Evolutionary genomics of adaptation in Atlantic salmon from northern Europe

Insight into genomic mechanisms of phenotypic variation and adaptation is essential for understanding evolutionary and population dynamics in wild populations. Knowledge about whether it is the same genetic architecture that underlies adaptation over different geographical scales and regions, and what role population history plays, is paramount for the consequent development of efficient conservation practices for the species. Salmonid fishes are commonly characterised by a wide geographic range, distinct population structure, and high incidence of local adaptation, which makes them a great target for studies exploring both the genomic basis of adaptation and the comparative significance of loci involved in adaptation within and between species. The Atlantic salmon (Salmo salar) populations of northern Europe are particularly interesting: they include the least disturbed populations left in the wild, belong to several distinct phylogeographic lineages, and exhibit astonishing natural variation in response to a salmon ectoparasite, Gyrodactylus salaris, ranging from near resistance in the landlocked and Baltic salmon to high susceptibility with devastating effect in Atlantic Ocean salmon. In this study, I used genome-wide approaches to further characterize the population structure and phylogeographic history of northern European Atlantic salmon (Chapters I-III). I explored the mechanisms behind the observed variation in the levels of susceptibility to G. salaris, by searching for genes playing a key role in the response to the parasite (Chapters I and II). Subsequently, I broadened my work to search for genomic regions involved in local adaptation in general. I examined whether the identified selection targets were similar over a broad geographic range and independent studies, and thus whether there are patterns of adaptive divergence that could be universal across Atlantic salmon populations (Chapter III). To achieve this, I used a large collection of Atlantic salmon samples and applied two SNP arrays of varying density to individual and pooled-per-population DNA samples. I looked for genomic signatures of directional selection in response to specific selective pressures, including G. salaris presence (Chapters I and II). I also looked for loci that may underly local adaptation in general by examining signatures of divergent directional selection among three geographically and genetically distinct sets of populations (Chapter III). To overcome the challenge of correlated environmental traits and the confounding effects of neutral evolution I used a careful methodological strategy, taking into account the phylogeographic relationships of populations and considering only repeated lines of evidence over multiple analyses. Several genomic regions, genes, and single SNP outliers were identified in relation to the observed variation in susceptibility to G. salaris, and to other potential selective pressures. Analyses of gene functions and comparison to other research suggest that the detected loci under G. salaris-mediated selection are participating in control of both innate and acquired immune systems. As there were few genes involved uniquely in immunity among the parasite-related candidates, my results highlight that the immune response in Atlantic salmon may be mediated by a large number of multi-functional loci (Chapters I and II). When examining for locally adaptive candidates in general, seventeen haploblocks were repeatedly found as candidates for divergent selection within different population groups. Several of these genomic regions contained loci known to be of large effect and to be associated with life-history traits and, interestingly, immunity (Chapter III). Overall, this thesis provides evidence that diversification in Atlantic salmon is driven both by multiple loci acting in specific population groups, and by few largeeffect loci acting over a wide geographic range. Exploring the effect of these loci on salmon fitness would help to validate the importance of identified genes and help to assess the long-term viability of northern European salmon

Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar)

Abstract Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.Peer reviewe

Footprints of directional selection in wild atlantic salmon populations: Evidence for parasite-driven evolution?

Mechanisms of host-parasite co-adaptation have long been of interest in evolutionary biology; however, determining the genetic basis of parasite resistance has been challenging. Current advances in genome technologies provide new opportunities for obtaining a genome-scale view of the action of parasite-driven natural selection in wild populations and thus facilitate the search for specific genomic regions underlying inter-population differences in pathogen response. European populations of Atlantic salmon (Salmo salar L.) exhibit natural variance in susceptibility levels to the ectoparasite Gyrodactylus salaris Malmberg 1957, ranging from resistance to extreme susceptibility, and are therefore a good model for studying the evolution of virulence and resistance. However, distinguishing the molecular signatures of genetic drift and environment-associated selection in small populations such as land-locked Atlantic salmon populations presents a challenge, specifically in the search for pathogen-driven selection. We used a novel genome-scan analysis approach that enabled us to i) identify signals of selection in salmon populations affected by varying levels of genetic drift and ii) separate potentially selected loci into the categories of pathogen (G. salaris)-driven selection and selection acting upon other environmental characteristics. A total of 4631 single nucleotide polymorphisms (SNPs) were screened in Atlantic salmon from 12 different northern European populations. We identified three genomic regions potentially affected by parasite-driven selection, as well as three regions presumably affected by salinity-driven directional selection. Functional annotation of candidate SNPs is consistent with the role of the detected genomic regions in immune defence and, implicitly, in osmoregulation. These results provide new insights into the genetic basis of pathogen susceptibility in Atlantic salmon and will enable future searches for the specific genes involved

Commencement Program, August (1966)

https://red.mnstate.edu/commencement/1105/thumbnail.jp

Footprints of directional selection in wild atlantic salmon populations: Evidence for parasite-driven evolution?

Mechanisms of host-parasite co-adaptation have long been of interest in evolutionary biology; however, determining the genetic basis of parasite resistance has been challenging. Current advances in genome technologies provide new opportunities for obtaining a genome-scale view of the action of parasite-driven natural selection in wild populations and thus facilitate the search for specific genomic regions underlying inter-population differences in pathogen response. European populations of Atlantic salmon (Salmo salar L.) exhibit natural variance in susceptibility levels to the ectoparasite Gyrodactylus salaris Malmberg 1957, ranging from resistance to extreme susceptibility, and are therefore a good model for studying the evolution of virulence and resistance. However, distinguishing the molecular signatures of genetic drift and environment-associated selection in small populations such as land-locked Atlantic salmon populations presents a challenge, specifically in the search for pathogen-driven selection. We used a novel genome-scan analysis approach that enabled us to i) identify signals of selection in salmon populations affected by varying levels of genetic drift and ii) separate potentially selected loci into the categories of pathogen (G. salaris)-driven selection and selection acting upon other environmental characteristics. A total of 4631 single nucleotide polymorphisms (SNPs) were screened in Atlantic salmon from 12 different northern European populations. We identified three genomic regions potentially affected by parasite-driven selection, as well as three regions presumably affected by salinity-driven directional selection. Functional annotation of candidate SNPs is consistent with the role of the detected genomic regions in immune defence and, implicitly, in osmoregulation. These results provide new insights into the genetic basis of pathogen susceptibility in Atlantic salmon and will enable future searches for the specific genes involved

Data from: Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar)

Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factor

Zueva_etal_2018_code&files_for_pictures.tar

code&files_for_pictures (readme file inside package

Zueva_etal_2018_allelotyping.tar

Allelotyping data for 220,000 SNPs (readme file inside package

Final overlap of results based on all applied designs: genome-wide evidence of directional selection.

<p>Vertical coloured shadings (green) show genomic regions, where two or three regions detected by kernel-smoothing-based designs overlap. “Parasite” (red) and “salinity” (blue) single outlier SNPs from design 4 are plotted as smaller vertical lines. Chromosome numbers are given, chromosomes bearing regions exclusively containing “parasite outliers” are marked with red font colour, and “salinity outliers” - with blue.</p

Map of northern Europe indicating the study populations: anadromous Atlantic Ocean, <i>G. salaris</i> susceptible (red); anadromous Baltic, moderately resistant (blue); landlocked, resistant to the parasite (green).

<p>Map of northern Europe indicating the study populations: anadromous Atlantic Ocean, <i>G. salaris</i> susceptible (red); anadromous Baltic, moderately resistant (blue); landlocked, resistant to the parasite (green).</p