Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse1,2. In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development2,3. However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species’ distribution differ in their sex-determining mechanisms, with temperature-dependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Bull, J. J. The Evolution of Sex Determining Systems (Benjamin/Cummings Inc., 1983)
Valenzuela, N. & Lance, V. Temperature-Dependent Sex Determination in Vertebrates (Smithsonian Books, 2004)
Janzen, F. J. & Phillips, P. C. Exploring the evolution of environmental sex determination, especially in reptiles. J. Evol. Biol. 19, 1775–1784 (2006)
Radder, R., Pike, D. A., Quinn, A. E. & Shine, R. Offspring sex in a lizard depends on egg size. Curr. Biol. 19, 1–4 (2009)
Quinn, A. E. et al. Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411–416 (2007)
Crews, D. & Bull, J. J. Mode and tempo in environmental sex determination in vertebrates. Semin. Cell Dev. Biol. 20, 251–255 (2009)
Warner, D. A. & Shine, R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–569 (2008)
Uller, T., Pen, I., Wapstra, E., Beukeboom, L. W. & Komdeur, J. The evolution of sex ratios and sex-determining systems. Trends Ecol. Evol. 22, 292–297 (2007)
Charnov, E. & Bull, J. J. When is sex environmentally determined? Nature 266, 828–830 (1977)
Conover, D. O. Adaptive significance of temperature-dependent sex determination in a fish. Am. Nat. 123, 297–313 (1984)
Warner, D. A., Uller, T. & Shine, R. Fitness effects of the timing of hatching may drive the evolution of temperature-dependent sex determination in short-lived lizards. Evol. Ecol. 23, 281–294 (2009)
Conover, D. O. & Heins, S. W. Adaptive variation in environmental and genetic sex determination in a fish. Nature 326, 496–498 (1987)
Wapstra, E. & Swain, R. Geographic and annual variation in life history traits in a temperate zone Australian skink. J. Herpetol. 35, 194–203 (2001)
Wapstra, E. et al. Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc. R. Soc. Lond. B 271, S230–S232 (2004)
Olsson, M. et al. Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection. Evolution 56, 1538–1542 (2002)
Atkins, N. Parental Effects in Two Species of Viviparous Lizards: Niveoscincus microlepidotus and N. ocellatus. PhD thesis, University of Tasmania. (2007)
Wapstra, E., Swain, R. & O’Reilly, J. M. Geographic variation in age and size at maturity in a small Australian viviparous skink. Copeia 3, 646–655 (2001)
Bulmer, M. G. & Bull, J. J. Models of polygenic sex determination and sex ratio control. Evolution 36, 13–26 (1982)
van Dooren, T. J. M. & Leimar, O. The evolution of environmental and genetic sex determination in fluctuating environments. Evolution 57, 2667–2677 (2003)
Leimar, O., Hammerstein, P. & van Dooren, T. J. M. A new perspective on developmental plasticity and the principles of adaptive morph determination. Am. Nat. 167, 367–376 (2006)
West-Eberhard, M.-J. Developmental Plasticity and Evolution (Oxford University Press, 2003)
Adolph, S. C. & Porter, W. P. Growth, seasonality, and lizard life histories: age and size at maturity. Oikos 77, 267–278 (1996)
Cadby, C. D. et al. Multi-scale approach to understanding climate effects on offspring size at birth and date of birth in a reptile. Integr. Zool. 5, 164–175 (2010)
Ospina-Alvarez, N. & Pifferer, F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS ONE 3, E2837 (2008)
Uller, T. & Badyaev, A. V. Evolution of “determinants” in sex determination: a novel hypothesis for the origin of environmental contingencies in avian sex-bias. Semin. Cell Dev. Biol. 20, 304–312 (2009)
Wapstra, E. et al. Climate effects on offspring sex ratio in a viviparous lizard. J. Anim. Ecol. 78, 84–90 (2009)
Neaves, L. et al. Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus. J. Exp. Zool. 305A, 74–82 (2006)
Melville, J. & Swain, R. Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lyosomaniae). Biol. J. Linn. Soc. 70, 667–680 (2000)
Funding was provided by the Australian Research Council to E.W., T.U. and I.P. (DP0877948), by the Hermon Slade Foundation to E.W., T.U. and I.P., and by the Wenner-Gren Foundations to T.U.
The authors declare no competing financial interests.
About this article
Cite this article
Pen, I., Uller, T., Feldmeyer, B. et al. Climate-driven population divergence in sex-determining systems. Nature 468, 436–438 (2010) doi:10.1038/nature09512
Phylogeography, more than elevation, accounts for sex chromosome differentiation in Swiss populations of the common frog ( Rana temporaria )
Polar Biology (2019)
Sizes, condition factors and sex ratios of the scattered populations of the small cichlid fish, Alcolapia grahami, that inhabits the lagoons and sites of Lake Magadi (Kenya), one of the most extreme aquatic habitat on Earth
Environmental Biology of Fishes (2019)
Breadth of the thermal response captures individual and geographic variation in temperature‐dependent sex determination
Functional Ecology (2019)
Ecology and Evolution (2019)