Gideon Gywa DEME,Xin HAO,Liang MA,et al.Elevational Variation in Reproductive Strategy of a Widespread Lizard: High-Elevation Females Lay Fewer but Larger Eggs[J].Asian Herpetological Research(AHR),2022,13(3):198-204.[doi:10.16373/j.cnki.ahr.210068]
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Elevational Variation in Reproductive Strategy of a Widespread Lizard: High-Elevation Females Lay Fewer but Larger Eggs
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2022 VoI.13 No.3
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Elevational Variation in Reproductive Strategy of a Widespread Lizard: High-Elevation Females Lay Fewer but Larger Eggs
Gideon Gywa DEME12 Xin HAO3 Liang MA1 Baojun SUN1 and Weiguo DU1*
1 Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
2 University of Chinese Academy of Sciences, Beijing 100039, China
3 College of Forestry, Hainan University, Haikou 570228, Hainan, China
between-population variation clutch size egg size elevational gradient Eremias argus local adaptation reproductive output
Identifying how reproductive strategies such as the trade-off between clutch size versus egg mass vary with elevational gradients is essential for our understanding of life-history evolution. We studied lacertid lizards (Eremias argus) in China, from six populations at different altitudes, to assess elevational variation in reproductive strategy. We found significant between-population variation in maternal body size and clutch mass, but these variations were not explained by elevational differences. However, high-elevation females tended to produce smaller clutches of larger eggs compared with their low-elevation counterparts, demonstrating an elevational change in the trade-off between egg size and number. The egg size-number trade-off is a reproductive strategy that may favor large offspring, better enabling them to survive severe and unpredictable environments found at high elevations.


Angilletta M. J., Niewiarowski P. H., Dunham A. E., Leache A. D., Porter W. P. 2004. Bergmann’s clines in ectotherms: Illustrating a life-history perspective with Sceloporus lizards. Am Nat, 164: E168–E183
Ashton K. G., Feldman C. R. 2003. Bergmann’s rule in nonavian reptiles: Turtles follow it, lizards and snakes reverse it. Evolution, 57: 1151–1163
Badyaev A. V. 1997. Altitudinal variation in sexual dimorphism: A new pattern and possible underlying causes. Behav Ecol, 8: 675–690
Blackburn T. M., Gaston K. J., Loder N. 1999. Geographic gradients in body size: A clarification of Bergmann’s rule. Divers Distrib, 5: 165–174
Castilla A., Bauwens D. 2000. Reproductive characteristics of the lacer?tid lizard Podarcis atrata. Copeia, 3: 748–756
Chown S. L., Klok C. J. 2003. Altitudinal body size clines: Latitudinal effects associated with changing seasonality. Ecography, 26: 445–455
Du W. G. 2006. Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis. Oikos, 112: 363–369
Du W. G., Ji X., Zhang Y. P., Xu X. F., Shine R. 2005. Identifying sources of variation in reproductive and life-history traits among five populations of a Chinese lizard (Takydromus septentrionalis, Lacertiade). Biol J Linn Soc, 85: 443–453
Du W. G., Ji X., Zhang Y. P., Lin Z. H., Xu X. F. 2010. Geographic variation in offspring size of a widespread lizard (Takydromus septentrionalis): Importance of maternal investment. Biol J Linn Soc, 101: 59–67
Du W. G., Warner D. A., Langkilde T., Robbins T., Shine R. 2012. The roles of pre- and post-hatching growth rates in generating a latitudinal cline of body size in the eastern fence lizard (Sceloporus undulatus). Biol J Linn Soc, 106: 202–209
