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.
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.
Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, 1930)
Bull, J. J. & Charnov, E. L. Enigmatic reptilian sex ratios. Evolution 43, 1561–1566 (1989)
Shine, R. Why is sex determined by nest temperatures in many reptiles? Trends Ecol. Evol. 14, 186–189 (1999)
Charnov, E. L. & Bull, J. J. When is sex environmentally determined? Nature 266, 828–830 (1977)
Janzen, F. J. & Paukstis, G. L. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66, 149–179 (1991)
Charnov, E. L. & Bull, J. J. The primary sex ratio under environmental sex determination. J. Theor. Biol. 139, 431–436 (1989)
Conover, D. O. in Temperature-Dependent Sex Determination in Vertebrates (eds Valenzuela, N. & Lance, V. A.) 11–20 (Smithsonian Institution, Washington DC, 2004)
Janzen, F. J. Experimental evidence for the evolutionary significance of temperature-dependent sex determination. Evolution 49, 864–873 (1995)
Gutzke, W. H. N. & Crews, D. Embryonic temperature determines adult sexuality in a reptile. Nature 332, 832–834 (1988)
Janzen, F. J. & Paukstis, G. L. A preliminary test of the adaptive significance of temperature-dependent sex determination in reptiles. Evolution 45, 435–440 (1991)
Shine, R., Elphick, M. J. & Harlow, P. S. Sisters like it hot. Nature 378, 451–452 (1995)
Janzen, F. J. & Phillips, P. C. Exploring the evolution of environmental sex determination, especially in reptiles. J. Evol. Biol. 19, 1775–1784 (2006)
Tousignant, A. & Crews, D. Effect of exogenous estradiol applied at different embryonic stages on sex determination, growth, and mortality in the leopard gecko (Eublepharis macularius). J. Exp. Zool. 268, 17–21 (1994)
Tousignant, A. & Crews, D. Incubation temperature and gonadal sex affect growth and physiology in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. J. Morphol. 224, 159–170 (1995)
Harlow, P. S. & Taylor, J. E. Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Aust. Ecol. 25, 640–652 (2000)
Wibbels, T. & Crews, D. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J. Endocrinol. 141, 295–299 (1994)
Warner, D. A. & Shine, R. The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard. Evolution 59, 2209–2221 (2005)
Shine, R., Warner, D. A. & Radder, R. S. Windows of sexual lability during embryonic development in two lizard species with environmental sex determination. Ecology 88, 1781–1788 (2007)
Wennstrom, K. A. & Crews, D. Making males from females: the effects of aromatase inhibitors on a parthenogenetic species of whiptail lizards. Gen. Comp. Endocrinol. 99, 316–322 (1995)
Freedberg, S., Bowden, R. M., Ewert, M. A., Sengelaub, D. R. & Nelson, C. E. Long-term sex reversal by oestradiol in amniotes with heteromorphic sex chromosomes. Biol. Lett. 2, 378–381 (2006)
Warner, D. A. & Shine, R. Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154, 65–73 (2007)
Warner, D. A. & Shine, R. Maternal nest-site choice in a lizard with temperature-dependent sex determination. Anim. Behav. (in the press)
Austin, J. J., Rose, R. J. & Melville, J. Polymorphic microsatellite markers in the painted dragon lizard, Ctenophorus pictus. Mol. Ecol. Notes 6, 194–196 (2006)
Schwartz, T. S., Warner, D. A., Beheregaray, L. & Olsson, M. Microsatellite loci for Australian agamid lizards. Mol. Ecol. Notes 7, 528–531 (2007)
Marshall, T., Slate, J., Kruuk, L. & Pemberton, J. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998)
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.
About this article
Cite this article
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
Biology Letters (2020)
Evolutionary Ecology (2020)
Sex-specific effects of developmental temperature on morphology, growth and survival of offspring in a lizard with temperature-dependent sex determination
Biological Journal of the Linnean Society (2020)
Gene Dose Indicates Presence of Sex Chromosomes in Collared Lizards (Crotaphytus collaris), a Species with Temperature-Influenced Sex Determination
Sex and Incubation Temperature Independently Affect Embryonic Development and Offspring Size in a Turtle with Temperature-Dependent Sex Determination
Physiological and Biochemical Zoology (2020)