Letter | Published:

Climate-driven population divergence in sex-determining systems

Nature volume 468, pages 436438 (18 November 2010) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

References

  1. 1.

    The Evolution of Sex Determining Systems (Benjamin/Cummings Inc., 1983)

  2. 2.

    & Temperature-Dependent Sex Determination in Vertebrates (Smithsonian Books, 2004)

  3. 3.

    & Exploring the evolution of environmental sex determination, especially in reptiles. J. Evol. Biol. 19, 1775–1784 (2006)

  4. 4.

    , , & Offspring sex in a lizard depends on egg size. Curr. Biol. 19, 1–4 (2009)

  5. 5.

    et al. Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411–416 (2007)

  6. 6.

    & Mode and tempo in environmental sex determination in vertebrates. Semin. Cell Dev. Biol. 20, 251–255 (2009)

  7. 7.

    & The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–569 (2008)

  8. 8.

    , , , & The evolution of sex ratios and sex-determining systems. Trends Ecol. Evol. 22, 292–297 (2007)

  9. 9.

    & When is sex environmentally determined? Nature 266, 828–830 (1977)

  10. 10.

    Adaptive significance of temperature-dependent sex determination in a fish. Am. Nat. 123, 297–313 (1984)

  11. 11.

    , & Fitness effects of the timing of hatching may drive the evolution of temperature-dependent sex determination in short-lived lizards. Evol. Ecol. 23, 281–294 (2009)

  12. 12.

    & Adaptive variation in environmental and genetic sex determination in a fish. Nature 326, 496–498 (1987)

  13. 13.

    & Geographic and annual variation in life history traits in a temperate zone Australian skink. J. Herpetol. 35, 194–203 (2001)

  14. 14.

    et al. Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc. R. Soc. Lond. B 271, S230–S232 (2004)

  15. 15.

    et al. Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection. Evolution 56, 1538–1542 (2002)

  16. 16.

    Parental Effects in Two Species of Viviparous Lizards: Niveoscincus microlepidotus and N. ocellatus. PhD thesis, University of Tasmania. (2007)

  17. 17.

    , & Geographic variation in age and size at maturity in a small Australian viviparous skink. Copeia 3, 646–655 (2001)

  18. 18.

    & Models of polygenic sex determination and sex ratio control. Evolution 36, 13–26 (1982)

  19. 19.

    & The evolution of environmental and genetic sex determination in fluctuating environments. Evolution 57, 2667–2677 (2003)

  20. 20.

    , & A new perspective on developmental plasticity and the principles of adaptive morph determination. Am. Nat. 167, 367–376 (2006)

  21. 21.

    Developmental Plasticity and Evolution (Oxford University Press, 2003)

  22. 22.

    & Growth, seasonality, and lizard life histories: age and size at maturity. Oikos 77, 267–278 (1996)

  23. 23.

    et al. Multi-scale approach to understanding climate effects on offspring size at birth and date of birth in a reptile. Integr. Zool. 5, 164–175 (2010)

  24. 24.

    & 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)

  25. 25.

    & Evolution of “determinants” in sex determination: a novel hypothesis for the origin of environmental contingencies in avian sex-bias. Semin. Cell Dev. Biol. 20, 304–312 (2009)

  26. 26.

    et al. Climate effects on offspring sex ratio in a viviparous lizard. J. Anim. Ecol. 78, 84–90 (2009)

  27. 27.

    et al. Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus. J. Exp. Zool. 305A, 74–82 (2006)

  28. 28.

    & Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lyosomaniae). Biol. J. Linn. Soc. 70, 667–680 (2000)

Download references

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.

Author information

Author notes

    • Barbara Feldmeyer

    Present address: Biodiversity and Climate Research Centre (BiK-F), Siesmayerstrasse 70A, D-60325 Frankfurt and Main, Germany.

Affiliations

  1. Theoretical Biology Group, University of Groningen, PO Box 14, 9750 AA Haren, the Netherlands

    • Ido Pen
    • , Barbara Feldmeyer
    •  & Anna Harts
  2. Edward Grey Institute, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • Tobias Uller
  3. School of Zoology, Private Bag 5, University of Tasmania, Hobart 7001, Tasmania, Australia

    • Geoffrey M. While
    •  & Erik Wapstra

Authors

  1. Search for Ido Pen in:

  2. Search for Tobias Uller in:

  3. Search for Barbara Feldmeyer in:

  4. Search for Anna Harts in:

  5. Search for Geoffrey M. While in:

  6. Search for Erik Wapstra in:

Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ido Pen.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text, additional references, Supplementary Tables 1-3 and Supplementary Figures 1-6 with legends.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature09512

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.