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Adaptation genomics of trophic polymorphism

Final Report Summary - GEN ECOL ADAPT (Adaptation genomics of trophic polymorphism)

Summary: My research programme aims to identify the genetic foundations and environmental conditions that promote species diversity. Importantly, some lineages diversify rapidly and abundantly while others do not and I aim to disentangle some of the factors that underlie those asymmetries. I have an established programme of research on adaptive and evolutionary radiations of fishes because they provide an excellent comparative framework.
With my Career Integration Grant to the Institute of Biodiversity, Animal Health & Comparative Medicine at the University of Glasgow, I joined a research environment that has a long and strong history in fish biology complementary to my interests. This Marie Curie CIG project, GEN ECOL ADAPT, advanced my research effort on evolutionary potential through a comparative analysis of diversifying and non-diversifying populations of fishes, especially postglacial lake populations of salmonid fishes. This research has important implications for identifying the genetic basis of diversification in diverse populations of postglacial fishes, including those of high conservation and natural heritage value.
My project set two major pairs of Research & Integration Objectives for the duration of GEN ECOL ADAPT, with integration objectives woven into research objectives across two complementary projects. Here I summarise the results of the projects as abstracts.
Project 1. To identify the role of differential gene expression associated with divergence in trophic polymorphisms in fishes.
Salmonid fishes exhibit high levels of phenotypic and ecological variation and are thus ideal model systems for studying evolutionary processes of adaptive divergence and speciation. Furthermore, salmonids are of major interest in fisheries, aquaculture, and conservation research. Improving understanding of the genetic mechanisms underlying traits in these species would significantly progress research in these fields. We generated high quality de novo transcriptomes for four salmonid species: Atlantic salmon (Salmo salar), brown trout (Salmo trutta), Arctic charr (Salvelinus alpinus), and European whitefish (Coregonus lavaretus). All species except Atlantic salmon have no reference genome publicly available and few if any genomic studies to date. We used paired-end RNA-seq on Illumina to generate high coverage sequencing of multiple individuals. The final assemblies consisted of ~35k protein-coding transcripts for Atlantic salmon, brown trout, Arctic charr, and European whitefish and will be made publicly available. We further compare completeness and annotation statistics of our new assemblies to available related species, which demonstrated that our new data provided greater transcript length and transcriptome completeness than currently available resources. We found no phylogenetic bias with relation to transcript mapping, which simplified comparisons across subfamilies. Therefore this represents a useful contribution to the existing genomic resources for these species and provides valuable tools for future investigation of gene expression and sequence evolution in these and other salmonid species.
We conducted ecological transcriptomics analyses of natural populations of Arctic charr across replicate divergences in Scottish and Siberian lakes. We found that differences in gene expression were greater between trophically polymorphic sympatric populations than among individuals, which was an important step in demonstrating that these approaches provide useful ecological and evolutionary signal on ‘noisy’ collections. Few transcriptomics signals were shared across lakes though there was a stronger signal at the level of biological network. These findings contributed new understanding of the genomic basis of trophic polymorphism in fishes.
Project 2. A) To identify genetic polymorphisms under selection between trophically polymorphic fishes, and to determine the extent of linkage between genomic regions under selection.
Some of the most longstanding questions in evolutionary biology concern the origin of biodiversity and the ability of species to rapidly diversify in the face of gene flow. Fundamental to answering these questions is the ability to understand the extent to which evolution is predictable. To understand if parallel ecotypes evolved using parallel or non-parallel evolutionary routes, we examined phenotypic and population genomic patterns of replicated divergence in 19 Arctic charr (Salvelinus alpinus) populations from two evolutionary lineages (Atlantic and Siberian). We found that ecotypes show strong levels of phenotypic parallelism among populations within lineages, but differing levels of phenotypic parallelism among lineages. A population genomic analysis based on 648 individuals genotyped at ~200,000 loci from ddRADseq, revealed a pronounced speciation continuum, ranging from no neutral genetic divergence to strong reproductive isolation between ecotypes. However, the detailed histories of divergence, admixture and phylogenetic relationships between ecotypes differ substantially among populations. Our study highlights the flexibility of evolution through the interplay of parallel and non-parallel evolutionary and genomic patterns across populations and gives insights into mechanisms underpinning rapid diversification in the face of gene flow.
Project 2B) To assess whether there is commonality in genomic patterns of response selection across replicate species.
The organization of functional regions within genomes has important implications for evolutionary potential. Considerable research effort has gone toward identifying the genomic basis of phenotypic traits of interest through quantitative trait loci (QTL) analyses. Less research has assessed the arrangement of QTL in the genome within and across species. To investigate the distribution, extent of co-localization, and the synteny of QTL for ecologically relevant traits, we used a comparative genomic mapping approach within and across a range of salmonid species. We compiled 943 QTL from all available species (lake whitefish (Coregonus clupeaformis), coho salmon (Oncorhynchus kisutch), rainbow trout (Oncorhynchus mykiss), Chinook salmon (Oncorhynchus tshawytscha), Atlantic salmon (Salmo salar), Arctic charr (Salvelinus alpinus)). We developed a novel analytical framework for mapping and testing the distribution of these QTL. We found no correlation between QTL-density and gene-density at the chromosome level but did at the fine-scale. Two chromosomes were significantly enriched for QTL. We found multiple synteny blocks for morphological, life history, and physiological traits across species, but only morphology and physiology had significantly more than expected. Two or three pairs of traits were significantly co-localized in three species (lake whitefish, coho salmon, and rainbow trout). Co-localization and fine-scale synteny suggest genetic linkage between traits within species and a conserved genetic basis across species. However this pattern was overall weak, with co-localization and synteny being relatively rare. These findings advance our understanding of the role of genomic organization in the renowned ecological and phenotypic variability of salmonid fishes.

Impact
GEN ECOL ADAPT had socio-economic impact beyond my direct research area:
• In collaboration with Glasgow Polyomics my research group developed a new modification of the genotyping-by-sequencing approach. This was published in Molecular Ecology Resources 2015. We advertised the method on my website including providing a bench protocol for interested scientists to test the method.
• This research trains and mentors young scientists in my lab in advance genomics and transcriptomics analyses in evolutionary context. During the period of the award I trained and supervised six PhD students in the discipline and one co-supervised. Additionally I hosted four interns through national and European programmes.
• Because of my scientific and leadership record I was awarded a position in Scottish Crucible (2014), a national professional leadership programme, and Royal Society of Edinburgh Young Academy of Scotland, a learned multidisciplinary academy (2016)
• I received the Fisheries Society of the British Isles Medal (2015) for outstanding contributions by an emerging leader in fish biology research.
• I was invited to speak on my research as a keynote or invited speaker at multiple conferences and workshops.