Cerebellum size is positively correlated with geographic distribution range in anurans

in Animal Biology
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The ‘cognitive buffer’ hypothesis predicts that the costs of relatively large brains are compensated for later in life by the increased benefits of large brains providing a higher chance of survival under changing environments through flexible behaviors in the animal kingdom. Thus, animals that live in a larger range (with a higher probability of environmental variation) are expected to have larger brains than those that live in a restricted geographic range. Here, to test the prediction of the ‘cognitive buffer’ hypothesis that larger brains should be expected to occur in species living in geographic ranges of larger size, we analyzed the relationship between the size of the geographic range and brain size and the size of various brain regions among 42 species of anurans using phylogenetic comparative methods. The results show that there is no correlation between relative brain size and size of the species’ geographic range when correcting for phylogenetic effects and body size. Our findings suggest that the effects of the cognitive buffer and the energetic constraints on brains result in non-significant variation in overall brain size. However, the geographic range is positively correlated with cerebellum size, but not with optic tecta, suggesting that species distributed in a wider geographic range do not exhibit larger optic tecta which would provide behavioral flexibility to allow for an early escape from potential predators and discovery of new food resources in unpredictable environments.

Cerebellum size is positively correlated with geographic distribution range in anurans

in Animal Biology



  • AllmanJ.McLaughlinT. & HakeemA. (1993) Brain-weight and life-span in primate species. Proc. Natl Acad. Sci. USA90118-122.

  • AmielJ.J.TingleyR. & ShineR. (2011) Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One6e18277.

  • BartonR.A. (1998) Visual specialization and brain evolution in primates. Proc. R. Soc. B2651933-1937.

  • BartonR.A. & HarveyP.H. (2000) Mosaic evolution of brain structure in mammals. Nature4051055-1058.

  • BergerJ.SwensonJ.E. & PerssonI.L. (2001) Recolonizing carnivores and naive prey: conservation lessons from Pleistocene extinctions. Science2911036-1039.

  • ChenC.HuangY.Y. & LiaoW.B. (2016a) A comparison of testes size and sperm length between Polypedates megacephalus populations at different altitudes. Herpetol. J.26249-252.

  • ChenM.HuangY.LiuG.QinF.YangS. & XuX. (2016b) Effects of enhanced UV-B radiation on morphology, physiology, biomass, leaf anatomy and ultrastructure in male and female mulberry (Morus alba) saplings. Environ. Exp. Bot.12985-93.

  • DarribaD.TaboadaG.L.DoalloR. & PosadaD. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods9772.

  • DarwinC. (1871) The Origin of Species. John MurrayLondon, UK.

  • DeanerR.O.BartonR.A. & van SchaikC.P. (2003) Primate brains and life histories: renewing the connection. In: P.M. Kappeler & M.E. Pereira (Eds) Primates Life Histories and Socioecology pp. 233-265. University of Chicago PressChicago, IL, USA.

  • DrummondA.J.SuchardM.A.XieD. & RambautA. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol.291969-1973.

  • DukasR. & BernaysE.A. (2000) Learning improves growth rate in grasshoppers. Proc. Natl Acad. Sci. USA972637-2640.

  • DukasR. (2004) Evolutionary biology of animal cognition. Ann. Rev. Ecol. Evol. Syst.35347-374.

  • DunbarR.I.M. & ShultzS. (2007) Evolution in the social brain. Science3171344-1347.

  • EstesJ.A.TinkerM.T.WilliamsT.M. & DoakD.F. (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science282473-476.

  • FeiL. & YeC.Y. (2001) The Colour Handbook of Amphibians of Sichuan. China Forestry Publishing HouseBeijing, China.

  • FreckletonR.P.HarveyP.H. & PagelM. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat.160712-726.

  • GaramszegiL.Z.MøllerA.P. & ErritzøeJ. (2002) Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc. R. Soc. B269961-967.

  • GondaA.TrokovicN.HerczegG.LaurilaA. & MeriläJ. (2010) Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles. J. Evol. Biol.232300-2308.

  • GuJ.LiD.Y.LuoY.YingS.B.ZhangL.Y.ShiQ.M.ChenJ.ZhangS.P.ZhouZ.M. & LiaoW.B. (2017) Brain size in Hylarana guentheri seems unaffected by variation in temperature and growth season. Anim. Biol.67209-225.

  • IwaniukA.N. & NelsonJ.E. (2001) A comparative analysis of relative brain size in waterfowl (Anseriformes). Brain Behav. Evol.5787-97.

  • JerisonH.J. (1973) Evolution of the Brain and Intelligence. Academic PressNew York, NY, USA.

  • JiangA.ZhongM.J.YangR.L.LiaoW.B. & JehleR. (2015) Seasonality and age is positively related to brain size in Andrew’s toad (Bufo andrewsi). Evol. Biol.42339-348.

