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Brain size evolution in anurans: a review
In: Animal BiologyAbstract
Selection pressure is an important force in shaping the evolution of vertebrate brain size among populations within species as well as between species. The evolution of brain size is tightly linked to natural and sexual selection, and life-history traits. In particular, increased environmental stress, intensity of sexual selection, and slower life history usually result in enlarged brains. However, although previous studies have addressed the causes of brain size evolution, no systematic reviews have been conducted to explain brain size in anurans. Here, we review whether brain size evolution supports the cognitive buffer hypothesis (CBH), the expensive tissue hypothesis (ETH), or the developmental cost hypothesis (DCH) by analyzing the intraspecific and/or interspecific patterns in brain size and brain regions (i.e., olfactory nerves, olfactory bulbs, telencephalon, optic tectum, and cerebellum) associated with ecological factors (habitat, diet and predator risk), sexual selection intensity, life-history traits (age at sexual maturity, mean age, longevity, clutch size and egg size, testis size and sperm length), and other energetic organs. Our findings suggest that brain size evolution in anurans supports the CBH, ETH or DCH. We also suggest future directions for studying the relationships between brain size evolution and crypsis (i.e., ordinary mucous glands in the skin), and food alteration in different developmental stages.
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-
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.
-
Allman, J. (2000) Evolving Brains. Scientific American Library. W.H. Freeman and Co., New York, NY, USA.
-
Allman, J., McLaughlin, T. & Hakeem, A. (1993) Brain-weight and lifespan in primate species. Proc. Natl Acad. Sci. USA, 90, 118-122.
-
Amiel, J.J., Tingley, R. & Shine, R. (2011) Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One, 6, e18277. DOI:10.1371/journal.pone.0018277.
-
Barton, R.A. & Capellini, I. (2011) Maternal investment, life histories, and the costs of brain growth in mammals. Proc. Natl Acad. Sci. USA, 108, 6169-6174.
-
Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E.M. & Holekamp, K.E. (2016) Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl Acad. Sci. USA, 113, 2532-2537.
-
Berven, K.A. (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. 1. An experimental analysis of life history traits. Evolution, 36, 962-983.
-
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.
-
Cai, Y.L., Mai, C.L., Yu, X. & Liao, W.B. (2019) Effect of population density on relationship between pre- and postcopulatory sexual traits. Anim. Biol., 69, 281-292. DOI:10.1163/15707563-20181057.
-
Caro, T.M. (2005) Antipredator Defenses in Birds and Mammals. University of Chicago Press, Chicago, IL, USA.
-
Chen, C., Huang, Y.T. & Liao, W.B. (2016) A comparison of testes size and sperm length in Polypedates megacephalus between two populations at different altitudes. Herpetol. J., 26, 249-252.
-
Chivers, D.P., Kiesecker, J.M. & Blaustein, A.R. (1998) Mate choice by chemical cues in western redback (Plethodon vehiculum) and Dunn’s (P. dunni) salamanders. Ethology, 104, 781-788.
-
Clutton-Brock, T.H. & Harvey, P.H. (1980) Primates, brains and ecology. J. Zool., 190, 309-323.
-
Corral-López, A., Garate-Olaizola, M., Buechel, S.D., Kolm, N. & Kotrschal, A. (2017) On the role of body size, brain size, and eye size in visual acuity. Behav. Ecol. Sociobiol., 71, 179. DOI:10.1007/s00265-017-2408-z.
-
Cummins, C.P. (1986) Temporal and spatial variation in egg size and fecundity in Rana temporaria. J. Anim. Ecol., 55, 303-316.
-
Darst, R. & Cummings, M.E. (2006) Predator learning favors mimicry of a less-toxic model in poison frogs. Nature, 440, 208-211.
-
Dechmann, D.K.N. & Safi, K. (2009) Comparative studies of brain evolution: a critical insight from the Chiroptera. Biol. Rev., 84, 161-172.
