Changing sex with changing climate: mechanisms and consequences of divergence in sex determination across a glaciated landscape (APSF 17-8)

APSF 17-8 | Amount: $ 44,400 | Project Leader: E Wapstra | Project Period: Jul 2017 - Jul 2020

A project undertaken at the University of Tasmania in conjunction with the University of Canberra and led by Erik Wapstra, Chris Burridge and Tariq Ezaz

The global aim of our project was to understand the transitions between sex determination systems in snow skinks across the Tasmanian landscape and to model the impacts of long-term global climate change.

The division of individuals into separate sexes is ancient and 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 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. 

The prevailing paradigm was that sex determination in vertebrates is fixed within lineages. A series of recent papers in the past two decades have challenged this paradigm and we now understand that sex determination is highly labile in reptiles with evidence of multiple transitions between systems occurring. 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. Tasmanian snow skinks provide a rich research opportunity because within one species (Carinascincus ocellatus – photo supplied) there is divergence in how sex is determined – in warm lowland populations (photo supplied), temperature plays a pivotal role in influencing offspring sex.

Warm conditions during spring and summer (that is when females are pregnant) leads to a higher proportion of sons whereas cold conditions leads to a higher proportion of sons. In contrast, in cold subalpine sites (photo supplied) environmental temperature plays no role in sex determination. Thus, we appear to have a rare case of within species divergence in sex determination with TSD effects in some populations and GSD sex determination in others.

Overall, the project achieved its global aim to understand the transitions between sex determination systems in snow skinks across the Tasmanian landscape and to model the impacts of long-term global climate change. The project leveraged a long term field dataset that showed temperature effects in sex determination in warm lowland populations but no effects in cold highland populations suggesting the presence of incipient within species variation is sex determination. This was backed up by experimental and theoretical modelling which demonstrated the evolutionary and ecological scenarios under which this divergence may be selected.

This project then focussed on understanding the mechanism between this divergence including the evolutionary transitions in sex chromosomes, gene flow between populations, and the mechanism between temperature and sexual phenotype. We showed that i) our species has XY (male) heterogamety with shared sex-linked genetic sequence in 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, ii) the homomorphic X and Y chromosomes in both populations of C. ocellatus are chromosome pair seven, iii) there are small population-level differences between the X and Y chromosomes, and sex chromosomes in C. ocellatus likely arose independently, iv) 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 v) 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.

We also mapped responses to climate and made predictions of impacts of future climate change on a range of phenotypic outcomes (including distribution, birth dates, offspring sex ratios) as well as exploring the potential evolutionary outcomes of climate on sex determination. Climate change will result in earlier birth dates across the geographic range of this species, but the strength of the effects will depend on locality both because climate change is predicted to be variable across the landscape and because the effects we observed were also population-specific.

Ultimately, effects of climate and climate change on processes such as developmental rate (and their effect on birth dates) have very real potential to affect distribution. Ultimately, as the species currently has an upper distributional limit into the subalpine areas of Tasmania, warmer conditions will potentially allow invasion into higher alpine areas with potential consequences for range-restricted alpine specialist species.

This project provides a novel interpretation of the N. ocellatus system undergoing the very earliest stages in a sex determination transition 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.