Evolution of vertebrate brain size is associated with sexual traits
In: Animal BiologyAbstract
The expensive tissue hypothesis predicts a trade-off between investments in the brain and other energetically costly organs due to the costs associated with their growth and maintenance within the finite energy resources available. However, few studies address the strength of relationships between brain size and investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits. Here, in a broad comparative study, we tested the prediction that the relationship between brain size and investment in sexual traits differs among taxa relative to the importance of sperm competition within them. We found that brain size was negatively correlated with sexual size dimorphism (SSD) in anurans and primates, and it tended to decrease with SSD in ungulates and cetaceans. However, brain size did not covary significantly with armaments (e.g., canine length, horn, antler, and muscle mass). Brain size was not correlated with postcopulatory sexual traits (testes and ejaculates). The intensity of covariance between brain size and precopulatory sexual traits decreased with increasing relative testis size.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Aiello, L.C. & Wheeler, P. (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol., 36, 199-221. DOI:10.1086/204350.
-
Andersson, M. (1994) Sexual Selection. Princeton University Press, Princeton, NJ, USA.
-
Andersson, M. & Norberg, R.Å. (1981) Evolution of reversed sexual size dimorphism and role partitioning among predatory birds, with a size scaling of flight performance. Biol. J. Linn. Soc., 15, 105-130. DOI:10.1111/j.1095-8312.1981.tb00752.x.
-
Arnqvist, G. & Rowe, L. (2015) The shape of preference functions and what shapes them: a comment on Edward. Behav. Ecol., 26, 325. DOI:10.1093/beheco/aru20.
-
Boogert, N.J., Fawcett, T.W. & Lefebvre, L. (2011) Mate choice for cognitive traits: a review of the evidence in nonhuman vertebrates. Behav. Ecol, 22, 447-459. DOI:10.1093/beheco/arq173.
-
Buzatto, B.A., Thyer, E.M., Roberts, J.D. & Simmons, L.W. (2017) Sperm competition and the evolution of precopulatory weapons: testis size and amplexus position, but not arm strength, affect fertilization success in a chorusing frog. Evolution, 71, 329-341. DOI:10.1111/evo.13136.
-
Darwin, C. (1871) The Descent of Man, and Selection in Relation to Sex. John Murray, London, UK.
-
Drummond, AJ., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol., 29, 1969-1973. DOI:10.1093/molbev/mss075.
-
Emlen, D.J. (2001) Costs and the diversification of exaggerated animal structures. Science, 291, 1534-1536. DOI:10.1126/science.1056607.
-
Fitzpatrick, J.L., Almbro, M., Gonzalez-Voyer, A., Hamada, S., Pennington, C., Scanlan, J. & Kolm, N. (2012) Sexual selection uncouples the evolution of brain and body size in pinnipeds. J. Evol. Biol., 25, 1321-1330. DOI:10.1111/j.1420-9101.2012.02520.x.
-
Freckleton, R.P., Harvey, P.H. & Pagel, M. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat., 160, 712-726.
-
Garamszegi, L.Z., Eens, M., Hurtrez-Boussès, S. & Møller, A. (2005) Testosterone, testes size, and mating success in birds: a comparative study. Horm. Behav., 47, 389-409. DOI:10.1016/j.yhbeh.2004.11.008.
-
García-Peña, C., García-Fabela, L.C., Gutiérrez-Robledo, L.M., García-González, J.J., Arango-Lopera, V.E. & Pérez-Zepeda, M.U. (2013) Handgrip strength predicts functional decline at discharge in hospitalized male elderly: a hospital cohort study. PloS One, 8, e69849. DOI:10.1371/journal.pone.0069849.
-
González-Lagos, C., Sol, D. & Reader, S.M. (2010) Large-brained mammals live longer. J. Evol. Biol., 23, 1064-1074. DOI:10.1111/j.1420-9101.2010.01976.x.
-
Healy, S.D. & Rowe, C. (2006) A critique of comparative studies of brain size. Proc. R. Soc. B Biol. Sci., 274, 453-464. DOI:10.1098/rspb.2006.3748.
-
Huang, Y., Mai, C.L., Liao, W.B. & Kotrschal, A. (2020) Body mass variation is negatively associated with brain size – evidence for the fat-brain trade-off in anurans. Evolution. DOI:10.1111/evo.13991.
