Variation in somatic condition and testis mass in Feirana quadranus along an altitudinal gradient

in Animal Biology
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The competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, the mechanisms shaping reproductive allocation and the resulting variations in reproductive investment relative to environmental variables such as resource availability and male-male competition remain poorly known in frogs. Here, we investigated inter-population variation in male somatic condition and testis mass across four populations of the swelled vent frog Feirana quadranus along an altitudinal gradient. We found that relative testis mass did not increase with altitude, which was inconsistent with previous predictions that an increase in latitude and/or altitude should result in decreased sperm production in anurans due to shortened breeding seasons and the decline in resource availability. We also found no increase in somatic condition and male/female operational sex ratio with altitude. However, the somatic condition exhibited a positive correlation with testis mass, which indicated the condition-dependent testis size in F. quadranus. Moreover, an increase of testis mass with increasing male/female operational sex ratio suggest that male-male competition can result in an increased intensity of sperm competition, thereby increasing testis mass.

Variation in somatic condition and testis mass in Feirana quadranus along an altitudinal gradient

in Animal Biology



  • AltonL.A.CondonC.WhiteC.R. & AngillettaM.J. Jr (2017) Colder environments did not select for a faster metabolism during experimental evolution of Drosophila melanogaster. Evolution71145-152.

  • AtkinsonD. & SiblyR.M. (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol. Evol.l12235-239.

  • BlanckenhornW.U. & DemontM. (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr. Comp. Biol.l44413-424.

  • BurnessG.Schulte-HosteddeA.I. & MontgomerieR. (2008) Body condition influences sperm energetics in lake whitefish (Coregonus clupeaformis). Can. J. Fish. Aquat. Sci.65615-620.

  • BuzattoB.A.ThyerE.M.RobertsJ.D. & SimmonsL.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. Evolution71329-341.

  • BuzattoB.A.RobertsJ.D. & SimmonsL.W. (2015) Sperm competition and the evolution of precopulatory weapons: increasing male density promotes sperm competition and reduces selection on arm strength in a chorusing frog. Evolution692613-2624.

  • ByrneP.G. & RobertsJ.D. (2004) Intrasexual selection and group spawning in quacking frogs (Crinia georgiana). Behav. Ecol.15872-882.

  • ByrneP.G.RobertsJ.D. & SimmonsL.W. (2002) Sperm competition selects for increased testis mass in Australian frogs. J. Evol. Biol.15347-355.

  • ChenC.HuangY.Y. & LiaoW.B. (2016b) 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. (2016a) 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.

  • ChenW.PikeD.A.HeD.WangY.RenL.WangX.FanX. & LuX. (2014) Altitude decreases testis weight of a frog (Rana kukunoris) on the Tibetan Plateau. Herpetol. J.24183-188.

  • DewsburyD.A. (1982) Ejaculate cost and male choice. Am. Nat.119601-610.

  • DziminskiM.A.RobertsJ.D.BeveridgeM. & SimmonsL.W. (2010) Among-population covariation between sperm competition and ejaculate expenditure in frogs. Behav. Ecol.21322-328.

  • FeiL.YeC.Y. & JiangJ.P. (2010) Colored Atlas of Chinese Amphibians. Sichuan Publishing House of Science and TechnologyChengdu, China.

  • 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.

  • HanH.Y.LiS.GanX.H. & ZhangX.M. (2017) Phenotypic diversity in natural populations of an endangered plant Tetracentron sinense. Bot. Sci.95283-294.

  • HettyeyA. & RobertsJ.D. (2006) Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition. Behav. Ecol. Sociobiol.59389-396.

  • HettyeyA.LaurilaA.HerczegG.JönssonK.I.KovácsT. & MeriläJ. (2005) Does testis weight decline towards the subarctic? A case study on the common frog, Rana temporaria. Naturwissenschaften92188-192.

  • HjernquistM.B.SödermanF.JönssonK.I.HerczegG.LaurilaA. & MeriläJ. (2012) Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate. Oecologia170641-649.

  • JamesF.C. (1970) Geographic variation in birds and its relationship to climate. Ecology51365-390.

  • 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.MiZ.P. & LiaoW.B. (2016a) Altitudinal variation in male reproductive investment in a polyandrous frog species (Hyla gongshanensis jingdongensis). Anim. Biol.66289-303.

  • JinL.YangS.N.LiaoW.B. & LüpoldS. (2016b) 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.

  • KusanoT.TodaM. & FukuyamaK. (1991) Testes size and breeding systems in Japanese anurans with special reference to large testes in the treefrog, Rhacophorus arboreus (Amphibia: Rhacophoridae). Behav. Ecol. Sociobiol.2927-31.

  • KvarnemoC. & AhnesjoI. (1996) The dynamics of operational sex ratios and competition for mates. Trends Ecol. Evol.11404-408.

  • LanuzaG.P.CarreteroM.A. & FontE. (2017) Intensity of male-male competition predicts morph diversity in a color polymorphic lizard. Evolution711832-1840.

  • LiY.X.SwaisgoodR.R.WeiW.NieY.G.HuY.B.YangX.Y.GuX.D. & ZhangZ.J. (2017) Withered on the stem: is bamboo a seasonally limiting resource for giant pandas? Environ. Sci. Pollut. Res. Int.2410537-10546.

