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Lehnert, Sarah J.; Bentzen, Paul; Kess, Tony; Lien, Sigbjorn; Horne, John B.; Clément, Marie; Bradbury, Ian R. — 2019-02-19 Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 YBP, with the two lineages isolated in different southern refugia during glacial maxima, driving trans-Atlantic genomic and karyotypic divergence. Here, we investigate genomic consequences of glacial isolation and trans-Atlantic secondary contact using 108,870 single nucleotide polymorphisms (SNPs) genotyped in 80 North American and European populations. Throughout North America, we identified extensive inter-individual variation and discrete linkage blocks within and between chromosomes with known trans-Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post-glacial trans-Atlantic secondary contact, contrasting low European ancestry genome-wide (3%). Ssa08/Ssa29 showed greater intra-population diversity suggesting a derived chromosome fusion polymorphism within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large-scale intraspecific variation in genomic architecture of northern species.

Salisbury, Sarah; McCracken, Gregory; Perry, Robert; Keefe, Donald; Layton, Kara; Kess, Tony; Nugent, Cameron; Leong, Jong; Bradbury, Ian; Koop, Ben; Ferguson, Moira; Ruzzante, Daniel — 2022-04-11 <p><span style="background:white;">The potentially significant genetic consequences associated with the loss of migratory capacity of </span>diadromous fishes which have become landlocked in freshwater are poorly understood. Consistent selective pressures associated with freshwater residency may drive repeated differentiation both between allopatric landlocked and anadromous populations and within landlocked populations (resulting in sympatric morphs). Alternatively, the strong genetic drift anticipated in isolated landlocked populations could hinder consistent adaptation, limiting genetic parallelism. Understanding the degree of genetic parallelism underlying differentiation has implications for both the predictability of evolution and management practices. We employed an 87k SNP array to examine the genetic characteristics of landlocked and anadromous Arctic Charr (<em>Salvelinus alpinus</em>) populations from five drainages within Labrador, Canada. One gene was detected as an outlier between sympatric, size-differentiated morphs in each of two landlocked lakes. While no single locus differentiated all replicate pairs of landlocked and anadromous populations, several SNPs, genes, and paralogs, were consistently detected as outliers in at least 70% of these pairwise comparisons. A significant C-score suggested the amount of shared outlier SNPs across all paired landlocked and anadromous populations was greater than expected by chance. Our results indicate that despite their isolation, selection due to the loss of diadromy may drive consistent genetic responses in landlocked populations.</p>

Watson, Beth; Lehnert, Sarah; Bentzen, Paul; Kess, Tony; Einfeldt, Anthony; Duffy, Steven; Perriman, Ben; Lien, Sigbjorn; Kent, Matthew; Bradbury, Ian — 2021-12-17 <p>Chromosomal rearrangements (e.g., inversions, fusions, and translocations) have long been associated with environmental variation in wild populations. New genomic tools provide the opportunity to examine the role of these structural variants in shaping adaptive differences within and among wild populations of non-model organisms. In Atlantic Salmon (Salmo salar), variations in chromosomal rearrangements exist across the species natural range, yet the role and importance of these structural variants in maintaining adaptive differences among wild populations remains poorly understood. We genotyped Atlantic Salmon (n = 1429) from 26 populations within a highly genetically structured region of southern Newfoundland, Canada with a 220K SNP array. Multivariate analysis, across two independent years, consistently identified variation in a structural variant (translocation between chromosomes Ssa01 and Ssa23), previously associated with evidence of trans-Atlantic secondary contact, as the dominant factor influencing population structure in the region. Redundancy analysis suggested that variation in the Ssa01/Ssa23 chromosomal translocation is strongly correlated with temperature. Our analyses suggest environmentally mediated selection acting on standing genetic variation in genomic architecture introduced through secondary contact may underpin fine-scale local adaptation in Placentia Bay, Newfoundland, Canada, a large and deep embayment, highlighting the importance of chromosomal structural variation as a driver of contemporary adaptive divergence.</p> https://creativecommons.org/publicdomain/zero/1.0/