Du W. G., Robbins T. R., Warner D. A., Langkilde T., Shine R. 2014. Latitudinal and seasonal variation in reproductive effort of the eastern fence lizard (Sceloporus undulatus). Integr Zool, 9: 360–371
Feldman A., Meiri S. 2014. Australian snakes do not follow Bergmann’s rule. Evol Biol, 41: 327–335
Fischer K., Brakefield P. M., Zwaan B. J. 2003. Plasticity in butterfly egg size: Why larger offspring at lower temperatures? Ecology, 84: 3138–3147
Fitch H. S. 1980. Reproductive strategies of reptiles. SSAR Contrib Herpet, 7: 25–30
Foster K. L., Garland T. J., Schmitz L., Higham T. E. 2018. Skink ecomorphology: Forelimb and hind limb lengths, but not static stability, correlate with habitat use and demonstrate multiple solutions. Biol J Linn Soc, 125: 673–692
Guo C. 2016. Bergmann’s rule among Chinese amphibians and squamates. Ph.D. Thesis. Wuhan University
Hao X., Wang C. X., Han X. Z., Wang Y., Zhang Q., Zhang F. S., Sun B. J., Du W. G. 2021. A reciprocal egg-swap experiment reveals sources of variation in developmental success among populations of a desert lizard. Oecologia, 196: 27–35
Hille S. M., Cooper C. B. 2015. Elevational trends in life histories: Revising the pace-of-life framework. Biol Rev, 90: 204–213
Ji X., Wang Z. W. 2005. Geographic variation in reproductive traits and trade-offs between size and number of eggs of the Chinese cobra (Naja atra). Biol J Linn Soc, 85: 27–40
Jin Y. T., Tian R. R., Liu N. F. 2006. Altitudinal variations of morphological characters of Phrynocephalus sand lizards: On the validity of Bergmann’s and Allen’s rules. Acta Zool Sinica, 52: 838–845
Laugen A. T., Laurila A., Rasanen K., Merila J. 2003. Latitudinal counter gradient variation in the common frog (Rana temporaria) development rates — Evidence for local adaptation. J Evol Biol, 16: 996–1005
Liang T., Zhang Z., Dai W. Y., Shi L., Lu C. H. 2021. Spatial patterns in the size of Chinese lizards are driven by multiple factors. Ecol Evol, 11: 9621–9630
Lu H. L., Xu C. X., Jin Y. T., Hero J. M., Du W. G. 2018a. Proximate causes of altitudinal differences in body size in an agamid lizard. Ecol Evol, 8: 645–654
Lu H. L., Xu C. X., Zeng Z. G., Du W. G. 2018b. Environmental causes of between-population difference in growth rate of a high-altitude lizard. BMC Ecol, 18: 37
Ma L., Sun B. J., Li S. R., Sha W., Du W. G. 2014. Maternal thermal environment induces plastic responses in the reproductive life history of oviparous lizards. Physiol Biochem Zool, 87: 677–683
Ma L., Liu P., Su S., Luo L. G., Zhao W. G., Ji X. 2019a. Life‐history consequences of local adaptation in lizards: Takydromus wolteri (Lacertidae) as a model organism. Biol J Linn Soc, 127: 88–99
Ma L., Guo K., Su S., Lin L. H., Xia Y., Ji X. 2019b. Age-related reproduction of female Mongolian racerunners (Eremias argus; Lacertidae): Evidence of reproductive senescence. J Exp Zool, 331: 290–298
Martin T. E. 2002. A new view of avian life-history evolution tested on an incubation paradox. Proc Biol Sci, 269: 309–316
Meiri S., Avila L., Bauer A., Chapple D., Das I., Doan T., Doughty P., Ellis R., Grismer L., Kraus F., Morando M., Oliver P., Pincheira-Donoso D., Ribeiro-Junior M., Shea G., Torres-Carvajal O., Slavenko A., Roll U. 2020. The global diversity and distribution of lizard clutch sizes. Glob Ecol Biogeogr, 29: 1515–1530
Meiri S. 2018. Traits of lizards of the world: Variation around a successful evolutionary design. Glob Ecol Biogeogr, 27: 1168–1172
Meiri S., Dayan T. 2003. On the validity of Bergmann’s rule. J Biogeogr, 30: 331–351
Morita K., Tamate T., Sugimoto Y., Tago Y., Watanabe T., Konaka H., Sato M., Miyauchi Y., Ohkuma K., Nagasawa T. 2009. Latitudinal variation in egg size and number in anadromous masu salmon Oncorhynchus masou. J Fish Biol, 74: 699–705
