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Climate-driven population divergence in sex-determining systems

Abstract

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.

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Figure 1: Experimental effects of thermal conditions on sex ratio and birth date.
Figure 2: Life-history and temperature differences between lowland and highland populations of N. ocellatus.
Figure 3: Evolutionary simulation results with genetic sex determination as ancestral state.

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Acknowledgements

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.

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T.U., I.P. and E.W. initiated, planned and coordinated the project; E.W. collected field and experimental data, assisted by G.M.W.; T.U., G.M.W. and I.P. analysed data and generated parameter estimates for the model; I.P., B.F., A.H. and T.U. constructed the model and analysed its outcome; T.U. and I.P. wrote the paper with input from all other authors.

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Correspondence to Ido Pen.

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The authors declare no competing financial interests.

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Pen, I., Uller, T., Feldmeyer, B. et al. Climate-driven population divergence in sex-determining systems. Nature 468, 436–438 (2010). https://doi.org/10.1038/nature09512

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