Articles
The directional testes asymmetry increases with temperature in seven plateau brown frog (Rana kukunoris) populations
Published 2022-04-29
Keywords
- Environmental factor,
- testes asymmetry,
- body condition,
- age,
- the brown frog
How to Cite
Li, H. Y., Shang , M. J., Guo, J., Chen, B. J., Chen, P. Z., & Yu, T. L. (2022). The directional testes asymmetry increases with temperature in seven plateau brown frog (Rana kukunoris) populations. Acta Herpetologica, 17(1), 5–11. https://doi.org/10.36253/a_h-12187
Abstract
Environmental stress is generally regarded as an important evolutionary force for promoting the differentiation of shape, structure and function of animal organs closely related to survival and reproduction. Geographical variation of temperature and corresponding change in intensity of male-male competition might drive inter-population differences in directional testes asymmetry (DTA). Here, we investigated inter-population variation in DTA of the brown frog (Rana kukunoris) at seven different altitudes on the eastern Tibetan Plateau. We found that the size of right testes increased with temperature, but not left testes. We also found that male age, body mass or body condition, and testis mass had not effect on DTA, suggesting that heavier or older R. kukunoris males or those with larger testes had not stronger DTA. The operational sex ratio did not affect DTA, but there was a positive correlation between DTA and temperature, suggesting that differences in the length of activity period and resources availability across locations may affect the energy budget of this frog, resulting in a gradual change in reproduction energy parallel to increasing temperature.
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References
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Delbarco-Trillo, J., Tourmente, M., Roldan, E.R.S. (2013): Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis. PLoS One 8:e76510.
Friedmann, H. (1927): Testicular asymmetry and sex ratio in birds. Biol. Pharm. Bull. 52: 197–207.
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Gage, M.J.G. (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. P. Roy. Soc. B-Biol. Sci. 261:25–30.
Graves, G.R. (2004): Testicular volume and asymmetry are age dependent in black-throated blue warblers (Dendroica caerulescens). Auk 121:473–485.
Hettyey, A., Laurila, A., Herczeg, G., Jönsson, K.I., Kovács, T., Merilä, J. (2005): Does testis weight decline towards the Subarctic? A case study on the common frog, Rana temporaria. Naturwissenschaften 92:188–192.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. (2005): Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25:1965–1978.
Iddriss, A.R.I., Obese, F.Y., Robinson, J.E. (2018): Testis size and asymmetry in the guinea fowl (Numida meleagris): a test of the compensation hypothesis. Avian Biol. Res. 11:123-131.
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Kempenaers, B., Peer, K., Vermeirssen, E.L.M., Robertson, R.J. (2002): Testes size and asymmetry in the tree swallow Tachycineta bicolor: A test of the compensation hypothesis. Avian Sci. 3:115-122.
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Mai, C.L., Liu, Y.H., Jin, L., Mi, Z.P., Liao, W.B. (2017): Altitudinal variation in somatic condition and investment in reproductive traits in male Yunnan pond frog (Pelophylax pleuraden). Zool. Anz. 266:189-195.
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Møller, A.P. (1994): Directional selection and directional asymmetry: testes size and secondary sexual characters in birds. P. Roy. Soc. B-Biol. Sci. 258:147–151.
Møller, A.P., Briskie, J.V. (1995): Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36:357–365.
Palo, J.U., O’Hara, R.B., Laugen, A.T., Laurila, A., Primmer, C.R., Merilä, J. (2003): Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Mol. Ecol. 12:1963–1978.
Pitcher, T.E., Dunn, P.O., Whittingham, L.A. (2005): Sperm competition and the evolution of testes size in birds. J. Evolution. Biol. 18:557–567.
Ramm, S.A., Stockley, P. (2010): Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Letters. 6:219–221.
Rising, J.D. (1996): Relationship between testis size and mating systems in American sparrows (Emberizinae). Auk 113:224–228.
Sara, C., Stephen, P.J., Webster, M.S., Melissah, R. (2019): Asymmetries in reproductive anatomy: insights from promiscuous songbirds. Biol. J. Linn. Soc. 128:569-582.
Simmons, L.W., Kotiaho, J.S. (2002): Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631.
Soulsbury, C.D. (2010): Genetic patterns of paternity and testes size in mammals. PLoS One 5:e9581.
Tan, G.N., Govedich, F.R., Burd, M. (2004): Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae). J. Evolution. Biol. 17: 574–580.