Lehnert, Sarah; Kess, Tony; Bentzen, Paul; Clément, Marie; Bradbury, Ian — 2020-05-28 <p>As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged &gt;600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 SNPs and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and processes shaping them. We found evidence of high (mean FST=0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans-Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1-3Mbp) on four chromosomes (Ssa06, Ssa13, Ssa16, and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium despite no local reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near fixed and potentially adaptive trans-Atlantic differences concurrent with a background of high genome-wide differentiation supports subspecies designation in Atlantic salmon.</p>

Jeffery, Nicholas W.; Vercaemer, Benedikte; Stanley, Ryan; Kess, Tony; Dufresne, France; Noisette, Fanny; O'Connor, Mary; Wong, Melisa — 2024-03-03 <p>A global decline in seagrass populations has led to renewed calls for their conservation as important providers of biogenic and foraging habitat, shoreline stabilisation, and carbon storage. Eelgrass (Zostera marina) occupies the largest geographic range among seagrass species spanning a commensurately broad spectrum of environmental conditions. In Canada, eelgrass is managed as a single phylogroup despite occurring across three oceans and a range of ocean temperatures and salinity gradients. Previous research has focused on applying relatively few markers to reveal population structure of eelgrass, whereas a whole genome approach is warranted to investigate cryptic structure among populations inhabiting different ocean basins and localized environmental conditions. We used a pooled whole-genome re-sequencing approach to characterise population structure, gene flow, and environmental associations of 23 eelgrass populations ranging from the Northeast United States, to Atlantic, subarctic, and Pacific Canada. We identified over 500,000 SNPs, which when mapped to a chromosome-level genome assembly revealed six broad clades of eelgrass across the study area, with pairwise FST ranging from 0 among neighbouring populations to 0.54 between Pacific and Atlantic coasts. Genetic diversity was highest in the Pacific and lowest in the subarctic, consistent with colonisation of the Arctic and Atlantic oceans from the Pacific less than 300 kya. Using redundancy analyses and two climate change projection scenarios, we found that subarctic populations are predicted to be more vulnerable to climate change through genomic offset predictions. Conservation planning in Canada should thus ensure that representative populations from each identified clade are included within a national network so that latent genetic diversity is protected, and gene flow is maintained. Northern populations, in particular, may require additional mitigation measures given their potential susceptibility to a rapidly changing climate.</p>

Kess, Tony; Galindo, Juan; Boulding, Elizabeth G. — 2019-06-11 The rough periwinkle, Littorina saxatilis, is a model system for studying parallel ecological speciation in microparapatry. Phenotypically parallel wave-adapted and crab-adapted ecotypes that hybridize within the middle shore are replicated along the northwestern coast of Spain, and have likely arisen from two separate glacial refugia. We tested whether greater geographic separation corresponding to reduced opportunity for contemporary or historical gene flow between parallel ecotypes resulted in less parallel genomic divergence. We sequenced double-digested restriction-associated DNA (ddRAD) libraries from individual snails from upper, mid, and low intertidal levels of three separate sites colonized from two separate refugia. FDIST analysis of 4256 SNP markers identified 34.4% sharing of divergent loci between two geographically-close sites, however, these sites each shared only 9.9-15.1% of their divergent loci with a third more-distant site. STRUCTURE analysis revealed that genotypes from only three of 166 phenotypically intermediate mid-shore individuals appeared to result from recent hybridization suggesting that hybrids cannot be reliably identified using shell traits. Hierarchical AMOVA indicated that the primary source of genomic differentiation was geographic separation, but also revealed greater similarity of the same ecotype across the two geographically-close sites than previously estimated with dominant markers. These results from a model system for ecological speciation suggest that genomic parallelism is affected by the opportunity for historical or contemporary gene flow between populations.