  • LiaoW.B.MiZ.P.ZhouC.Q.JinL.LouS.L.HanX. & MaJ. (2011) Relative testis size and mating systems in anurans: large testis in multiple-male mating in foam-nesting frogs. Anim. Biol.61225-238.

  • LiaoW.B.LuX. & JehleR. (2014) Altitudinal variation in maternal investment and trade-offs between egg size and clutch size in the Andrew’s toad. J. Zool.29384-91.

  • 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. DOI:0.1186/s12983-016-0138-0.

  • LiaoW.B.LouS.L.ZengY. & KotrschalA. (2016b) Large brains, small guts: the expensive tissue hypothesis supported in anurans. Am. Nat.188693-700.

  • LiaoW.B.HuangY.ZengY.ZhongM.J. & LüpoldS. (2018) Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation?. Evolution424-17. DOI:10.1111/evo.13372.

  • 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.

  • LiuY.H.LiaoW.B.ZhouC.Q.MiZ.P. & MaoM. (2011) Asymmetry of testes in Guenther’s frog, Hylarana guentheri (Anuar: Ranidae). Asian Herpetol. Res.2234-239.

  • LüpoldS.TomkinsJ.L.SimmonsL.W. & FitzpatrickJ.L. (2014) Female monopolization mediates the relationship between pre- and post-copulatory sexual traits. Nat. Commun.53184. DOI:10.1038/ncomms4184.

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

  • 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.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.66189-195.

  • McDonaldG.C.SpurginL.G.FairfieldE.A.RichardsonD.S. & PizzariT. (2017) Pre- and postcopulatory sexual selection favor aggressive, young males in polyandrous groups of red jungle fowl. Evolution711653-1669.

  • MorrisonC. & HeroJ.M. (2003) Geographic variation in life-history characteristics of amphibians: a review. J. Anim. Ecol.72270-279.

  • OlssonM.MadsenT. & ShineR. (1997) Is sperm really so cheap? Costs of reproduction in male adders, Viper aberus. Proc. R. Soc. B264455-459.

  • PascoalS.MendrokM.WilsonA.J.HuntJ. & BaileyN.W. (2017) Sexual selection and population divergence II. Divergence in different sexual traits and signal modalities in field crickets (Teleogryllus oceanicus). Evolution711614-1626.

  • PischeddaA. & ChippindaleA.K. (2017) Direct benefits of choosing a high-fitness mate can offset the indirect costs associated with intralocus sexual conflict. Evolution711710-1718.

  • RoffD.A. (2002) Life-History Evolution. Sinauer AssociatesSunderland, MA, USA.

  • SamaniP. (2018) Digest: evolution of sperm size and number in external fertilizers. Evolution72404-405. DOI:10.1111/evo.13400.

  • Schulte-HosteddeA.I. & MillarJ.S. (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav. Ecol. Sociobiol.55272-277.

  • ShultzA.J. & BurnsK.J. (2017) The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae). Evolution711061-1074.

  • SimmonsL.W. & FitzpatrickJ.L. (2012) Sperm wars and the evolution of male fertility. Reproduction144519-534.

  • SimmonsL.W. & KotiahoJ.S. (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution561622-1631.

  • van NoordwijkA.J. & de JongG. (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat.128137-142.

  • WangB.JiangJ.P.ChenX.H.XieF. & ZhengZ.H. (2007) Morphometrical study on populations of the genus Feirana (Amphibia, Anura, Ranidae). Dong Wu Fen Lei Xue Bao (Acta Zootaxon. Sin.)3139-145.

  • WangB.JiangJ.P.XieF. & LiC. (2012) Postglacial colonization of the Qinling mountains: phylogeography of the swelled vent frog (Feirana quadranus). Plos One7e41579. DOI:10.1371/journal.pone.0041579.

  • WangW.Y.ZhangR.YinQ.X.ZhangS.P.LiW.Q.LiD.Y. & MiZ.P. (2017) Digestive tract length is positively correlated with altitude across Fejervarya limnocharis populations. Anim. Biol.67227-237.

  • WellK.D. (1977) The social behaviour of anuran amphibians. Anim. Behav.25666-693.

  • WuQ.G. & LiaoW.B. (2017) Evidence for directional testes asymmetry in Hyla gongshanensis jindongensis. Acta Herpetol.1289-93.

  • 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.

  • 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.

  • 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. (2014) Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location. BMC Evol. Biol.14104. DOI:10.1186/1471-2148-14-104.

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

  • ZhongM.J.WangX.Y.HuangY.Y. & LiaoW.B. (2016) Altitudinal variation in organ size in Polypedates megacephalus. Herpetol. J.27235-238.

  • ZhouC.Q.MaoM.LiaoW.B.MiZ.P. & LiuY.H. (2011) Testis asymmetry in the dark-spotted frog Rana nigromaculata. Herpetol. J.21181-185.


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    Location, sampling, mean and standard deviations of body size, somatic mass and testis mass among Feirana quadranus populations on Micang mountain, China.

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    Variation in relative testis mass among Feirana quadranus populations along an altitudinal gradient in western China. Relative testis mass=log10(testis mass)/log10(soma mass).

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    Positive correlation between testis mass and soma mass for all Feirana quadranus populations along an altitudinal gradient in western China.

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    Increase in relative testis mass with increasing OSR among Feirana quadranus populations along an altitudinal gradient in western China.


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