-
Dreher, C.E., Cummings, M.E. & Pröhl, H. (2015) An analysis of predator selection to affect aposematic coloration in a poison frog species. PLoS One, 10, e0130571. DOI:10.1371/journal.pone.0130571.
-
Dunbar, R.I.M. & Shultz, S. (2007) The social brain hypothesis. Science, 317, 1344-1347.
-
Faivovich, J., McDiarmid, R.W. & Myers, C.W. (2013) Two new species of Myersiohyla (Anura: Hylidae) from Cerro de la Neblina, Venezuela, with comments on other species of the genus. Am. Mus. Novit., 3792, 1-63.
-
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.
-
Garamszegi, L.Z., Eens, M., Erritzøe, J. & Møller, A.P. (2005) Sperm competition and sexually size dimorphic brains in birds. Proc. Biol. Sci., 272, 159-166.
-
Gonda, A., Trokovic, N., Herczeg, G., Laurila, A. & Merilä, J. (2010) Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles. J. Evol. Biol., 23, 2300-2308.
-
Gonzalez-Voyer, A. & Kolm, N. (2010) Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids. PLoS One, 5, e14355. DOI:10.1371/journal.pone.0014355.
-
Gu, J., Li, D.Y., Luo, Y., Ying, S.B., Zhang, L.Y., Shi, Q.M., Chen, J., Zhang, S.P., Zhou, Z.M. & Liao, W.B. (2017) Brain size in Hylarana guentheri seems unaffected by variation in temperature and growth season. Anim. Biol., 67, 209-225.
-
Huang, C.H., Yu, X. & Liao, W.B. (2018) The expensive-tissue hypothesis in vertebrates: gut microbiota effect, a review. Int. J. Mol. Sci., 19, 1792. DOI:10.3390/ijms19061792.
-
Isler, K. & van Schaik, C.P. (2006) Costs of encephalization: the energy trade-off hypothesis tested on birds. J. Hum. Evol., 51, 228-243.
-
Isler, K. & van Schaik, C.P. (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol., 57, 392-400.
-
Jerison, H.J. (1973) Evolution of the Brain and Intelligence. Academic Press, New York, NY, USA.
-
Jiang, A., Zhong, M.J., Xie, M., Lou, S.L., Jin, L., Jehle, R. & Liao, W.B. (2015) Seasonality and age is positively related to brain size in Andrew’s toad (Bufo andrewsi). Evol. Biol., 42, 339-348. DOI:10.1007/s11692-015-9329-4.
-
Jin, L., Zhao, L., Liu, W.C., Li, Y.H., Zeng, Y. & Liao, W.B. (2015) Evidence for the expensive-tissue hypothesis in the Omei wood frog (Rana omeimontis). Herpetol. J., 25, 127-130.
-
Jin, L., Yang, S.N., Liao, W.B. & Lüpold, S. (2016a) Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis). Behav. Ecol. Sociobiol., 70, 1197-1208.
-
Jin, L., Mi, Z.P. & Liao, W.B. (2016b) Altitudinal variation in male reproductive investments in a polyandrous frog species (Hyla gongshanensis jingdongensis). Anim. Biol., 66, 289-303.
-
Jones, K.E. & MacLarnon, A.M. (2004) Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat., 164, 20-31.
-
Joseph, P.N., Emberts, Z., Sasson, D.A. & Miller, C.W. (2018) Males that drop a sexually selected weapon grow larger testes. Evolution, 72, 113-122.
-
Kotrschal, A., Rogell, B., Bundsen, A., Svensson, B., Zajitschek, S., Brannstrom, 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.
-
Kotrschal, A., Buechel, S.D., Zala, S.M., Corral-Lopez, A., Penn, D.J. & Kolm, N. (2015) Brain size affects female but not male survival under predation threat. Ecol. Lett., 8, 6-52.
-
Kotrschal, A., Zeng, H.L., van der Bijl, W., Öhman-Mägi, C., Kotrschal, K., Pelckmans, K. & Kolm, N. (2017) Evolution of brain region volumes during artificial selection for relative brain size. Evolution, 71, 2942-2951.
