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Prentice, Melanie B.; Bowman, Jeff; Wilson, Paul J. 2016-10-14 Background: The androgen receptor, an X-linked gene, has been widely studied in human populations because it contains highly polymorphic trinucleotide repeat motifs that have been associated with a number of adverse human health and behavioral effects. A previous study on the androgen receptor gene in carnivores reported somatic mosaicism in the tissues of a number of species including Eurasian lynx (Lynx lynx). We investigated this claim in a closely related species, Canada lynx (Lynx canadensis). The presence of somatic mosaicism in lynx tissues could have implications for the future study of exonic trinucleotide repeats in landscape genomic studies, in which the accurate reporting of genotypes would be highly problematic. Methods: To determine whether mosaicism occurs in Canada lynx, two lynx individuals were sampled for a variety of tissue types (lynx 1) and tissue locations (lynx 1 and 2), and 1,672 individuals of known sex were genotyped to further rule out mosaicism. Results: We found no evidence of mosaicism in tissues from the two necropsied individuals, or any of our genotyped samples. Conclusions: Our results indicate that mosaicism does not manifest in Canada lynx. Therefore, the use of hide samples for further work involving trinucleotide repeat polymorphisms in Canada lynx is warranted. https://creativecommons.org/publicdomain/zero/1.0/
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Prentice, Melanie B.; Bowman, Jeff; Lalor, Jillian L.; McKay, Michelle M.; Thomson, Lindsay A.; Watt, Cristen M.; McAdam, Andrew G.; Murray, Dennis L.; Wilson, Paul J. 2017-08-23 Climate change is predicted to affect the reproductive ecology of wildlife; however, we have yet to understand if and how species can adapt to the rapid pace of change. Clock genes are functional genes likely critical for adaptation to shifting seasonal conditions through shifts in timing cues. Many of these genes contain coding trinucleotide repeats, which offer the potential for higher rates of change than single nucleotide polymorphisms (SNPs) at coding sites, and, thus, may translate to faster rates of adaptation in changing environments. We characterized repeats in 22 clock genes across all annotated mammal species and evaluated the potential for selection on repeat motifs in three clock genes (NR1D1, CLOCK, and PER1) in three congeneric species pairs with different latitudinal range limits: Canada lynx and bobcat (Lynx canadensis and L. rufus), northern and southern flying squirrels (Glaucomys sabrinus and G. volans), and white-footed and deer mouse (Peromyscus leucopus and P. maniculatus). Signatures of positive selection were found in both the interspecific comparison of Canada lynx and bobcat, and intraspecific analyses in Canada lynx. Northern and southern flying squirrels showed differing frequencies at common CLOCK alleles and a signature of balancing selection. Regional excess homozygosity was found in the deer mouse at PER1 suggesting disruptive selection, and further analyses suggested balancing selection in the white-footed mouse. These preliminary signatures of selection and the presence of trinucleotide repeats within many clock genes warrant further consideration of the importance of candidate gene motifs for adaptation to climate change.
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Klutsch, Cornelya F. C.; Manseau, Micheline; Trim, Vicki; Polfus, Jean; Wilson, Paul J. 2016-01-11 Understanding the evolutionary history of contemporary animal groups is essential for conservation and management of endangered species like caribou (Rangifer tarandus). In central Canada, the ranges of two caribou subspecies (barren-ground/woodland caribou) and two woodland caribou ecotypes (boreal/eastern migratory) overlap. Our objectives were to reconstruct the evolutionary history of the eastern migratory ecotype and to assess the potential role of introgression in ecotype evolution. STRUCTURE analyses identified five higher order groups (i.e. three boreal caribou populations, eastern migratory ecotype and barren-ground). The evolutionary history of the eastern migratory ecotype was best explained by an early genetic introgression from barren-ground into a woodland caribou lineage during the Late Pleistocene and subsequent divergence of the eastern migratory ecotype during the Holocene. These results are consistent with the retreat of the Laurentide ice sheet and the colonization of the Hudson Bay coastal areas subsequent to the establishment of forest tundra vegetation approximately 7000 years ago. This historical reconstruction of the eastern migratory ecotype further supports its current classification as a conservation unit, specifically a Designatable Unit, under Canada’s Species at Risk Act. These findings have implications for other sub-specific contact zones for caribou and other North American species in conservation unit delineation.
