Letter | Published:

Sex reversal triggers the rapid transition from genetic to temperature-dependent sex

Nature volume 523, pages 7982 (02 July 2015) | Download Citation


Sex determination in animals is amazingly plastic. Vertebrates display contrasting strategies ranging from complete genetic control of sex (genotypic sex determination) to environmentally determined sex (for example, temperature-dependent sex determination)1. Phylogenetic analyses suggest frequent evolutionary transitions between genotypic and temperature-dependent sex determination in environmentally sensitive lineages, including reptiles2. These transitions are thought to involve a genotypic system becoming sensitive to temperature, with sex determined by gene–environment interactions3. Most mechanistic models of transitions invoke a role for sex reversal3,4,5. Sex reversal has not yet been demonstrated in nature for any amniote, although it occurs in fish6 and rarely in amphibians7,8. Here we make the first report of reptile sex reversal in the wild, in the Australian bearded dragon (Pogona vitticeps), and use sex-reversed animals to experimentally induce a rapid transition from genotypic to temperature-dependent sex determination. Controlled mating of normal males to sex-reversed females produces viable and fertile offspring whose phenotypic sex is determined solely by temperature (temperature-dependent sex determination). The W sex chromosome is eliminated from this lineage in the first generation. The instantaneous creation of a lineage of ZZ temperature-sensitive animals reveals a novel, climate-induced pathway for the rapid transition between genetic and temperature-dependent sex determination, and adds to concern about adaptation to rapid global climate change.

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Primary accessions


Data deposits

The W chromosome sequence has been deposited in GenBank under accession number KM508988.


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We thank the following persons and institutions: W. Ruscoe and J. Richardson (animal husbandry); A. Quinn, M. Young and J. Richardson (field collections); A. Kilian and Diversity Arrays Technology (SNP genotyping); A. Livernois (sequencing assistance); B. Gruber and N. Garlapati (geographic information system); A. T. Adamack (modelling advice); A. Dobos and P. E. Geertz (graphic design); J. Deakin, R. Thompson and the Kioloa Science Writers Workshop (revisions of the manuscript). We particularly thank reviewer J. J. Bull for suggesting the modelling approach in Extended Data Fig. 4. Funding was from Australian Research Council Discovery Grant DP110104377 to A.G. and T.E. This research was conducted under appropriate approvals from the Victorian, New South Wales and Queensland authorities, and with approvals from the Animal Ethics Committee of the University of Canberra.

Author information

Author notes

    • Kazumi Matsubara
    •  & Bhumika Azad

    Present addresses: Research Center for Aquatic Genomics, National Research Institute of Fisheries Science, Fisheries Research Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan (K.M.); John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory 2601, Australia (B.A.).


  1. Institute for Applied Ecology, University of Canberra, Canberra, Australian Capital Territory 2601, Australia

    • Clare E. Holleley
    • , Denis O'Meally
    • , Stephen D. Sarre
    • , Jennifer A. Marshall Graves
    • , Tariq Ezaz
    • , Kazumi Matsubara
    • , Bhumika Azad
    • , Xiuwen Zhang
    •  & Arthur Georges
  2. School of Life Science, La Trobe University, Melbourne, Victoria 3086, Australia

    • Jennifer A. Marshall Graves


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C.E.H. and A.G. designed the study. C.E.H. conducted breeding experiments, egg incubations, parentage SNP analysis and prepared figures. D.O'M. collected the animals from the field. C.E.H. and X.Z. conducted the molecular sex testing. B.A. and K.M. undertook the cytogenetic analysis and prepared extended data figures, under the supervision of T.E. A.G. and C.E.H. undertook the statistical analyses and A.G. conducted the modelling of ZW genotype frequency with temperature. All authors contributed to writing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Clare E. Holleley or Arthur Georges.

Extended data

Supplementary information

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    Supplementary Information

    This file contains Supplementary Tables 1-4.

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    Supplementary data

    This file contains the source data used to make Supplementary Table 1.

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