Norris J., Tingley R., Meiri S., Chapple D. G. 2021. Environmental correlates of morphological diversity in Australian geckos. Glob Ecol Biogeogr, 30: 1086–1100
Parker G. A., Begon M. 1986. Optimal egg size and clutch size: Effects of environment and maternal phenotype. Am Nat, 128: 573–592
Peters R. H. 1986. The Ecological Implications of Body Size. Cambridge, UK: Cambridge University Press
Pincheira-Donoso D., Hodgson D. J., Tregenza T. 2008. The evolution of body size under environmental gradients in ectotherms: Why should Bergmann’s rule apply to lizards? BMC Evol Biol, 8: 68
Pincheira-Donoso D., Tregenza T. 2011. Fecundity selection and the evolution of reproductive output and sex-specific body size in the Liolaemus lizard adaptive radiation. Evol Biol, 38: 197–207
R Development Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing
Roy K. 2008. Dynamics of body size evolution. Science, 321: 1451–1452
Seebacher F., Shine R. 2004. uating thermoregulation in reptiles: The fallacy of the inappropriately applied method. Physiol Biochem Zool, 77: 688–695
Sears M. W., Angilletta M. J. 2004. Body size clines in Sceloporus lizards: Proximate mechanisms and demographic constraints. Integr Comp Biol, 44: 433–442
Shanbhag B. A., Radder R. S., Saidapur S. K. 2000. Maternal size deter?mines clutch mass, whereas breeding timing influences clutch and egg size in the tropical lizard, Calotes versicolor (Agamidae). Co?peia, 4: 1062–1067
Sibly R. M., Brown J. H. 2007. Effects of body size and lifestyle on evolution of mammal life histories. Proc Natl Acad Sci, 104: 17707–17712
Slavenko A., Feldman A., Allison A., Bauer A. M., B?hm M., Chirio L., Colli G. R., Das I., Doan T. M., LeBreton M., Martins M., Meirte D., Nagy Z. T., Nogueira C. D. C., Pauwels O. S. G., Pincheira-Donoso D., Roll U., Wagner P., Wang Y., Meiri S. 2019. Global patterns of body size evolution in squamate reptiles are not driven by climate. Glob Ecol Biogeogr, 28: 471–483
Stearns S. C. 1992. The Evolution of Life Histories. Oxford: Oxford University Press
Suárez-Varón G., Suárez-Rodríguez O., Granados-González G., Villagrán-Santa C. M., Gribbins K. M., Cortez-Quezada D., Hernández-Gallegos O. 2019. Relative clutch mass of Basiliscus vittatus Wiegmann, 1828 (Squamata, Corytophanidae): Female morphological constraints. Herpetozoa, 32: 211–219
Sun B. J., Tang W. Q., Zeng Z. G., Du W. G. 2014. The seasonal acclimatisation of locomotion in a terrestrial reptile, Plestiodon chinensis (Scincidae). Asian Herpetol Res, 5: 197–203
Sun B. J., Li S. R., Xu X. F., Zhao W. G., Luo L. G., Ji X., Du W. G. 2013. Different mechanisms lead to convergence of reproductive strategies in two lacertid lizards (Takydromus wolteri and Eremias argus). Oecologia, 172: 645–652
Tinkle D. W., Wilbur H. M., Tilley S. G. 1970. Evolutionary strategies in lizard reproduction. Evolution, 24: 55–74
Vitt L. J., Congdon J. D. 1978. Body shape, reproductive effort and rela?tive clutch mass in lizards: Resolution of a paradox. Am Nat, 112: 595–608
Weathers W. W., Davidson C. L., Olson C. R., Morton M., Nur N., Famula T. R. 2002. Altitudinal variation in in parental energy expenditure by white-crowned sparrows. J Exp Biol, 205: 2915–2924
Yampolsky L. Y., Scheiner S. M. 1996. Why larger offspring at lower temperatures? A demographic approach. Am Nat, 147: 86–100
Zammuto R. M. 1986. Life histories of birds: Clutch size, longevity, and body mass among North American game birds. Can J Zool, 64: 2739–2749
Zhao E. M., Zhao K. T., Zhou K. Y. 1999. Fauna Sinica Reptilia, Vol. 2, Squamata. Beijing: Science Press


Last Update: 2022-09-25