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Barth, Julia M. I.; Villegas-Ríos, David; Freitas, Carla; Moland, Even; Star, Bastiaan; André, Carl; Knutsen, Halvor; Bradbury, Ian; Dierking, Jan; Petereit, Christoph; Righton, David; Metcalfe, Julian; Jakobsen, Kjetill S.; Olsen, Esben M.; Jentoft, Sissel; Barth, Julia M.I. 2018-12-28 Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod, by exploring a unique dataset combining whole-genome sequencing data and behavioral data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population, and a local fjord-type cod. Continuous behavioral tracking over four years revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicative for an adaptive barrier to gene flow. In addition, behavioral data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioral barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioral isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.
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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>
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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/
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Moore, Jean-Sébastien; Bourret, Vincent; Dionne, Mélanie; Bradbury, Ian; O’Reilly, Patrick; Kent, Matthew; Chaput, Gérald; Bernatchez, Louis; O'Reilly, Patrick 2014-10-23 Anadromous Atlantic salmon (Salmo salar) is a species of major conservation and management concern in North America, where population abundance has been declining over the past 30 years. Effective conservation actions require the delineation of conservation units to appropriately reflect the spatial scale of intraspecific variation and local adaptation. Towards this goal, we used the most comprehensive genetic and genomic database for Atlantic salmon to date, covering the entire North American range of the species. The database included microsatellite data from 9,142 individuals from 149 sampling locations and data from a medium-density SNP array providing genotypes for >3,000 SNPs for 50 sampling locations. We used neutral and putatively selected loci to integrate adaptive information in the definition of conservation units. Bayesian clustering with the microsatellite dataset and with neutral SNPs identified regional groupings largely consistent with previously published regional assessments. The use of outlier SNPs did not result in major differences in the regional groupings, suggesting that neutral markers can reflect the geographic scale of local adaptation despite not being under selection. We also performed assignment tests to compare power obtained from microsatellites, neutral SNPs and outlier SNPs. Using SNP data substantially improved power compared to microsatellites, and an assignment success of 97% to the population of origin and of 100% to the region of origin was achieved when all SNP loci were used. Using outlier SNPs only resulted in minor improvements to assignment success to the population of origin but improved regional assignment. We discuss the implications of these new genetic resources for the conservation and management of Atlantic salmon in North America.
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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>
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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.
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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<sub>e</sub>. 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>

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