Einfeldt, Anthony; Kess, Tony — 2020-10-05 <p>Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes. To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multi-tissue transcriptomes, and population genomic data for the Atlantic Halibut (<i>Hippoglossus hippoglossus</i>), which<i> </i>has an XY/XX sex determination mechanism and has recently diverged from the Pacific Halibut (<i>Hippoglossus stenolepis</i>), which has a ZZ/ZW system. We used frequency and coverage-based population genomic approaches to identify a putative sex-determining factor, <i>GSDF</i>. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a recently formed sex chromosome. We detected testis-specific expression of <i>GSDF</i>, the sequence for which was highly conserved across flatfish. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfish, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic Halibut. A loss of function of the ancestral sex-determining gene <i>DMRT1</i> in regulating the downstream gene <i>GSDF</i> likely enabled <i>GSDF, </i>or a proximal regulatory element, to become the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multi-tissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes.</p>

Salisbury, Sarah J.; McCracken, Gregory R.; Perry, Robert; Keefe, Donald; K. S. Layton, Kara; Kess, Tony; Nugent, Cameron M.; Leong, Jong S.; Bradbury, Ian R.; Koop, Ben F.; Ferguson, Moira M.; Ruzzante, Daniel E. — 2020-09-30 <p>The genetic underpinnings of incipient speciation, including the genomic mechanisms which contribute to morphological and ecological differentiation and reproductive isolation, remain poorly understood. The repeated evolution of consistently, phenotypically distinct morphs of Arctic Charr (<i>Salvelinus alpinus</i>) within the Quaternary period offer an ideal model to study the repeatability of evolution at the genomic level. Sympatric morphs of Arctic Charr are found across this species' circumpolar distribution. However, the specific genetic mechanisms driving this morph differentiation are largely unknown despite the cultural and economic importance of the anadromous morph. We used a newly designed 87k SNP chip to investigate the character and consistency of the genomic differences among sympatric morphs within three recently deglaciated and geographically proximate lakes in Labrador, Canada. We found genetically distinct small and large morph Arctic Charr in all three lakes consistent with resident and anadromous morphs, respectively. A degree of reproductive isolation among sympatric morphs is likely given genome-wide distributions of outlier SNPs and high genome-wide <i>F</i>_STs. Across all lakes, outlier SNPs were largely non-overlapping suggesting a lack of genetic parallelism driving morph differentiation. Alternatively, several genes and paralogous copies of the same gene consistently differentiated morphs across multiple lakes suggesting their importance to the manifestation of morphs. Our results confirm the utility of Arctic Charr as a model for investigating the predictability of evolution and support the importance of both genetic parallelism and non-parallelism to the incipient speciation of Arctic Charr morphs.</p>

Kess, Tony; Bentzen, Paul; Lehnert, Sarah; Sylvester, Emma; Lien, Sigbjørn; Kent, Matthew; Sinclair-Waters, Marion; Morris, Corey; Wringe, Brendan; Fairweather, Robert; Bradbury, Ian — 2020-02-19 Genomic architecture and standing variation can play a key role in ecological adaptation, and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behaviour in regional analyses. However, the degree of parallelism , the extent of independent inheritance, and functional distinctiveness of these rearrangements remains poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine-scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangement with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures have likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine-scale adaptation in marine species.

Kess, Tony; Einfeldt, Anthony; Wringe, Brendan; Lehnert, Sarah; Layton, Kara; McBride, Meghan; Robert, Dominique; Fisher, Jonathan; Le Bris, Arnault; den Heyer, Cornelia; Shackell, Nancy; Ruzzante, Daniel; Bentzen, Paul; Bradbury, Ian — 2021-02-19 <p class="western" style="text-indent:1.27cm;text-align:left;"><span style="background:transparent none 0% 0%;">Characterizing the nature of genetic differentiation among individuals and populations and its distribution across the genome is increasingly important to inform both conservation and management of exploited species. Atlantic Halibut (<i>Hippoglossus hippoglossus</i>) is an ecologically and commercially important fish species, yet knowledge of population structure and genomic diversity in this species remains lacking. Here, we use restriction-site associated DNA sequencing and a chromosome-level genome assembly to identify over 86,000 single nucleotide polymorphisms mapped to 24 chromosome-sized scaffolds, genotyped in 734 individuals across the Northwest Atlantic. We describe subtle but significant genome-wide regional structuring between the Gulf of St. Lawrence and adjacent Atlantic continental shelf. However, the majority of genetic divergence is associated with a large putative chromosomal rearrangement (5.74 megabases) displaying high differentiation and linkage disequilibrium, but no evidence of geographic variation. Demographic reconstructions suggest <font color="#000000">periods of expansion</font> coinciding with glacial retreat, and more recent declines in N_e. This work highlights the utility of genomic data to identify multiple sources of genetic structure and genomic diversity in commercially exploited marine species. </span></p> <p class="western" style="text-align:left;"> </p>

