The maternal influence on fitness correlates in a lizard with sex reversal

Abstract

Sex in vertebrates is typically understood to follow two primary modes of sex determination: genotypic sex determination and environmental sex determination. In genotypic sex determination (GSD), the genes that trigger sex differentiation are located on sex-specific chromosomes and are typically either male heterogametic (XX female and XY male) or female heterogametic (ZZ male and ZW female). Organisms with environmental sex determination (ESD) have no sex chromosomes, and the presence of an environmental cue (e.g., temperature) triggers sexual differentiation. Despite this conceptual dichotomy in sex determination, several lineages of vertebrates with GSD have shown a temperature override of sexual differentiation pathways producing sex-reversed individuals. These sex-reversed individuals have a mismatched sexual genotype and phenotype (e.g., ZZ female). Within reptiles, several species have exhibited sex reversal under laboratory and natural conditions, and it has been proposed that the propensity for sex reversal may partly explain the multiple evolutionary transitions between GSD and ESD (in the form of temperature-dependent sex determination (TSD)) seen in this taxon. Identifying how or if sex reversal influences fitness related traits of a species is critical to understanding how modes of sex determination evolve or persist in a population. Here, I use a combination of laboratory and field-based studies to understand the consequences of sex reversal in the Central Bearded Dragon lizard (Pogona vitticeps) by 1) quantifying reproductive output and the propensity to sex reverse between captive concordant and sex-reversed females; 2) quantifying morphology, growth, survival, and locomotor performance of the offspring of both concordant and sex-reversed females; 3) quantifying the nesting behaviours of free-ranging P. vitticeps, and 4) using predictive models to understand the relative risk of sex reversal. Using a captive colony of P. vitticeps, I measured the reproductive rate of concordant (ZW) and sex-reversed (ZZ) females across two reproductive seasons and analysed historical data. I found that sex-reversed females produce fewer eggs per reproductive season than concordant females. This is contrary to previous published findings. I show that one hyper-fecund, sex-reversed female drove the results from the previous study. Additionally, I note that the pivotal temperature for offspring of concordant mothers is lower than previously suggested and not significantly different than sex-reversed mothers. I also found that sex-reversed females produce larger eggs suggesting that there may be a trade-off between reproductive rate and egg size. These results suggest that sex reversal does not provide a reproductive advantage. Then, I used the offspring produced from the previous study to quantify fitness-related phenotypes. I found that offspring of sex-reversed mothers are larger with better body condition at hatching than those of concordant mothers, but this difference dissipates quickly after hatching. Maternal sex genotype did not influence growth, survival, performance, or critical thermal limits. However, developmental temperatures did influence locomotor performance as well as the critical thermal minimums of offspring. The larger size at hatching afforded to offspring of sex-reversed mothers may provide an advantage allowing survival to adulthood increasing the persistence of sex reversal in a population. I next used free-ranging, concordant female P. vitticeps to quantify nesting behaviours and nest site microclimate variables. I provide the first documentation of the nesting ecology in this species. Although sample sizes were relatively low, I found that nesting concordant females chose open canopy locations but varied the depth of their nests across the reproductive season, which alters the temperatures experienced by the developing embryos. I show that late season nests have a higher risk of sex reversal than early nests. So far, sex reversal has only been documented in approximately 24 percent of the range of P. vitticeps, while ambient temperatures suggest that sex reversal should extend well beyond. To address my final aim, I deployed temperature loggers and collected microhabitat data from open and shaded potential nest sites at eight locations to determine the relative risk of sex reversal across the species’ range. I used these data to test the accuracy of and then inform the microclimate model NicheMapR (Shiny app interface) to predict the risk of sex reversal at these point locations. I found that areas where no sex reversal has been recorded may have refugia that allow females to mitigate the risk of sex reversal. Furthermore, I show that open canopy areas where sex reversal has been documented may be at the greatest risk if females continue to choose open canopy nest sites. Overall, my research suggests a change in the perception of sex reversal in P. vitticeps in the context of evolutionary transitions. Sex reversal does not convey a reproductive advantage, nor does it provide much of an advantage past hatching. Although free-ranging females choose nest sites that may induce sex reversal late in the reproductive season, they may be able to mitigate the risk of sex reversal by altering their behaviours or shifting their reproductive phenology. In full, the phenotypes associated with sex reversal in P. vitticeps alone are unlikely to provide the momentum to advance this species towards a transition in mode of sex determination.

Date of Award	2023
Original language	English
Supervisor	Stephen Sarre (Supervisor) & Janine DEAKIN (Supervisor)