Evolutionary history, population genomics and epigenomics, and conservation consequences for European whitefish

Crotti, Marco (2020) Evolutionary history, population genomics and epigenomics, and conservation consequences for European whitefish. PhD thesis, University of Glasgow.

Abstract

Understanding the mechanisms behind species adaptation and differentiation is a major undertaking in evolutionary biology, particularly in light of advancing threats to biodiversity. Studying species whose current distribution was heavily influenced by glacial periods represent an ideal system to disentangle the effect of historical contingency and demographic history from evolutionary forces, and can provide important clues on how populations can deal with environmental change in the long term. However, there is also a dire need for research focusing on adaptation occurring in a much shorter time scale, as to help conservationists protect endangered populations from fluctuating environmental conditions. This PhD aimed to shed light on the processes of differentiation and adaptation in the European whitefish Coregonus lavaretus in Scotland, focussing on a natural, glacial time scale, and a man-made, recent translocation.

In Britain, European whitefish is one of the rarest freshwater species, is considered a glacial relict and presents a patchy distribution across Scotland, England, and Wales. While several studies have focused on the relationship between the British populations, it is still unclear how British population are related to continental European ones, in particular to the three mitochondrial DNA clades previously identified, and whether they come from the same origin. Using a genomic dataset and samples from all seven native British populations and four mainland European and Russian ones, I aimed to reconstruct the evolutionary history and to discern the demographic and evolutionary forces underpinning divergence between British populations. I find lower genetic diversity in the Scottish populations and high differentiation (FST = 0.433 – 0.712) with the British and other European populations. I also find evidence of separate postglacial colonisation of Britain, with the Scottish populations having been separated from the Welsh and English populations for more than 50 Ky. Differentiation was elevated genome-wide, rather than in particular genomic regions, suggesting genetic drift due to the long isolation of the Scottish populations as the main driver of differentiation. In addition, there was discordance between the nuclear and mitochondrial DNA data at the European scale, with the previously reported northern and southern mtDNA clades not being supported by nuclear data. These findings indicate neutral processes and historical contingency to be the drivers of genomic divergence in British populations of European whitefish and shed new light on the establishment of the native British freshwater fauna after the last ice age.

Epigenetic processes are one of the mechanisms that can generate phenotypic plasticity, and therefore are particularly relevant to study rapid adaptation. Using a single method to extract genomic and epigenomic information is much more efficient, cheaper and more timesaving than using two separate approaches, which is usually what has been done to date. In Chapter 3, I assessed the possibility of using epiRADseq, a technique originally developed for the study of DNA methylation, to extract genomic SNPs, so that the data obtained from one technique could be used for both genomic and epigenomic analyses. I used previously published data on coral, and generated new data on European whitefish to compare the number of SNPs retained, population genetic summary statistics, and population genetic structure between data drawn from ddRADseq, the genomic equivalent, and epiRADseq library preparations. I showed that SNPs obtained from epiRADseq are highly similar to those from ddRADseq and are equivalent for estimating genetic diversity and population structure. This finding is particularly relevant to researchers interested in genetics and epigenetics on the same individuals because using a single epigenomic approach to generate two datasets greatly reduces the time and financial costs compared to using these techniques separately.

In Scotland, the European whitefish Coregonus lavaretus, is natively present in only two lakes and is suffering steep declines, and six refuge populations were established over the last 30 years as a conservation measure. This represents an ideal system to gain an insight into the processes of differentiation and adaptation at the first stages of population divergence. To do so, I used a combination of morphological, genomic and epigenomic analyses. I found a significant difference in body shape and linear traits between source and refuge populations, and convergence in body shape between refuge populations derived from different source populations. Analyses of genome-mapped SNPs showed significant FST divergence between source and refuge populations, increased inbreeding and relatedness, and reduced genetic diversity in the refuge populations. Using two separate approaches, I found genomic outliers associated with the translocations, located within or near genes involved in the immune and nervous system, and hepatic functions. DNA methylation analysis showed that refuge populations tended to be differentially methylated from the source in the same genomic regions, and identified many loci having distinct methylation signal between source and refuge populations. Finally, I found some evidence of epigenetic variation having a stronger correlation with phenotypic variation in more recently translocated populations, and genetic variation a stronger correlation with phenotypic variation in the older translocated populations, suggesting different adaptation mechanisms as time since establishment increases. These results suggest that translocations to new environments can affect evolutionary potential by impacting both genetic and epigenetic components of diversity.

In conclusion, this research increases our understanding of the interplay between historical contingency and evolutionary forces in the process differentiation and adaptation at different stages of population divergence. In particular, the distinct evolutionary history of European whitefish populations in Britain and the rapid divergence observed between source and refuge populations in Scotland have profound implications for the conservation of this species.

• Item Type: Thesis (PhD)
• Qualification Level: Doctoral
• Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
• Supervisor's Name: Elmer, Prof K and Adams, Prof C
• Date of Award: 2020
• Embargo Date: 10 December 2023
• Depositing User: Dr M Crotti
• Unique ID: glathesis:2020-81853
• Copyright: Copyright of this thesis is held by the author.
• Date Deposited: 10 Dec 2020 11:15
• Last Modified: 08 Apr 2022 17:04
• Thesis DOI: 10.5525/gla.thesis.81853
• URI: https://theses.gla.ac.uk/id/eprint/81853

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