-
Lefebvre, L., Nicolakakis, N. & Boire, D. (2002) Tools and brains in birds. Behaviour, 139, 939-973.
-
Liao, W.B. & Lu, X. (2011) A comparison of reproductive output of the Omei treefrog (Rhacophorus omeimontis) between high and low elevations. Anim. Biol., 61, 263-276.
-
Liao, W.B., Mi, Z.P., Zhou, C.Q., Jin, L., Lou, S.L., Han, X. & Ma, J. (2011) Relative testis size and mating systems in anurans: large testis in multiple-male mating in foam-nesting frogs. Anim. Biol., 61, 225-238.
-
Liao, W.B., Xiao, W.M. & Cai, Y.L. (2013) Within population variation in testis size in the mole-shrew (Anourosorex squamipes). Ital. J. Zool., 80, 204-209.
-
Liao, W.B., Lou, S.L., Zeng, Y. & Merilä, J. (2015) Evolution of anuran brains: disentangling ecological and phylogenetic sources of variation. J. Evol. Biol., 28, 1986-1996.
-
Liao, W.B., Lou, S.L., Zeng, Y. & Kotrschal, A. (2016) Large brains, small guts: the expensive tissue hypothesis supported in anurans. Am. Nat., 188, 693-699.
-
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.
-
Liu, Y.H., Liao, W.B., Zhou, C.Q., Mi, Z.P. & Mao, M. (2011) Asymmetry of testes in Guenther’s frog, Hylarana guentheri (Anuar: Ranidae). Asian Herpetol. Res., 2, 234-239.
-
Liu, J., Zhou, C.Q. & Liao, W.B. (2014) Neither evidences for the compensation hypothesis nor the expensive-tissue hypothesis in Carassius auratus. Anim. Biol., 64, 177-187.
-
Liu, Y.T., Luo, Y., Gu, J., Jiang, S., Li, D.Y. & Liao, W.B. (2018) The relationship between brain size and digestive tract do not support expensive-tissue hypothesis in Hylarana guentheri. Acta. Herpetol., 13, 141-146. DOI:10.13128/Acta_Herpetol-20920.
-
Lou, S.L., Li, Y.H., Jin, L., Mi, Z.P., Liu, W.C. & Liao, W.B. (2013) Altitudinal variation in digestive tract length in Yunnan pond frog (Pelophylax pleuraden). Asian Herpetol. Res., 4, 263-267.
-
Luo, Y., Zhong, M.J., Huang, Y., Li, F., Liao, W.B. & Kotrschal, A. (2017) Seasonality and brain size are negatively associated in frogs: evidence for the expensive brain framework. Sci. Rep., 7, 16629. DOI:10.1038/s41598-017-16921-1.
-
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.
-
Ma, X.H., Zhong, M.J., Long, J., Mi, Z.P. & Liao, W.B. (2016) Digestive tract adaptation associated with temperature and precipitation in male Bufo andrewsi. Anim. Biol., 66, 279-288.
-
Mai, C.L., Liao, J., Zhao, L., Liu, S.M. & Liao, W.B. (2017a) Brain size evolution in the frog Fejervarya limnocharis does neither support the cognitive buffer nor the expensive brain framework hypothesis. J. Zool., 302, 63-72.
-
Mai, C.L., Liu, Y.H., Jin, L., Mi, Z.P. & Liao, W.B. (2017b) Altitudinal variation in somatic condition and reproductive investment of male Yunnan pond frogs (Dianrana pleuraden). Zool. Anz., 266, 189-195.
-
McCullough, E.L., Buzatto, B.A. & Simmons, L.W. (2018) Population density mediates the interaction between pre- and postmating sexual selection. Evolution, 72, 893-905.
-
Mi, Z.P., Liao, W.B., Jin, L., Lou, S.L., Cheng, J. & Wu, H. (2012) Testes asymmetry and sperm length in Rhacophorus omeimontis. Zool. Sci., 29, 368-372.
-
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.
