Evolutionary stability inferred for a free ranging lizard with sex‐reversal

Abstract

The sex of vertebrates is typically determined genetically, but reptile sex can also be determined by developmental temperature. In some reptiles, temperature interacts with genotype to reverse sex, potentially leading to transitions from a chromosomal to a temperature‐dependent sex determining system. Transitions between such systems in nature are accelerated depending on the frequency and fitness of sex‐reversed individuals. The Central Bearded Dragon, Pogona vitticeps, exhibits female heterogamety (ZZ/ZW) but can have its sex reversed from ZZ male to ZZ female by high incubation temperatures. The species exhibits sex‐reversal in the wild and it has been suggested that climate change and fitness of sex‐reversed individuals could be increasing the frequency of reversal within the species range. Transitions to temperature‐dependent sex determination require low levels of dispersal and high (>50%) rates of sex‐reversal. Here, we combine genotype‐by‐sequencing, identification of phenotypic and chromosomal sex, exhaustive field surveys, and radio telemetry to examine levels of genetic structure, rates of sex‐reversal, movement, space use, and survival of P. vitticeps in a location previously identified as a hot spot for sex‐reversal. We find that the species exhibits low levels of population structure (FST ~0.001) and a modest (~17%) rate of sex‐reversal, and that sex‐reversed and nonsex‐reversed females have similar survival and behavioural characteristics to each other. Overall, our data indicate this system is evolutionary stable, although we do not rule out the prospect of a more gradual transition in sex‐determining mechanisms in the future in a more fragmented landscape and as global temperatures increase.

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…If their altered behaviour also affects their microhabitat use or results in changed activity during the breading season, these individuals might be harder to find by conventional capturing methods. There is currently very little information on the survival and behaviour of sex-reversed individuals in nature (Wild et al, 2022), so testing the above ideas will require further research.…”

Metabolic consequences of sex-reversal in two lizard species: a test of the like genotype and like phenotype hypotheses

“…Although we did not detect a significant difference in survivorship, in both species, sex-reversed hatchlings had a higher frequency of mortality over a 6-month period than the other sexes. High mortality has been previously observed in sex-reversed individuals in laboratory experiments (Mikó et al, 2021) and in the wild (Wild et al, 2022). Further investigation is required to understand the cause of this low survivorship and the demographic consequences these results have for the emergence of sex-reversal (Cotton & Wedekind, 2009).…”

“…For example, if larger phenotypic females have similar amounts of energy intake in the ZZ/ZW system, and all other aspects of the energy budget are the same, femaleSR ZZ would have more residual energy than female ZW to allocate to production and activity after resting metabolic costs have been paid. However, these "male-like" phenotypes may also be a selective disadvantage for femaleSR ZZ in the wild because femaleSR ZZ are known to have high mortality and lower fecundity rates than female ZW (Wild et al, 2022). Different strategies of energy allocation between ZZ and ZW individuals across ontogeny may explain previously observed differences in morphology and behaviours as adults.…”

“…Sex-reversal in B. duperreyi occurs when chromosomal females (female XX) develop male phenotypes [maleSR XX] (Dissanayake, Holleley, Deakin, et al, 2021;Quinn et al, 2009), whereas sex-reversal in P. vitticeps occurs when chromosomal males (male ZZ) develop female phenotypes [femaleSR ZZ] (Holleley et al, 2015;Quinn et al, 2007). In both species, this phenomenon has been documented in the wild (Dissanayake et al, 2020;Holleley et al, 2015;Wild et al, 2022), with evidence indicating both species are sensitive to climate change Holleley et al, 2015;Schwanz et al, 2020). Similarities between phenotypic forms (femaleSR ZZ and female ZW in P. vitticeps; or maleSR XX and male XY in B. duperreyi) in these traits would suggest a lack of fitness differences imparted by sex-reversal, while similarities between genotypic forms (femaleSR ZZ and male ZZ in P. vitticeps; or maleSR XX and female XX in B. duperreyi) would indicate the potential for differences in fitness between discordant and concordant sex.…”

Corrigendum

“…The authors would like to acknowledge an error in the article entitled “Evolutionary stability inferred for a free ranging lizard with sex‐reversal” which was published in Molecular Ecology (Volume 31, Issue 8, Pages 2281–2292; 2022).…”