  • JinL.LiuW.C.LiY.H.ZengY. & LiaoW.B. (2015) Evidence for the expensive-tissue hypothesis in the Omei wood frog (Rana omeimontis). Herpetol. J.25127-130.

  • JinL.YangS.N.LiaoW.B. & LüpoldS. (2016) Altitude underlies variation in the mating system, somatic condition and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis). Behav. Ecol. Sociobiol.701197-1208.

  • KotrschalA. & TaborskyB. (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol.8e1000351.

  • KotrschalA.ZengH.L.van der BijlW.Öhman-MägiC.KotrschalK.PelckmansK. & KolmN. (2017) Evolution of brain region volumes during artificial selection for relative brain size. Evolution712942-2951.

  • LefebvreL.ReaderS.M. & SolD. (2004) Brains, innovations and evolution in birds and primates. Brain Behav. Evol.63233-246.

  • LiZ.T.GuoB.C.YangJ.HerczegG.GondaA.BalázsG.ShikanoT.CalboliF.C.F. & MeriläJ. (2017) Deciphering the genomic architecture of the stickleback brain with a novel multilocus gene-mapping approach. Mol. Ecol.261557-1575.

  • LiaoW.B.LiuW.C. & MeriläJ. (2015a) Andrew meets Rensch: sexual size dimorphism and the inverse of Rensch’s rule in Andrew’s toad (Bufo andrewsi). Oecologia177389-399.

  • LiaoW.B.LouS.L.ZengY. & MeriläJ. (2015b) Evolution of anuran brains: disentangling ecological and phylogenetic sources of variation. J. Evol. Biol.281986-1996.

  • LiaoW.B.LuoY.LouS.L. & JehleR. (2016a) Geographic variation in life-history traits: growth season affects age structure, egg size and clutch size in Andrew’s toad (Bufo andrewsi). Front. Zool.136.

  • LiaoW.B.LouS.L.ZengY. & KotrschalA. (2016b) Large brains, small guts: the expensive tissue hypothesis supported in anurans. Am. Nat.188693-699.

  • LiaoW.B.HuangY.ZengY.ZhongM.J.LuoY. & LüpoldS. (2018) Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation? Evolution724-17.

  • LiuQ.FengH.JinL.MiZ.P.ZhouZ.M. & LiaoW.B. (in press) Latitudinal variation in body size in Fejervarya limnocharis supports the inverse of Bergmann’s rule. Anim. Biol. DOI:10.1163/15707563-17000129.

  • LuoY.ZhongM.J.HuangY.LiF.LiaoW.B. & KotrschalA. (2017) Seasonality and brain size are negatively associated in frogs: evidence for the expensive brain framework. Sci. Rep.716629.

  • LüpoldS.JinL. & LiaoW.B. (2017) Population density and structure drive differential investment in pre- and post-mating sexual traits in frogs. Evolution711686-1699.

  • MaX.H.ZhongM.J.LongJ.MiZ.P. & LiaoW.B. (2016) Evolution in digestive tract in Bufo andrewsi associated with temperature and precipitation. Anim. Biol.66279-288.

  • MaiC.L.LiaoJ.ZhaoL.LiuS.M. & LiaoW.B. (2017a) Brain size evolution in the frog Fejervarya limnocharis does neither support the cognitive buffer nor the expensive brain framework hypothesis. J. Zool. Lond.30263-72.

  • MaiC.L.LiuY.H.JinL.MiZ.P. & LiaoW.B. (2017b) Altitudinal variation in somatic condition and investment in reproductive traits in male Yunnan pond frog (Pelophylax pleuraden). Zool. Anz.266189-195.

  • MøllerA.P. & ErritzøeJ. (2014) Predator-prey interactions, flight initiation distance and brain size. J. Evol. Biol.2734-42.

  • OrmeC.D.L.FreckletonR.P.ThomasG.H.PetzoldtT. & FritzS.A. (2012) Caper: comparative analyses of phylogenetics and evolution in R. http://R-Forge.R-project.org/projects/caper/.

  • PravosudovV.V. & ClaytonN.S. (2002) A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav. Neurosci.116515-522.

  • R Development Core Team (2016) R: a Language and Environment for Statistical Computing. R Foundation for Statistical ComputingVienna, Austria. http://www.R-project.org.

  • RambautA.SuchardM.A.XieD. & DrummondA.J. (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer.

  • RanadeS.C.RoseA.RaoM.GallegoJ.GressensP. & ManiS. (2008) Different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neuroscience152859-866.

  • ReaderS.M. & LalandK.N. (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA994436-4441.

  • RicklefsR.E. (2004) The cognitive face of avian life histories: the 2003 Margaret Morse Nice lecture. Wilson Bull.116119-133.

  • RohlfF.J. (2004) TpsDig 1.40. Department of Ecology and Evolution State University at Stony Brook NY USA.

