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Mechanisms underlying intraspecific divergence in sex determination in Carinascincus ocellatus

Hill, P ORCID: 0000-0002-6190-6426 2021 , 'Mechanisms underlying intraspecific divergence in sex determination in Carinascincus ocellatus', PhD thesis, University of Tasmania.

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Abstract

The division of individuals into separate sexes is ancient and near-ubiquitous in sexually reproducing organisms. However, sex determination, the switch that controls this division is diverse and subject to ongoing research. Sex can be determined by genes on sex chromosomes, known as genetic sex determination, GSD; or by the environment, often by temperature, known as temperature dependent sex determination, TSD. GSD is either male heterogametic, i.e. XX females and XY males such as in mammals, or female heterogametic, ZZ males and ZW females such as in birds. Mammals and birds possess ancient, conserved systems of genetic sex determination. However, sex determination is both more diverse and more labile in reptiles, with multiple and often recent evolutionary transitions and this is epitomised in lizards. Within lizards there are species with GSD – both XY and ZW heterogamety – and TSD. However, many lizard groups also combine genes and temperature to determine sex and the mechanisms of sex determination occur along a continuum. Understanding how transitions between TSD and GSD, and within GSD how transitions between XY and ZW heterogamety occur remains a major challenge in evolutionary biology.
In this thesis I use the viviparous Tasmanian spotted snow skink, Carinascincus ocellatus (formerly Niveoscincus), an extraordinary example of a species exhibiting incipient divergence in sex determination to understand the mechanisms that underpin evolutionary transitions in sex determination. Long term data on this species shows that in a high elevation population, sex ratios do not deviate from parity regardless of temperature, suggesting GSD. In a low elevation population, sex ratios correlate with developmental temperature and males are favoured in cool temperatures while females are favoured in warm temperatures implicating a strong role of temperature in sex determination. Warmer temperatures at low elevation result in an extended activity season which benefits females. Females that are born early in this population mature early and therefore have a higher lifetime reproductive output. Cooler temperatures and short activity seasons at high elevation means there are no sex specific benefits associated with birthdate. Building on this work by combining long-term field data, next generation sequencing, traditional cytogenetic and population genetics approaches and experimental manipulation I explored the mechanisms operating during early stages of within species incipient transitions in sex determination.
Specifically, I a) examined similarities and differences in sex-linked genetic sequences between the populations, b) identified the sex chromosomes in C. ocellatus and described both population-level and species level differences, c) investigated the role of temperature in determining sex in both populations and d) estimated the age of the divergence between the two populations and the amount of gene flow occurring since the divergence. I found that a) C. ocellatus has XY (male) heterogamety with sex-linked genetic sequence common to both populations in addition to population-specific sex-linked sequence, and evidence that recombination among sex chromosomes has been more disrupted in the high elevation population, b) the homomorphic X and Y chromosomes in both populations of C. ocellatus are chromosome pair seven, there are small differences between the Y chromosomes of each population, and sex chromosomes in some Scincid lineages likely evolved independently c) temperature influences sex determination in both populations of C. ocellatus by overriding the genetic signal to produce individuals with a sexual phenotype / genotype mismatch despite population-specific response of the sex ratio to temperature and d) high and low elevation populations of C. ocellatus diverged less than 900,000 years ago during the glacial cycles of the Pleistocene with no gene flow occurring between these populations since.
My thesis builds and expands on existing knowledge of sex determination transitions and provides a solid basis for understanding the mechanisms involved. In addition, this thesis provides a novel interpretation of the C. ocellatus system and the incipient transition in sex determination, and highlights that such transitions occur frequently because the changes to the genome that are required are minor and very little evolutionary time is needed for these changes to become apparent on the sex chromosomes and in the phenotype.

Item Type: Thesis - PhD
Authors/Creators:Hill, P
Keywords: Sex determination, cryptic sex chromosomes, karyotype, GSD, TSD, reptile
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Copyright 2021 the author

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