Abstract
The sex of an organism can be determined by its genetics or its early environment. Across the animal kingdom, genetic sex determination (GSD) is far more common than environmental sex determination (ESD). Here, we propose an explanation for this pattern: the coupling of genes that bias offspring sex ratios towards one sex with genes that are beneficial in that sex but costly in the other. Gradual strengthening of the sex-specific tendency of this association eventuates in a neo-sex chromosome; that is, GSD. Our model predicts to which system of heterogamety ESD will evolve when nesting behaviour is an important determinant of brood sex ratios. It explains the puzzling observation in some GSD species of sex reversal induced by extreme environments. The model also suggests an approach to discovering sex-determining genes in ESD species.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bull, J. J. Evolution of Sex Determining Mechanisms (Benjamin Cummings, Menlo Park, 1983).
Beukeboom, L. W. & Perrin, N. The Evolution of Sex Determination (Oxford Univ. Press, Oxford, 2014).
Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).
Charnov, E. L. & Bull, J. J. When is sex environmentally determined? Nature 266, 828–830 (1977).
Bull, J. J. Sex ratio evolution when fitness varies. Heredity 46, 9–26 (1981).
Shine, R. Why is sex determined by nest temperature in many reptiles? Trends Ecol. Evol. 14, 186–189 (1999).
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).
Warner, D. A. & Shine, R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–568 (2008).
Charnov, E. L. & Bull, J. J. Non-Fisherian sex ratios with sex change and environmental sex determination. Nature 338, 148–150 (1989).
Bull, J. J. Sex determination in reptiles. Q. Rev. Biol. 55, 3–21 (1980).
Janzen, F. J. & Paukstis, G. L. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66, 149–179 (1991).
Ospina-Alvarez, N. & Piferrer, 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).
Van Dooren, T. J. M. & Leimar, O. The evolution of environmental and genetic sex determination in fluctuating environments. Evolution 57, 2667–2677 (2003).
Schwanz, L. E. & Proulx, S. R. Mutual information reveals variation in temperature-dependent sex determination in response to environmental fluctuation, lifespan and selection. Proc. R. Soc. B Biol. Sci. 275, 2441–2448 (2008).
Bulmer, M. G. & Bull, J. J. Models of polygenic sex determination and sex ratio control. Evolution 36, 13–26 (1982).
Bull, J. J., Vogt, R. C. & Bulmer, M. G. Heritability of sex ratio in turtles with environmental sex determination. Evolution 36, 333–341 (1982).
Morjan, C. L. How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination? Am. Nat. 162, 205–219 (2003).
Mitchell, T. S., Maciel, J. A. & Janzen, F. J. Does sex-ratio selection influence nest-site choice in a reptile with temperature-dependent sex determination? Proc. R. Soc. B Biol. Sci. 280, 1–8 (2013).
Refsnider, J. M., Milne-Zelman, C., Warner, D. A. & Janzen, F. J. Population sex ratios under differing local climates in a reptile with environmental sex determination. Evol. Ecol. 28, 977–989 (2014).
Bull, J. J. & Bulmer, M. G. Longevity enhances selection of environmental sex determination. Heredity 63, 315–320 (1989).
McGaugh, S. E., Bowden, R. M., Kuo, C.-H. & Janzen, F. J. Field-measured heritability of the threshold for sex determination in a turtle with temperature-dependent sex determination. Evol. Ecol. Res. 13, 75–90 (2011).
McGaugh, S. E. & Janzen, F. J. Effective heritability of targets of sex‐ratio selection under environmental sex determination. J. Evol. Biol. 24, 784–794 (2011).
Janzen, F. J. Heritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina). Genetics 131, 155–161 (1992).
Grossen, C., Neuenschwander, S. & Perrin, N. Temperature‐dependent turnovers in sex‐determination mechanisms: a quantitative model. Evolution 65, 64–78 (2010).
Quinn, A. E., Sarre, S. D., Ezaz, T., Graves, J. A. M. & Georges, A. Evolutionary transitions between mechanisms of sex determination in vertebrates. Biol. Lett. 7, 443–448 (2011).
Schwanz, L. E., Ezaz, T., Gruber, B. & Georges, A. Novel evolutionary pathways of sex‐determining mechanisms. J. Evol. Biol. 26, 2544–2557 (2013).
Pezaro, N., Doody, J. S. & Thompson, M. B. The ecology and evolution of temperature‐dependent reaction norms for sex determination in reptiles: a mechanistic conceptual model. Biol. Rev. 92, 1348–1364 (2017).
Rice, W. R. Sexually antagonistic genes: experimental evidence. Science 256, 1436–1439 (1992).
Rice, W. R. & Chippindale, A. K. Intersexual ontogenetic conflict. J. Evol. Biol. 14, 685–693 (2001).
Haig, D., Ubeda, F. & Patten, M. M. Specialists and generalists: the sexual ecology of the genome. Cold Spring Harb. Perspect. Biol. 6, a017525 (2014).