-
Navarrete, A., van Schaik, C.P. & Isler, K. (2011) Energetics and the evolution of human brain size. Nature, 480, 91-93.
-
Penry, D.L. & Jumars, P.A. (1987) Modeling animal guts as chemical reactors. Am. Nat., 129, 69-96.
-
Piersma, T. & Lilliendahl, K. (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol. Biochem. Zool., 72, 405-415.
-
Pitnick, S., Jones, K.E. & Wilkinson, G.S. (2006) Mating system and brain size in bats. Proc. Biol. Sci., 273, 719-724.
-
Pontzer, H., Brown, M.H., Raichlen, D.A., Dunsworth, H.M., Hare, B., Walker, K.K., Luke, A., Dugas, L.R., Durazo-Arvizu, R., Schoeller, D.A., Plange-Rhule, J., Bovet, P., Forrester, T.E., Lambert, E.V., Thompson, M.E., Shumaker, R.W. & Ross, S.R. (2016) Metabolic acceleration and the evolution of human brain size and life history. Nature, 533, 390-392.
-
Powell, L.E., Isler, K. & Barton, R.A. (2017) Re-evaluating the link between brain size and behavioral ecology in primates. Proc. Biol. Sci., 284, 20171765. DOI:10.1098/rspb.2017.1765.
-
Qin, F., Liu, G., Huang, G., Dong, T., Liao, Y. & Xu, X. (2018) Zinc application alleviates the adverse effects of lead stress more in female Morus alba than in males. Environ. Exp. Bot., 146, 68-76.
-
Reader, S.M. & Laland, K.N. (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA, 99, 4436-4441.
-
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.
-
Salas, C., Broglio, C. & Rodríguez, F. (2003) Evolution of forebrain and spatial cognition in vertebrates: conservation across diversity. Brain. Behav. Evol., 62, 72-82.
-
Samuk, K., Xue, J. & Rennision, D.J. (2018) Exposure to predators does not lead to the evolution of larger brains in experimental populations of threespine stickleback. Evolution, 72, 916-929.
-
Sayol, F., Maspons, J., Lapiedra, O., Iwaniuk, A.N., Székely, T. & Sol, D. (2016) Environmental variation and the evolution of large brains in birds. Nat. Commun., 7, 13971. DOI:10.1038/ncomms13971.
-
Sol, D. (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett., 5, 130-133.
-
Sol, D., Duncan, R.P., Blackburn, T.M., Cassey, P. & Lefebvre, L. (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl Acad. Sci. USA, 102, 5460-5465.
-
Sol, D., Bacher, S., Reader, S.M. & Lefebvre, L. (2008) Brain size predicts the success of mammal species introduced into novel environments. Am. Nat., 172, S63-S71.
-
Stevens, M. (2007) Predator perception and the interrelation between different forms of protective coloration. Pcoc. Biol. Sci., 274, 1457-1464.
-
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.
-
Striedter, G.F. (2005) Principles of Brain Evolution. Sinauer Associates Inc., Sunderland, MA, USA.
-
Tang, T., Luo, Y., Huang, C.H., Liao, W.B. & Huang, W.C. (2018) Variation in somatic condition and testis mass in Feirana quadranus along an altitudinal gradient. Anim. Biol., 68, 277-288.
-
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.
-
Taylor, G.M., Nol, E. & Boire, D. (1995) Brain regions and encephalization in anurans: adaptation or stability. Brain. Behav. Evol., 45, 96-109.
-
Tsuboi, M., Husby, A., Kotrschal, A., Hayward, A., Buechel, S.D., Zidar, J. & Kolm, N. (2015) Comparative support for the expensive tissue hypothesis: big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids. Evolution, 69, 190-200.
-
Tsuboi, M., Shoji, J., Sogabe, A., Ahnesjö, I. & Kolm, N. (2016) Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of the Pacific seaweed pipefish. Ecol. Evol., 6, 647-655.
-
Van Woerden, J.T., Willems, E.P., van Schaik, C.P. & Isler, K. (2012) Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution, 66, 191-199.
