Evolving thermal thresholds explain the distribution of temperature sex reversal in an Australian dragon lizard

Abstract

Aim Species with temperature‐dependent sex determination (TSD) are particularly vulnerable to climate change because a resultant skew in population sex ratio can have severe demographic consequences and increase vulnerability to local extinction. The Australian central bearded dragon (Pogona vitticeps) has a thermosensitive ZZ male/ZW female system of genetic sex determination (GSD). High incubation temperatures cause reversal of the ZZ genotype to a viable female phenotype. Nest temperatures in the wild are predicted to vary on a scale likely to produce heterogeneity in the occurrence of sex reversal, and so we predict that sex reversal will correlate positively with inferred incubation conditions. Location Mainland Australia. Methods Wild‐caught specimens of P. vitticeps vouchered in museum collections and collected during targeted field trips were genotypically and phenotypically sexed to determine the distribution of sex reversal across the species range. To determine whether environmental conditions or genetic structure can explain this distribution, we infer the incubation conditions experienced by each individual and apply a multi‐model inference approach to determine which conditions associate with sex reversal. Further, we conduct reduced representation sequencing on a subset of specimens to characterize the population structure of this broadly distributed species. Results Here we show that sex reversal in this widespread Australian dragon lizard is spatially restricted to the eastern part of the species range. Neither climatic variables during the inferred incubation period nor geographic population genetic structure explain this disjunct distribution of sex reversal. The main source of genetic variation arose from isolation by distance across the species range. Main conclusions We propose that local genetic adaptation in the temperature threshold for sex reversal can counteract the sex‐reversing influence of high incubation temperatures in P. vitticeps. Our study demonstrates that complex evolutionary processes need to be incorporated into modelling biological responses to future climate scenarios.

With or Without W? Molecular and Cytogenetic Markers are Not Sufficient for Identification of Environmentally-Induced Sex Reversal in the Bearded Dragon

“…Notably, all 28 animals with the mismatch were phenotypic females and they were recorded only in the south-western part of the Sex Dev 2021;15:272-281 DOI: 10.1159/000514195 species range. While this clustered distribution is consistent with non-random occurrence of sex reversals in certain environmental conditions at the edge of the species distribution as interpreted by Castelli et al [2020], the spatial clustering can also reflect the geographic spread of a mutation, recombination, or other rearrangement concerning the region of the W chromosome containing the otherwise female-specific marker used for identification of the individuals with the mismatch. The current study discloses that the given marker might not be as reliable as thought for identification of sex-reversed individuals in the field and that the causes of the mismatch between the phenotypic and genotypic sex should be investigated more rigorously.…”

“…Sex-reversed animals identified by molecular and cytogenetic markers were reported in the bearded dragon also in the field, and their slightly higher incidence in recent years was put into connection with global warming [Holleley et al, 2015]. In the recent study [Castelli et al, 2020], the mismatch between phenotypic and genotypic sex was assigned by the same molecular marker [Quinn et al, 2010;Holleley et al, 2015;Ehl et al, 2017] (all these studies used the same contig as the sex-specific marker although they differed in the primers used for amplifications of fragments from the same W-linked regions) and was found in 5% out of 534 examined individuals of P. vitticeps covering the whole species range. Notably, all 28 animals with the mismatch were phenotypic females and they were recorded only in the south-western part of the Sex Dev 2021;15:272-281 DOI: 10.1159/000514195 species range.…”

“…This species became a popular pet worldwide [Cogger, 1992;De Vosjoli et al, 2016]. During a genetic screening of captive bred central bearded dragons and the previous experiment with sex-reversed individuals [Ehl et al, 2017], we uncovered a male with a mismatch between the phenotypic sex and the genotype: it possessed a female-specific allele in the locus assigned as 'contig C' by Quinn et al [2010], serving as a sex-specific PCR marker previously used for detection of sex-reversed individuals in this species [Quinn et al, 2010;Holleley et al, 2015;Ehl et al, 2017;Castelli et al, 2020]. The W-specific fragment represents an anonymous sequence which differs in 4 single nucleotide polymorphisms (SNPs) from the homologous Z-linked locus [Quinn et al, 2010].…”

“…At a population level, the derived ESD could then potentially sweep out GSD and become fixed in a population. Sex-reversed animals identified by molecular and cytogenetic markers were reported in the central bearded dragon also in the field [Holleley et al, 2015;Castelli et al, 2020], and their higher incidence in recent years is thought to be in connection with global warming [Holleley et al, 2015]. While the scenario of a climate changedriven transition in sex determination in the central bearded dragon sounds theoretically appealing, here we show that both cytogenetic and molecular genetic markers used for the demonstration of the occurrence of sex reversal in the field in this species are not sufficient for detection of sex reversals, hence evidence for sex-reversed animals in wild populations is not very strong.…”

Ovotestes suggest cryptic genetic influence in a reptile model for temperature-dependent sex determination

“…These differences in thresholds can subsequently shift an individual embryo's propensity for developing as one sex or the other at a given temperature, which can create sex ratio biases, such as those we observed in A. muricatus [42][43][44][45]. We argue that such genetic variation in thermal thresholds likely exists alongside other genotypic determinants of sex in A. muricatus, so explaining the variation observed in both sex ratios and ovotestes frequency at different incubation temperatures [46]. This is akin to observations in close relative, P. vitticeps, where rates of sex reversal increase as temperature increases, though some Table 1.…”