Rice, W. R. On the instability of polygenic sex determination: the effect of sex-specific selection. Evolution 40, 633–639 (1986).
Van Doorn, G. S. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007).
Van Doorn, G. S. & Kirkpatrick, M. Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186, 629–645 (2010).
Fisher, R. A. The evolution of dominance. Biol. Rev. 6, 345–368 (1931).
Charlesworth, D. & Charlesworth, B. Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35, 205–214 (1980).
Rice, W. R. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911–914 (1987).
Charlesworth, B. The evolution of sex chromosomes. Science 251, 1030–1033 (1991).
Trivers, R. L. in The Evolution of Sex: An Examination of Current Ideas (eds Michod, R. E. & Levin, B. R.) 270–286 (Sinauer, Sunderland, 1988).
Miles, G. et al. A genetic linkage map for the saltwater crocodile (Crocodylus porosus). BMC Genom. 10, 339 (2009).
McGaugh, S. E., Schwanz, L. E., Bowden, R. M., Gonzalez, J. E. & Janzen, F. J. Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination. Proc. R. Soc. B Biol. Sci. 277, 1219–1226 (2009).
Tanaka, C. M. & Iwasa, Y. Cultural evolution of a belief controlling human mate choice: dynamic modeling of the hinoeuma superstition in Japan. J. Theor. Biol. 309, 20–28 (2012).
Organ, C. L. & Janes, D. E. Evolution of sex chromosomes in Sauropsida. Integr. Comp. Biol. 48, 512–519 (2008).
Hillis, D. M. & Green, D. M. Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J. Evol. Biol. 3, 49–64 (1990).
Van Doorn, G. S. Evolutionary transitions between sex-determining mechanisms: a review of theory. Sex. Dev. 8, 7–19 (2014).
Veller, C., Muralidhar, P., Constable, G. W. A. & Nowak, M. A. Drift-induced selection between male and female heterogamety. Genetics 203, 711–727 (2017).
Matsumoto, Y. & Crews, D. Molecular mechanisms of temperature-dependent sex determination in the context of ecological developmental biology. Mol. Cell. Endocrinol. 354, 103–110 (2012).
Schroeder, A. L., Metzger, K. J., Miller, A. & Rhen, T. A novel candidate gene for temperature-dependent sex determination in the common snapping turtle. Genetics 207, 557–571 (2016).
Valenzuela, N., Adams, D. C. & Janzen, F. J. Pattern does not equal process: exactly when is sex environmentally determined? Am. Nat. 161, 676–683 (2003).
Quinn, A. E. et al. Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411 (2007).
Radder, R. S., Quinn, A. E., Georges, A., Sarre, S. D. & Shine, R. Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol. Lett. 4, 176–178 (2008).
Holleley, C. E. et al. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523, 79–82 (2015).
Perrin, N. Sex reversal: a fountain of youth for sex chromosomes? Evolution 63, 3043–3049 (2009).
Ghiselin, M. T. The evolution of hermaphroditism among animals. Q. Rev. Biol. 44, 189–208 (1969).
Charnov, E. L. The Theory of Sex Allocation (Princeton Univ. Press, Princeton, 1982).
Kazancıoğlu, E. & Alonzo, S. H. Costs of changing sex do not explain why sequential hermaphroditism is rare. Am. Nat. 173, 327–336 (2009).
Charnov, E. L., Bull, J. J. & Maynard Smith, J. Why be an hermaphrodite? Nature 263, 125–126 (1976).
Kazancıoğlu, E. & Alonzo, S. H. A comparative analysis of sex change in Labridae supports the size advantage hypothesis. Evolution 64, 2254–2264 (2010).
Charnov, E. L., Los-den Hartogh, R. L., Jones, W. T. & van den Assem, J. Sex ratio evolution in a variable environment. Nature 289, 27–33 (1981).
Janzen, F. J. & Phillips, P. C. Exploring the evolution of environmental sex determination, especially in reptiles. J. Evol. Biol. 19, 1775–1784 (2006).
Pokorna, M. & Kratochvil, L. Phylogeny of sex‐determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 156, 168–183 (2009).
Acknowledgements
We are grateful to L. Beukeboom, J. Bull, J. Gerold, D. Haig, M. Lambert, J. Losos and R. Trivers for helpful comments, as well as to N. Edelman and K. Burns-Edelman for help with figure preparation. P.M. is supported by a National Science Foundation Graduate Research Fellowship. The computations in this paper were run on the Odyssey cluster supported by the FAS Division of Science, Research Computing Group at Harvard University.
Author information
Authors and Affiliations
Contributions
P.M. conceived the project. C.V. performed the modelling work. P.M. and C.V. developed the theory, analysed the results and wrote the paper.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Supplementary Information
Supplementary Methods and Supplementary Figures.
Rights and permissions
About this article
Cite this article
Muralidhar, P., Veller, C. Sexual antagonism and the instability of environmental sex determination. Nat Ecol Evol 2, 343–351 (2018). https://doi.org/10.1038/s41559-017-0427-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-017-0427-9