-
Isler, K. & van Schaik, C. (2006) Costs of encephalization: the energy trade-off hypothesis tested on birds. J. Hum. Evol., 51, 228-243. DOI:10.1016/j.jhevol.2006.03.006.
-
Jennions, M.D. & Petrie, M. (2010) Why do females mate multiply? A review of the genetic benefits. Biol. Rev., 75, 21-64. DOI:10.1017/S0006323199005423.
-
Jerison, H. (1973) Evolution of the Brain and Intelligence. Academic Press, New York, NY, USA.
-
Jones, K.E. & MacLarnon, A.M. (2004) Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat., 164, E20-E31. DOI:10.1086/421334.
-
Kotrschal, A., Rogell, B., Bundsen, A., Svensson, B., Zajitschek, S., Brännström, I., Immler, S., Maklakov, A.A. & Kolm, N. (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol., 23, 168-171. DOI:10.1016/j.cub.2012.11.058.
-
Lefebvre, L., Whittle, P., Lascaris, E. & Finkelstein, A. (1997) Feeding innovations and forebrain size in birds. Anim. Behav., 53, 549-560. DOI:10.1006/anbe.1996.0330.
-
Lemaître, J.-F., Ramm, S.A., Barton, R. & Stockley, P. (2009) Sperm competition and brain size evolution in mammals. J. Evol. Biol., 22, 2215-2221. DOI:10.1111/j.1420-9101.2009.01837.x.
-
Liao, W.B., Lou, S.L., Zeng, Y. & Kotrschal, A. (2016) Large brains, small guts: the expensive tissue hypothesis supported within anurans. Am. Nat., 188, 693-700.
-
Liao, W.B., Huang, Y., Zeng, Y., Zhong, M.J., Luo, Y. & Lüpold, S. (2018) Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation? Evolution, 72, 4-17. DOI:10.1111/evo.13372.
-
Lindenfors, P., Tullberg, B.S. & Biuw, M. (2002) Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav. Ecol. Sociobiol., 52, 188-193. DOI:10.1007/s00265-002-0507-x.
-
Lüpold, S., Linz, G.M., Rivers, J.W., Westneat, D.F. & Birkhead, T.R. (2009) Sperm competition selects beyond relative testes size in birds. Evolution, 63, 391-402. DOI:10.1111/j.1558-5646.2008.00571.x.
-
Lüpold, S., Tomkins, J.L., Simmons, L.W. & Fitzpatrick, J.L. (2014) Female monopolization mediates the relationship between pre-and postcopulatory sexual traits. Nat. Communicat., 5, 3184. DOI:10.1038/ncomms4184.
-
Lüpold, S., Jin, L. & Liao, W.B. (2017) Population density and structure drive differential investment in pre- and postmating sexual traits in frogs. Evolution, 71, 1686-1699. DOI:10.1111/evo.13246.
-
Mai, C.L. & Liao, W.B. (2019) Brain size evolution in anurans: a review. Anim. Biol., 69, 265-279. DOI:10.1163/15707563-00001074.
-
Mai, C.L., Liao, W.B., Lüpold, S. & Kotrschal, A. (2020) Relative brain size is predicted by the intensity of intrasexual competition in frogs. Am. Nat. DOI:10.1086/709465.
-
Mink, J.W., Blumenschine, R.J. & Adams, D.B. (1981) Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis. Am. J. Physiol., 241, R203-R212. DOI:10.1152/ajpregu.1981.241.3.R203.
-
Olsson, M., Madsen, T. & Shine, R. (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. B Biol. Sci., 264, 455-459. DOI:10.1098/rspb.1997.0065.
-
Parker, G.A. & Begon, M.E. (1993) Sperm competition games: sperm size and sperm number under gametic control. Proc. R. Soc. B Biol. Sci., 253, 255-262. DOI:10.1098/rspb.1993.0111.
-
Pérez I de Lanuza, G., Carretero, M.A. & Font, E. (2017) Intensity of male-male competition predicts morph diversity in a color polymorphic lizard. Evolution, 71, 1832-1840. DOI:10.1111/evo.13256.
-
Pischedda, A. & Chippindale, A.K. (2017) Direct benefits of choosing a high-fitness mate can offset the indirect costs associated with intralocus sexual conflict. Evolution, 71, 1710-1718. DOI:10.1111/evo.13240.