Wu, Q.G., Liao, W.B. (2017): Evidence for directional testes asymmetry in Hyla gongshanensis jindongensis. Acta Herpetol. 12:89-93.
Yu, T.L., Guo, Y.S. (2015): Testes asymmetry of Bufo gargarizans in relation to body condition and age. Acta Herpetol. 10:155-158.
Yu, T.L., Jia, G., Sun, H.Q., Shi, W.H., Li, X.L., Wang, H.B., Huang, M.R., Ding, S.Y., Chen, J.P., Zhang, M. (2021): Altitudinal body size variation in Rana kukunoris: the effects of age and growth rate on the plateau brown frog from the eastern Tibetan Plateau. Ethol. Ecol. Evol. 1:1-13.
Yu, T.L., Lu, X. (2013): Body size variation of four latitudinally-separated populations of a toad species: age and growth rate as the proximate determinants. Integr. Zool. 8:315–323.
Yu, T.L., Wang, D.L., Busam, M., Deng, Y.H. (2019): Altitudinal variation in body size in Bufo minshanicus supports Bergmann’s rule. Evol. Biol. 33:449-460.
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 locations. BMC Evol. Biol. 14:1-8.
Zhang, L.X., An, D., He, Y., Li, Z., Fang, B., Chen, X., Lu, X. (2018): Variation in testis weight of the Tibetan toad Scutiger boulengeri along a narrow altitudinal gradient. Anim. Biol. 68:429-439.
Zhou, C.Q., Mao, M., Liao, W.B., Mi, .Z.P., Liu, Y.H. (2011): Testis asymmetry in the dark-spotted frog Rana nigromaculata. Herpetol. J. 21:181–185.
BLanckenhorn, W.U., Demont, M. (2004): Bergmann and converse Bergmann latitudinal clines in Arthropods: two ends of a continuum? Integr. Comp. Biol. 44:413–424.
Chen, W., Pike, D.A., He, D.J., Wang, Y., Ren, L.N., Wang, X.Y., Fan, X.G., Lu, X. (2014): Altitude decreases testis weight of a frog (Rana kukunoris) on the Tibetan Plateau. Herpetol. J. 24:183–188.
Chen, W., Wang, X.Y., Fan, X.G. (2013): Do anurans living in higher altitudes have higher prehibernation energy storage? investigations from a high-altitude frog. Herpetol. J. 23:45-49.
Delbarco-Trillo, J., Tourmente, M., Roldan, E.R.S. (2013): Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis. PLoS One 8:e76510.
Friedmann, H. (1927): Testicular asymmetry and sex ratio in birds. Biol. Pharm. Bull. 52: 197–207.
Gage, M.J.G. (1994): Associations between body size, mating pattern, testis size and sperm lengths across butterflies. P. Roy. Soc. B-Biol. Sci. 258:247–254.
Gage, M.J.G. (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. P. Roy. Soc. B-Biol. Sci. 261:25–30.
Graves, G.R. (2004): Testicular volume and asymmetry are age dependent in black-throated blue warblers (Dendroica caerulescens). Auk 121:473–485.
Hettyey, A., Laurila, A., Herczeg, G., Jönsson, K.I., Kovács, T., Merilä, J. (2005): Does testis weight decline towards the Subarctic? A case study on the common frog, Rana temporaria. Naturwissenschaften 92:188–192.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. (2005): Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25:1965–1978.
Iddriss, A.R.I., Obese, F.Y., Robinson, J.E. (2018): Testis size and asymmetry in the guinea fowl (Numida meleagris): a test of the compensation hypothesis. Avian Biol. Res. 11:123-131.
Jamieson, B.G.M., Briskie, J.V., Montgomerie, R. (2007): Testis size, sperm size and sperm competition. In Jamieson B. G. M. (Ed.), Reproductive Biology and Phylogeny of Birds. Part A: Phylogeny, Morphology, Hormones, Fertilization. Enfield 513–551.
Kempenaers, B., Peer, K., Vermeirssen, E.L.M., Robertson, R.J. (2002): Testes size and asymmetry in the tree swallow Tachycineta bicolor: A test of the compensation hypothesis. Avian Sci. 3:115-122.
Kimball, R.T., Ligon, D.J., Merola-Zwartjes, M. (1997): Testicular asymmetry and secondary sexual characters in red junglefowl. Auk 114: 221-228.