-
Wang, J.Y. & Liao, W.B. (2018) Digest: ontogenesis and evolutionary allometry shape divergent evolution of genitalia in female cetaceans. Evolution, 72, 404-405.
-
Wang, W.Y., Zhang, R., Yin, Q.X., Zhang, S.P., Li, W.Q., Li, D.Y. & Mi, Z.P. (2017) Digestive tract length is positively correlated with altitude across Fejervarya limnocharis populations. Anim. Biol., 67, 227-237.
-
Wells, K.D. (2007) The Ecology and Behaviour of Amphibians. University of Chicago Press, Chicago, IL, USA.
-
Winkler, H., Leisler, B. & Bernroider, G. (2004) Ecological constraints on the evolution of avian brains. J. Ornithol., 145, 238-244.
-
Wu, Q.G., Lou, S.L., Zeng, Y. & Liao, W.B. (2016) Spawning location is linked to the relative size of olfactory nerves in anurans. Herpetol. J., 26, 245-248.
-
Yang, S.N., Huang, X.F., Zhong, M.J. & Liao, W.B. (2017) Geographical variation in limb muscle mass of the Andrew’s toad (Bufo andrewsi). Anim. Biol., 67, 17-28.
-
Yang, S.N., Feng, H., Jin, L., Zhou, Z.M. & Liao, W.B. (2018) No evidence for the expensive-tissue hypothesis in Fejervarya limnocharis. Anim. Biol., 68, 265-276.
-
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.
-
Zeng, Y., Lou, S.L., Liao, W.B., Jehle, R. & Kotrschal, A. (2016) Sexual selection impacts brain anatomy in frogs and toads. Ecol. Evol., 6, 7070-7079.
-
Zhao, L., Mao, M. & Liao, W.B. (2016) No evidence for the ‘expensive-tissue hypothesis’ in the dark-spotted frog (Pelophylax nigromaculata). Acta Herpetol., 11, 69-73.
-
Zhao, C.L., Luo, Y., Zhong, M.J., Xie, F., Jiang, J.P., Li, D.Y. & Liao, W.B. (2018) The size of cerebellum is positively correlated with geographic distribution range in anurans. Anim. Biol., 68, 309-320.
-
Zhong, M.J., Wang, X.Y., Huang, Y.Y. & Liao, W.B. (2017) Altitudinal variation in organ size in Polypedates megacephalus. Herpetol. J., 27, 235-238.
-
Zhong, M.J., Yu, X. & Liao, W.B. (2018) A review for life-history traits variation in frogs especially for anurans in China. Asian Herpetol. Res., 9, 165-174.
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Abstract
Selection pressure is an important force in shaping the evolution of vertebrate brain size among populations within species as well as between species. The evolution of brain size is tightly linked to natural and sexual selection, and life-history traits. In particular, increased environmental stress, intensity of sexual selection, and slower life history usually result in enlarged brains. However, although previous studies have addressed the causes of brain size evolution, no systematic reviews have been conducted to explain brain size in anurans. Here, we review whether brain size evolution supports the cognitive buffer hypothesis (CBH), the expensive tissue hypothesis (ETH), or the developmental cost hypothesis (DCH) by analyzing the intraspecific and/or interspecific patterns in brain size and brain regions (i.e., olfactory nerves, olfactory bulbs, telencephalon, optic tectum, and cerebellum) associated with ecological factors (habitat, diet and predator risk), sexual selection intensity, life-history traits (age at sexual maturity, mean age, longevity, clutch size and egg size, testis size and sperm length), and other energetic organs. Our findings suggest that brain size evolution in anurans supports the CBH, ETH or DCH. We also suggest future directions for studying the relationships between brain size evolution and crypsis (i.e., ordinary mucous glands in the skin), and food alteration in different developmental stages.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1373 | 262 | 34 |
| Full Text Views | 68 | 37 | 9 |
| PDF Views & Downloads | 88 | 52 | 17 |