-
Pitnick, S., Jones, K.E. & Wilkinson, G.S. (2006) Mating system and brain size in bats. Proc. R. Soc. B Biol. Sci., 273, 719-724. DOI:10.1098/rspb.2005.3367.
-
Prenter, J., Elwood, R.W. & Montgomery, W.I. (1999) Sexual size dimorphism and reproductive investment by female spiders: a comparative analysis. Evolution, 53, 1987-1994. DOI:10.1111/j.1558-5646.1999.tb04580.x.
-
R Core Team (2016) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://cran.r-project.org.
-
Raichle, M.E. & Gusnard, D.A. (2002) Appraising the brain’s energy budget. Proc. Natl Acad. Sci. USA, 99, 10237-10239. DOI:10.1073/pnas.172399499.
-
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer (Accessed 2017-06-12).
-
Ramm, S.A. & Stockley, P. (2010) Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Lett., 6, 219-221. DOI:10.1098/rsbl.2009.0635.
-
Reader, S.M. & Laland, K.N. (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA, 99, 4436-4441. DOI:10.1073/pnas.062041299.
-
Rice, W.R. & Holland, B. (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol., 41, 1-10. DOI:10.1007/s002650050357.
-
Schillaci, M.A. (2006) Sexual selection and the evolution of brain size in primates. PloS One, 1, e62. DOI:10.1371/journal.pone.0000062.
-
Selander, R.K. (1966) Sexual dimorphism and differential niche utilization in birds. Condor, 68, 113-151.
-
Seyfarth, R.M. & Cheney, D.L. (2002) What are big brains for? Proc. Natl Acad. Sci. USA, 99, 4141-4142. DOI:10.1073/pnas.082105099.
-
Street, S.E., Navarrete, A.F., Reader, S.M. & Laland, K.N. (2017) Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates. Proc. Natl Acad. Sci. USA, 114, 7908-7914. DOI:10.1073/pnas.1620734114.
-
Tanner, J.C., Ward, J.L., Shaw, R.G. & Bee, M.A. (2017) Multivariate phenotypic selection on a complex sexual signal. Evolution, 71, 1742-1754. DOI:10.1111/evo.13264.
-
Thom, M.D., Harrington, L.A. & Macdonald, D.W. (2004) Why are American mink sexually dimorphic? A role for niche separation. Oikos, 105, 525-535. DOI:10.1111/j.0030-1299.2004.12830.x.
-
Trumbo, S.T. & Robinson, G.E. (2004) Nutrition, hormones and life history in burying beetles. J. Insect Physiol., 50, 383-391. DOI:10.1016/j.jinsphys.2004.01.008.
-
Yu, X., Zhong, M.J., Li, D.Y., Jin, L., Liao, W.B. & Kotrschal, A. (2018) Large-brained frogs mature later and live longer. Evolution, 72, 1174-1183. DOI:10.1111/evo.13478.
-
Zeng, Y., Lou, S.L., Liao, W.B. & Jehle, R. (2014) Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location. BMC Evol. Biol., 14, 104. DOI:10.1186/1471-2148-14-104.
-
Zhong, M., Yu, X. & Liao, W. (2018) A review for life-history traits variation in frogs especially for anurans in China. Asian Herpetol. Res., 9, 165-174. DOI:10.16373/j.cnki.ahr.180052.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 511 | 135 | 4 |
| Full Text Views | 23 | 7 | 0 |
| PDF Views & Downloads | 39 | 14 | 0 |
Evolution of vertebrate brain size is associated with sexual traits
In: Animal BiologyAbstract
The expensive tissue hypothesis predicts a trade-off between investments in the brain and other energetically costly organs due to the costs associated with their growth and maintenance within the finite energy resources available. However, few studies address the strength of relationships between brain size and investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits. Here, in a broad comparative study, we tested the prediction that the relationship between brain size and investment in sexual traits differs among taxa relative to the importance of sperm competition within them. We found that brain size was negatively correlated with sexual size dimorphism (SSD) in anurans and primates, and it tended to decrease with SSD in ungulates and cetaceans. However, brain size did not covary significantly with armaments (e.g., canine length, horn, antler, and muscle mass). Brain size was not correlated with postcopulatory sexual traits (testes and ejaculates). The intensity of covariance between brain size and precopulatory sexual traits decreased with increasing relative testis size.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 511 | 135 | 4 |
| Full Text Views | 23 | 7 | 0 |
| PDF Views & Downloads | 39 | 14 | 0 |