Sex reversal in the alpine skink Bassiana duperreyi : response to natural environment

  • Duminda Dissanayake Mudiyanselage

    Student thesis: Doctoral Thesis

    Abstract

    Global climatic change has significant impacts on several aspects of the biology and ecology of many reptile species on earth, which in some cases has led to population declines or other severe threats. Until now, however, such impacts have not been reviewed for many reptiles, even though these species are often at the critical stage at the conservation priorities. Changing temperature is increasingly being considered one of the major threats for reptiles, especially for species where temperature extremes can influence the outcome of sex determination. In reptiles, sex can be determined genetically (genotypic
    sex determination or GSD) or environmentally, depending on their incubation temperature (temperature sex determination or TSD). Typically, the two alternatives of sex determination were thought to be incompatible and were never observed in the same species, however sex reversal of some GSD species under extreme environmental conditions, confirmed in wild populations, has revealed that intermediate states are possible. Sex determination in the endemic Australian skink Bassiana duperreyi is influenced by both genetic factors and nest temperature. The discordance between genotypic and phenotypic was observed definitively in the laboratory conditions. Whether sex reversal occurs in natural nests and whether sex-reversed individuals survive to adulthood in wild populations is unknown. Furthermore, it is unclear whether the interaction of sex reversal of male XX individuals under low temperatures occurs at a rate sufficient to trigger loss of the Y chromosome and evolutionary transitions between GSD and TSD. To address these questions in the wild population of B. duperreyi, we first developed reliable molecular techniques to identify sex reversal male (XX) from normal male (XY), is known as in silico whole-genome subtraction. We used this technique to isolate seven Y chromosome specific markers for B. duperreyi. In chapter 3, using these markers, we demonstrated that sex reversal in the wild for the first time in adults of a reptile species with XX/XY sex determination. The highest frequency of sex reversal occurred at the highest coolest elevation location, Mt Ginini (18.46%) and decreased in frequency to zero with decreasing elevation. We model the impact of this under Fisher’s frequency-dependent selection to show that, at the highest elevations, populations risk the loss of the Y chromosome and a transition to temperature-dependent sex determination. We also applied our Y chromosome markers to hatchlings, in chapter 5, similar to what we discovered in adults, we discovered that the levels of sex reversal in nests of B. duperreyi, ranged from 28.6% at the highest, coolest locations to zero at the lowest, warmest locations. Further, we observed that the constant temperature equivalent in wild nests dropped below the 20°C during the thermosensitive period, for even for a short time during the incubation period, sex reversal was observed. Therefore, extreme cold temperature events might lead to 100% sex reversal of the XX genotype in the alpine populations. The variation in the frequency of sex reversal in B. duperreyi as a phenotypic response to environmental temperature with altitude, and early work using mtDNA has raised the possibility that underlying phylogenetic history may be confounding interpretation of variation in the frequency of sex reversal with elevation. To test this, in chapter 4, we examined the underlying genetic structure within the geographic wide populations on its distribution used single nucleotide polymorphisms (SNP) generated by reduced representation sequencing. We generated 12,532 reliable polymorphic SNP loci from 60 populations (263 individuals) covering the distribution of B. duperreyi to assess geneflow and to define population structure in the form of diagnosable lineages. We identified five well-supported diagnosable operational taxonomic units (OTUs) within B. duperreyi. Low levels of divergence of B. duperreyi between mainland Australia and Tasmania (no fixed allelic differences) support the notion of episodic exchange of alleles across Bass Strait (ca 60 m, 25 Kya) during periods of low sea level during the Upper Pleistocene rather than the much longer period of isolation (1.7 My) indicated by earlier studies using mitochondrial sequence variation. Our study provides foundational work for the detailed taxonomic re-evaluation of this species complex and the need for biodiversity assessment to include an examination of cryptic species and/or cryptic diversity below the level of species. This thesis contributes to our understanding of the risks of population demography due to climate change in species subject to sex reversal by temperature, and sex reversal in this alpine skink makes it a sensitive indicator of climate change, both in terms of changes in average temperatures, and in terms of climatic variability will provide focus for future research to test on-the-ground management strategies to mitigate the effects of climate in local populations. Further, we provide evidence that sex reversal by cool temperatures in B. duperreyi occurs in the wild, influences the sexual genotypes-phenotype combinations in adult populations, and is as such a potential means of rapid evolutionary responses to climate change.
    Date of Award2022
    Original languageEnglish
    SupervisorClare Holleley (Supervisor), Janine Deakin (Supervisor) & Arthur Georges (Supervisor)

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