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Sexual antagonism and the instability of environmental sex determination

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.

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Fig. 1: GSD dominates ESD in vertebrates.
Fig. 2: The advantage of ESD: exploiting the sex-specific benefits of different environments.
Fig. 3: GSD evolves from TSD via sexually antagonistic genes.
Fig. 4: Invasion conditions for sex-biasing, sex-antagonistic gene complexes promoting the evolution of GSD from TSD.
Fig. 5: Gradual evolution of heterogametic sex determination from TSD.

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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.

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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.

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Correspondence to Pavitra Muralidhar or Carl Veller.

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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

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