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Title: The population genomic origins of ecological specialisation in salmonid fishes
Author: Jacobs, Arne
ISNI:       0000 0004 7427 3757
Awarding Body: University of Glasgow
Current Institution: University of Glasgow
Date of Award: 2018
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Understanding the origin of biodiversity is a central question in evolutionary biology. Ecological specialisation, including the repeated rapid and parallel evolution of ecological specialists (‘ecotypes’), is a major source of biodiversity. The parallel evolution of ecotypes in salmonid fishes, such as Arctic charr, brown trout and European whitefish, has resulted in extensive diversity in northern postglacial freshwater ecosystems. Despite their ecological diversity and importance for northern ecosystems, the knowledge on the genetic basis of ecological specialisation, the evolutionary history of adaptive divergence, and the factors shaping the underlying genetic architecture are still not well understood in salmonids. Over the last decade many studies have investigated the genetic basis of ecologically relevant phenotypic traits in a wide range of salmonid species using genetic mapping approaches. However, knowledge on the conservation of the genetic basis for particular traits, or suits of traits, across species is limited, mainly due to a lack of genomic resources. Similarly, little is known about the genomic architecture of phenotypic diversity within species, such as the organisation of species-specific quantitative trait loci across the genome and the frequency of potential pleiotropy or genetic linkage. To understand how conserved the genomic basis for particular traits is across species and how quantitative trait loci (QTL) are organised within the genome, we analysed the genetic basis for a wide range of phenotypic traits (N=18) in six salmonid species using a dataset comprising of 943 QTL markers. We developed a novel analytical approach to analyse the colocalisation and synteny of QTL within and across species using a hetero-specific reference genome, in this case the Atlantic salmon (Salmo salar) genome. We found that QTL were not randomly distributed across the genome and that gene-density determined the distribution of QTL across chromosomes. By comparing QTL across species, we further identified genomic regions that were enriched for QTL for morphological and physiological traits (synteny blocks) in a range of species. Within three of the species, we also detected the significant colocalisation of QTL for different traits. Overall, the detection of synteny blocks and colocalised traits suggests a small but detectable role of pleiotropy and genetic linkage in trait evolution in salmonids and a conserved genetic basis for some traits across species. However, the observed patterns of conserved genetic basis and colocalisation were relatively weak, as QTL were mostly not conserved across species or colocalised within species. In general, the repeated evolution of similar ecotypes across populations and species implies a certain predictability of evolution. However, it is not well understood how phenotypic evolution overcomes the contingencies of heterogeneous genomic backgrounds of natural populations. To investigate the repeatability and predictability of parallel evolution, we used eco-morphological, genome-wide SNP and transcriptome data within and across lakes and evolutionary lineages of Arctic charr (Salvelinus alpinus). We found significant parallelism across replicated ecological specialists in foraging-associated traits. This phenotypic parallelism evolved despite population-specific variation in demographic histories, varying genomic response to selection and the non-parallel genetic basis of ecotype divergence. However, the regulatory molecular basis of ecological specialisation, inferred from gene expression and biological pathways, was highly parallel across ecotypes, bridging non-parallel genomic patterns and parallel eco-morphology. These findings suggest that parallel phenotypic evolution is possible despite non-parallel evolutionary routes when the functional molecular basis of ecological specialisation compensates for non-parallel genomic basis and histories. Evolutionary and genomic contingencies, such as demographic histories and genomic features can strongly influence the genomic architecture of adaptive divergence and reproductive isolation. To investigate how genomic features and demographic history influence the genetic architecture of adaptation and reproductive isolation, we reconstructed the demographic history and analysed the genetic architecture of divergence in brown trout (Salmo trutta) from the Maree Catchment in Scotland. Brown trout display reproductively isolated and divergent life histories and ecological specialisation, including a large piscivorous life-history form (ferox trout) and a smaller benthivorous life-history form. We found that ferox trout and benthivorous brown trout most likely diverged under a secondary contact of at least two distinct postglacial lineages and identified 33 genomic islands across the genome differentiating life-history forms. We demonstrated that some of these genomic islands formed under selection, and contained genes and biological pathways related to growth, development and immune response. Overall, we found strong genomic signals of divergence that were partially driven by selection on divergent phenotypes, and not only caused by genetic drift or through underlying genomic features, such as reduced recombination. The identification of the underlying evolutionary history and genetic architecture highlights the strength of genomic studies using species pairs for understanding the driving factors of adaptive divergence and reproductive isolation. Despite extensive knowledge on the genomic mechanisms underlying adaptive divergence over longer time scales and under the influence of phases of geographic isolation, less is known about the mechanisms underlying rapid ecological and phenotypic divergence. Rapid evolution plays an important role in the adaptation of species to human-induced environmental changes. However, it has been shown that in some cases human-driven environmental changes can lead to rapid loss of species and functional diversity, e.g. through species collapse and hybridization. Even though theoretical models predict that species can rapidly re-diverge under the right conditions following a species collapse and hybridization, the underlying mechanisms of rapid re-divergence remain to be elucidated. Empirical evidence for re-divergence following a species collapse is also lacking. We found evidence for the rapid evolution of ecologically-relevant phenotypic diversity in a European whitefish subspecies from Lake Constance, the gangfisch (Coregonus lavaretus macrophthalmus) after the recovery of pristine ecosystem conditions, following human-driven eutrophication, and speciation reversal. We found that a key functional trait, gill raker number, rapidly diversified within less than 10 generations following ecosystem recovery, allowing the use of vacant trophic niches. Variation in gill raker number is controlled by a sparse genetic architecture, as predicted by theory, and we further found evidence suggesting that introgression potentially provided the underlying adaptive variants. Several biological pathways that are known to be involved to ecological specialisation in fishes, such as metabolism, immune response and neural development, were identified based on coexpressed gene modules and genes under selection associated with gill raker number. Overall, our results demonstrate that functional diversity can rapidly re-emerge, given the right combination of genetic architecture, genetic diversity, and selection. In summary, this thesis demonstrates the evolutionary and genomic routes underlying phenotypic evolution and ecological specialisation in salmonid fishes. Comparing across different study systems, we find that secondary contact and historical gene flow played an important role in the evolution of salmonid species. Despite strong variation in the genomic basis of phenotypic traits across species and the genomic patterns of divergence across populations within species, we find some molecular parallelism across populations and species. Parallel ecotypes most likely evolved through parallel regulatory evolution and involvement of similar functional biological pathways. Furthermore, we find biological pathways that are repeatedly involved in adaptive divergence in different species. Overall, our results indicate that despite the flexibility of rapid and parallel phenotypic evolution on the genomic level, it is relatively conserved on the level of regulatory mechanisms and functional biological pathways.
Supervisor: Not available Sponsor: Not available
Qualification Name: Thesis (Ph.D.) Qualification Level: Doctoral
EThOS ID:  DOI: Not available
Keywords: QH Natural history ; QH301 Biology ; QH426 Genetics