Liao, W.B., Liu, W.C., Merilä, J. (2015): Andrew meets Rensch: sexual size dimorphism and the inverse of Rensch’s rule in Andrew’s toad (Bufo andrewsi). Oecologia 177:389–399.
Liu, W.C., Huang, Y., Liao, Y.M. (2012): Testes asymmetry of Chinese endemic frog (Rana omeimontis) in relation to body condition and age. North-West. J. Zool. 8:390-393.
Liu, Y.H., Liao, W.B., Zhou, C.Q., Mi, Z.P., Mao, M. (2011): Asymmetry of testes in Guenther's Frog, Hylarana guentheri (Anura: Ranidae). Asian Herpetol. Res. 2: 234–239.
Ma, X.Y., Lu, X., Merilä, J. (2009): Altitudinal decline of body size in a Tibetan frog. J. Zool. 279:364-371.
Mai, C.L., Liu, Y.H., Jin, L., Mi, Z.P., Liao, W.B. (2017): Altitudinal variation in somatic condition and investment in reproductive traits in male Yunnan pond frog (Pelophylax pleuraden). Zool. Anz. 266:189-195.
Mi, Z.P., Liao, W.B., Jin, L., Lou, S.L., Cheng, J., Wu, H. (2012): Testis asymmetry and sperm length in Rhacophorus omeimontis. Zool. Sci. 29:68–372.
Møller, A.P. (1991): Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am. Nat. 137:882–906.
Møller, A.P. (1994): Directional selection and directional asymmetry: testes size and secondary sexual characters in birds. P. Roy. Soc. B-Biol. Sci. 258:147–151.
Møller, A.P., Briskie, J.V. (1995): Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36:357–365.
Palo, J.U., O’Hara, R.B., Laugen, A.T., Laurila, A., Primmer, C.R., Merilä, J. (2003): Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Mol. Ecol. 12:1963–1978.
Pitcher, T.E., Dunn, P.O., Whittingham, L.A. (2005): Sperm competition and the evolution of testes size in birds. J. Evolution. Biol. 18:557–567.
Ramm, S.A., Stockley, P. (2010): Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Letters. 6:219–221.
Rising, J.D. (1996): Relationship between testis size and mating systems in American sparrows (Emberizinae). Auk 113:224–228.
Sara, C., Stephen, P.J., Webster, M.S., Melissah, R. (2019): Asymmetries in reproductive anatomy: insights from promiscuous songbirds. Biol. J. Linn. Soc. 128:569-582.
Simmons, L.W., Kotiaho, J.S. (2002): Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631.
Soulsbury, C.D. (2010): Genetic patterns of paternity and testes size in mammals. PLoS One 5:e9581.
Tan, G.N., Govedich, F.R., Burd, M. (2004): Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae). J. Evolution. Biol. 17: 574–580.
Wu, Q.G., Liao, W.B. (2017): Evidence for directional testes asymmetry in Hyla gongshanensis jindongensis. Acta Herpetol. 12:89-93.
Yu, T.L., Guo, Y.S. (2015): Testes asymmetry of Bufo gargarizans in relation to body condition and age. Acta Herpetol. 10:155-158.
Yu, T.L., Jia, G., Sun, H.Q., Shi, W.H., Li, X.L., Wang, H.B., Huang, M.R., Ding, S.Y., Chen, J.P., Zhang, M. (2021): Altitudinal body size variation in Rana kukunoris: the effects of age and growth rate on the plateau brown frog from the eastern Tibetan Plateau. Ethol. Ecol. Evol. 1:1-13.
Yu, T.L., Lu, X. (2013): Body size variation of four latitudinally-separated populations of a toad species: age and growth rate as the proximate determinants. Integr. Zool. 8:315–323.
Yu, T.L., Wang, D.L., Busam, M., Deng, Y.H. (2019): Altitudinal variation in body size in Bufo minshanicus supports Bergmann’s rule. Evol. Biol. 33:449-460.
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 locations. BMC Evol. Biol. 14:1-8.
Zhang, L.X., An, D., He, Y., Li, Z., Fang, B., Chen, X., Lu, X. (2018): Variation in testis weight of the Tibetan toad Scutiger boulengeri along a narrow altitudinal gradient. Anim. Biol. 68:429-439.
Zhou, C.Q., Mao, M., Liao, W.B., Mi, .Z.P., Liu, Y.H. (2011): Testis asymmetry in the dark-spotted frog Rana nigromaculata. Herpetol. J. 21:181–185.