Article Google Scholar More