  • RothG. & DickeU. (2005) Evolution of the brain and intelligence. Trends Cogn. Sci.9250-257.

  • RothG. & WalkowiakW. (2015) The influence of genome and cell size on brain morphology in amphibians. Cold Spring Harb. Perspect. Biol.7a019075.

  • RothG.BlankeJ. & WakeD.B. (1994) Cell size predicts morphological complexity in the brains of frogs and salamanders. Proc. Natl Acad. Sci. USA914796-4800.

  • RothG.NishikawaK.C. & WakeD.B. (1997) Genome size, secondary simplification, and the evolution of the brain in salamanders. Brain Behav. Evol.5050-59.

  • RothT.C. & PravosudovV.V. (2009) Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc. R. Soc. B276401-405.

  • RothT.C.LaDageL.D. & PravosudovV.V. (2010) Learning capabilities enhanced in harsh environments: a common garden approach. Proc. R. Soc. B2773187-3193.

  • SayolF.MasponsJ.LapiedraO.IwaniukA.N.SzékelyT. & SolD. (2016) Environmental variation and the evolution of large brains in birds. Nat. Commun.713971.

  • SolD. (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett.5130-133.

  • SolD.DuncanR.P.BlackburnT.M.CasseyP. & LefebvreL. (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl Acad. Sci. USA1025460-5465.

  • SolD.SzékelyT.LikerA. & LefebvreL. (2007) Big-brained birds survive better in nature. Proc. R. Soc. B274755-761.

  • StriedterG.F. (2005) Principles of Brain Evolution. Sinauer AssociatesSunderland, MA, USA.

  • TamuraK.StecherG.PetersonD.FilipskiA. & KumarS. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol.302725-2729.

  • TaylorG.M.NolE. & BoireD. (1995) Brain regions and encephalization in anurans: adaptation or stability? Brain Behav. Evol.4596-109.

  • van WoerdenJ.T.van SchaikC.P. & IslerK. (2010) Effects of seasonality on brain size evolution: evidence from strepsirrhine primates. Am. Nat.176758-767.

  • van WoerdenJ.T.WillemsE.P.van SchaikC.P. & IslerK. (2011) Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution66191-199.

  • van WoerdenJ.T.van SchaikC.P. & IslerK. (2014) Brief communication: seasonality of diet composition is related to brain size in new world monkeys. Am. J. Phys. Anthropol.154628-632.

  • VinczeO. (2016) Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds. Evolution702123-2133.

  • VinczeO.VágásiC.I.PapP.L.OsváthG. & MøllerA.P. (2015) Brain regions associated with visual cues are important for bird migration. Biol. Lett.1120150678.

  • WuQ.G.LouS.L.ZengY. & LiaoW.B. (2016) Spawning location promotes evolution of bulbus olfactorius size in anurans. Herpetol. J.26247-250.

  • YangS.N.HuangX.F.ZhongM.J. & LiaoW.B. (2017) Geographical variation in limb muscle mass of the Andrew’s toad (Bufo andrewsi). Anim. Biol.6717-28.

  • YangS.N.FengH.JinL.ZhouZ.M. & LiaoW.B. (in press) No evidence for the expensive-tissue hypothesis in Fejervarya limnocharis. Anim. Biol. DOI:10.1163/15707563-17000094.

  • YopakE.K.LisneyT.J.DarlingtonR.B.CollinS.P.MontgomeryJ.C. & FinlayB.L. (2010) A conserved pattern of brain scaling from sharks to primates. Proc. Natl Acad. Sci. USA10712946-12951.

  • YopakK.E.LisneyT.J.CollinS.P. & MontgomeryJ.C. (2007) Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans. Brain Behav. Evol.69280-300.

  • YuX.ZhongM.J.LiD.Y.JinL.LiaoW.B. & KotrschalA. (in press) Large-brained frogs mature later and live longer. Evolution. DOI:10.1111/evo.13478.

  • ZengY.LouS.L.LiaoW.B.JehleR. & KotrschalA. (2016) Sexual selection impacts brain anatomy in frogs and toads. Ecol. Evol.67070-7079.

  • ZhaoL.MaoM. & LiaoW.B. (2016) No evidence for the ‘expensive-tissue hypothesis’ in the dark-spotted frog, Pelophylax nigromaculatus. Acta Herpetol.1169-73.


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    Phylogeny of the 42 anuran species used based on three nuclear genes and the three mitochondrial genes and indicating the mean node height.

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    Regression models of sizes of different brain regions in relation to various predictor variables for males across 42 anuran species when controlling for phylogeny (PGLS). Brain size was added as a covariate. The partial regression slopes (β) and standard errors (se) for the predictor variable, t- and P-values are presented for each model.

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    Correlation between residual cerebellum size and size of the geographic range in 42 species of anurans, controlling for the effect of brain size and phylogeny.


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