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

Nature volume 523, pages 79–82 (2015)Cite this article

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Abstract

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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Figure 1: Geographical distribution of sex reversal in wild populations of P. vitticeps.
Figure 2: Offspring sex ratio as a function of egg incubation temperature in P. vitticeps.
Figure 3: Rate of sex reversal as a function of egg incubation temperature in P. vitticeps.

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GenBank/EMBL/DDBJ

Data deposits

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

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Acknowledgements

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.

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Author notes

  1. Kazumi Matsubara & Bhumika Azad

    Present address: †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.).,

Authors and Affiliations

  1. Institute for Applied Ecology, University of Canberra, Canberra, 2601, Australian Capital Territory, 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, 3086, Victoria, Australia

    Jennifer A. Marshall Graves

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Contributions

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.

Corresponding authors

Correspondence to Clare E. Holleley or Arthur Georges.

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Extended data figures and tables

Extended Data Figure 1 C-banded P. vitticeps chromosomes.

a, Mitotic metaphase chromosomes of a ZW control female individual. Arrowhead indicates the presence of a W chromosome identified by dense black staining of a single microchromosome. b, Mitotic metaphase chromosomes of a female putative ZZ sex-reversed individual. No evidence of a W chromosome was detected. c, Mitotic metaphase chromosomes of a control ZZ male individual. No evidence of a W chromosome was detected. Scale bar, 10 μm.

Extended Data Figure 2 Comparative genomic hybridization in P. vitticeps.

Genomic DNA was labelled by nick translation incorporating SpectrumGreen-dUTP for males and SpectrumOrange-dUTP for females. a, Mitotic metaphase chromosomes of a ZW control female individual. Arrowhead indicates the presence of a single W microchromosome identified by the enriched orange fluorescence of female specific genomic DNA labelled with SpectrumOrange-dUTP. b, Mitotic metaphase chromosomes of a female putative ZZ sex-reversed individual. No evidence of a W chromosome was detected. c, Mitotic metaphase chromosomes of a control ZZ male individual. No evidence of a W chromosome was detected. d–f, DAPI staining of the same metaphases, control ZW female, sex-reversed ZZ female and control ZZ male, respectively. Scale bar, 10 μm.

Extended Data Figure 3 Physical mapping of a W-chromosome-linked microsatellite motif in P. vitticeps.

a, Mitotic metaphase chromosomes of a ZW control female individual. Arrowhead indicates the presence of a W chromosome identified by a strong hybridization of (AAGG)8-Cy3 florescence (orange) on a single microchromosome. b, Mitotic metaphase chromosomes of a female putative ZZ sex-reversed individual. No evidence of a W chromosome was detected. c, Mitotic metaphase chromosomes of a control ZZ male individual. No evidence of a W chromosome was detected. d–f, DAPI staining of the same metaphases, control ZW female, sex-reversed ZZ female and control ZZ male, respectively. Scale bar, 10 μm.

Extended Data Figure 4 Modelling the decline of the ZW genotype resulting from frequency-dependent selection.

Frequency of the ZW genotype declines precipitously with increasing incubation temperature. Our wild population (shown in red, 14.3% sex reversal) resides on the precipice between GSD and TSD and requires only a small change in environmental temperature to precipitate loss of the W chromosome.

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Holleley, C., O'Meally, D., Sarre, S. et al. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523, 79–82 (2015). https://doi.org/10.1038/nature14574

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