The adaptive significance of temperature-dependent sex determination in a reptile

Abstract

Understanding the mechanisms that determine an individual’s sex remains a primary challenge for evolutionary biology. Chromosome-based systems (genotypic sex determination) that generate roughly equal numbers of sons and daughters accord with theory1, but the adaptive significance of environmental sex determination (that is, when embryonic environmental conditions determine offspring sex, ESD) is a major unsolved problem2,3. Theoretical models predict that selection should favour ESD over genotypic sex determination when the developmental environment differentially influences male versus female fitness (that is, the Charnov–Bull model)4, but empirical evidence for this hypothesis remains elusive in amniote vertebrates—the clade in which ESD is most prevalent5. Here we provide the first substantial empirical support for this model by showing that incubation temperatures influence reproductive success of males differently than that of females in a short-lived lizard (Amphibolurus muricatus, Agamidae) with temperature-dependent sex determination. We incubated eggs at a variety of temperatures, and de-confounded sex and incubation temperature by using hormonal manipulations to embryos. We then raised lizards in field enclosures and quantified their lifetime reproductive success. Incubation temperature affected reproductive success differently in males versus females in exactly the way predicted by theory: the fitness of each sex was maximized by the incubation temperature that produces that sex. Our results provide unequivocal empirical support for the Charnov–Bull model for the adaptive significance of temperature-dependent sex determination in amniote vertebrates.

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Figure 1: Theoretical predictions of the Charnov–Bull model for the adaptive significance of TSD based on the TSD pattern in Jacky dragons ( A. muricatus).
Figure 2: Sex-specific body-size comparisons between individuals that successfully reproduced versus those that did not reproduce.
Figure 3: Incubation temperature affected the fitness of sons differently from that of daughters.

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Acknowledgements

We thank D. Allsop, J. Cuervo, W. Du, M. Elphick, H. Giragossyan, P. Harlow, T. Langkilde, M. Olsson, R. Peters, B. Phillips, S. Ruggeri, T. Schwartz, F. Seebacher, J. Thomas, M. Thompson, D. Van Dyk, M. Wall and Novartis Pharmaceuticals for assistance. Comments by F. Janzen and members of his laboratory improved this manuscript. Research funding was provided by Sigma Xi, the American Society of Ichthyologists and Herpetologists, the Norman Wettenhall Foundation, the Linnean Society of New South Wales, the Society for Integrative and Comparative Biology, the Chicago Herpetological Society, the Royal Zoological Society of New South Wales, Environmental Futures Network (to D.A.W.) and the Australian Research Council (to R.S.). Grants awarded to D.A.W. funded the development of the microsatellite markers and the genetic work associated with paternity analyses, and grants awarded to R.S. funded all other aspects of the study. This research was approved by the New South Wales National Parks Service, and the Animal Care and Ethics Committees of The University of Sydney and Macquarie University.

Author Contributions D.A.W. conducted the experiment, maintained the lizard populations, genotyped all individuals, analysed the data and wrote the first draft of the manuscript. Both authors contributed equally to the design of the experiment, discussion of the results and preparation of the final manuscript.

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Correspondence to D. A. Warner.

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Warner, D., Shine, R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–568 (2008). https://doi.org/10.1038/nature06519

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