K. S. Layton, Kara; Dempson, J. Brian; Snelgrove, Paul V.R.; Duffy, Steven J.; Messmer, Amber M.; Paterson, Ian; Jeffery, Nicholas W.; Kess, Tony; Horne, John B.; Salisbury, Sarah J.; Ruzzante, Daniel E.; Bentzen, Paul; Côté, David; Nugent, Cameron M.; Ferguson, Moira M.; Leong, Jong S.; Koop, Ben F.; Bradbury, Ian R. — 2020-01-17 <p>The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such quantifying diversity is central to combatting ongoing wide spread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in northeastern Canada, Arctic charr (<i>Salvelinus alpinus</i>). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic charr in northeastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the SNP panel and with the microsatellite loci (&gt;90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery, and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.</p>

Kess, Tony; Brachmann, Matthew; Boulding, Elizabeth — 2020-10-19 <p class="western" style="text-align:left;"><span style="background:transparent none 0% 0%;"><font><i>Littorina saxatilis</i></font><font> is becoming a model system for understanding the genomic basis of ecological speciation. The parallel formation of crab-adapted ecotypes that exhibit partial reproductive isolation from wave-adapted ecotypes has enabled genomic investigation of conspicuous shell traits. Recent genomic studies </font><font color="#000000"><font><font>suggest that </font></font></font><font>chromosomal rearrangements may enable ecotype divergence by reducing gene flow. However, the genomic architecture of traits </font><font color="#000000"><font>that are divergent between ecotypes</font></font><font> remains poorly understood. Here, we use 11,504 single nucleotide polymorphism (SNP) markers called using the recently-released </font><font><i>L. saxatilis</i></font><font> genome to genotype 462 crab ecotype, wave ecotype, and phenotypically-intermediate </font><font><i>L. saxatilis</i></font><font> individuals with scored phenotypes. We used redundancy analysis to study the genetic architecture of loci associated with shell shape, shape corrected for size, shell size, and shell ornamentation, and to compare levels of co-association among different traits. We discovered </font><font color="#000000"><font>341</font></font><font> SNPs associated with shell traits. </font><font color="#000000"><font><font>Loci associated</font></font></font><font><font> with trait divergence between ecotypes</font></font><font> were often located inside putative chromosomal rearrangements recently </font><font><font>characterized in</font></font><font> Swedish </font><font><i>L. saxatilis</i></font><font>. In contrast, we found that shell shape corrected for </font><font color="#000000"><font>size varied primarily by site rather than by ecotype and showed </font></font><font>little association with these putative rearrangements. </font><font><font>Together, these results reveal that</font></font><font> genomic regions of elevated divergence with putative rearrangements </font><font><font>are</font></font><font> associated with divergence along </font><font color="#000000"><font><font>steep </font></font></font><font color="#000000"><font>environmental axes in </font></font><font color="#000000"><font><i>L. saxatilis</i></font></font><font color="#000000"><font><span style="font-style:normal;"> ecotypes</span></font></font><font>, c</font><font><font>onsistent with </font></font><font>models of adaptation with gene flow, but these regions are distinct from </font><font color="#000000"><font><font>genomic architecture associated with</font></font></font><font color="#000000"><font> site-specific variation. </font></font><font color="#000000"><font><font>Our</font></font></font><font color="#000000"><font> findings here further support </font></font><font color="#000000"><font><font>predictions from models indicating the</font></font></font><font color="#000000"><font> importance of genomic regions of reduced recombination </font></font><font color="#000000"><font><font>allowing</font></font></font><font color="#000000"> </font><font>co-association of loci during ecological speciation with ongoing gene flow.</font></span></p>