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Priadka, Pauline; Manseau, Micheline; Trottier, Tim; Hervieux, Dave; Galpern, Paul; McLoughlin, Philip D.; Wilson, Paul J. 2018-12-18 Isolation-by-distance (IBD) is a natural pattern not readily incorporated into theoretical models nor traditional metrics for differentiating populations, although clinal genetic differentiation can be characteristic of many wildlife species. Landscape features can also drive population structure additive to baseline IBD resulting in differentiation through isolation-by-resistance (IBR). We assessed the population genetic structure of boreal caribou across western Canada using non-spatial (STRUCTURE) and spatial (MEMGENE) clustering methods and investigated the relative contribution of IBD and IBR on genetic variation of 1221 boreal caribou multilocus genotypes across western Canada. We further introduced a novel approach to compare the partitioning of individuals into management units (MU) and assessed levels of genetic connectivity under different MU scenarios. STRUCTURE delineated five genetic clusters while MEMGENE identified finer-scale differentiation across the study area. IBD was significant and did not differ for males and females both across and among detected genetic clusters. MEMGENE landscape analysis further quantified the proportion of genetic variation contributed by IBD and IBR patterns, allowing for the relative importance of spatial drivers, including roads, water bodies and wildfires, to be assessed and incorporated into the characterization of population structure for the delineation of MUs. Local population units, as currently delineated in the boreal caribou recovery strategy, do not capture the genetic variation and connectivity of the ecotype across the study area. Here, we provide the tools to assess fine-scale spatial patterns of genetic variation, partition drivers of genetic variation and evaluate the best management options for maintaining genetic connectivity. Our approach is highly relevant to vagile wildlife species that are of management and conservation concern and demonstrate varying degrees of IBD and IBR with clinal spatial genetic structure that challenges the delineation of discrete population boundaries.
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Klütsch, Cornelya F. C.; Manseau, Micheline; Anderson, Morgan; Sinkins, Peter; Wilson, Paul J. 2017-09-20 Aim: The presence of refugia in the Canadian High Arctic has been subject to debate for decades. We investigated the potential existence of Arctic refugia during the Pleistocene for a large mammal species in the Canadian Archipelago because if these refugia were present, reconsideration of the evolutionary histories of North American fauna and flora beyond the major refugia of Beringia and south of the Laurentide and Cordilleran Ice Sheets would be required. Peary caribou (Rangifer tarandus pearyi), identified as a subspecies based on morphological characteristics, inhabits the Canadian Arctic Islands and Boothia Peninsula. Previous studies demonstrated incomplete lineage sorting of mitochondrial DNA interpreted as a Beringian origin but were based on small sample sizes. Location: Canadian Arctic. Major taxa studied: Mammals: caribou (Rangifer tarandus). Methods: We used two molecular markers (microsatellites and mitochondrial DNA) and approximate Bayesian computations (ABC) testing the hypotheses of colonization out of Beringia into the Arctic Islands following the Last Glacial Maximum (LGM) or a divergence from Beringia significantly before the end of the LGM within a different refugium. Results: The coalescent-based analyses rejected a recent Beringian origin with subsequent colonization, instead supporting a divergence of Peary caribou from Beringia ~100,000 years ago linking it to the last interglacial/early Wisconsin Glacial Stage (125,000–75,000 years ago). Admixture on Banks Island with Beringian-derived barren-ground caribou is indicative of post-Pleistocene secondary contact; further supporting a divergent history of Peary caribou within a separated Arctic refugium. Main conclusions: Our results offer support for the existence of an Arctic refugium for large mammal species and add to the increasing evidence of such refugia in North America. This has significant implications on understanding the evolution and conservation of Arctic species, particularly in light of sensitivities and adaptive potential to a rapidly changing climate.
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Marrotte, Robby R.; Bowman, Jeff; Brown, Michael G. C.; Cordes, Chad; Morris, Kimberley Y.; Prentice, Melanie B.; Wilson, Paul J. 2018-10-02 Background: Habitat fragmentation reduces genetic connectivity for multiple species, yet conservation efforts tend to rely heavily on single-species connectivity estimates to inform land-use planning. Such conservation activities may benefit from multi-species connectivity estimates, which provide a simple and practical means to mitigate the effects of habitat fragmentation for a larger number of species. To test the validity of a multi-species connectivity model, we used neutral microsatellite genetic datasets of Canada lynx (Lynx canadensis), American marten (Martes americana), fisher (Pekania pennanti), and southern flying squirrel (Glaucomys volans) to evaluate multi-species genetic connectivity across Ontario, Canada. Results: We used linear models to compare node-based estimates of genetic connectivity for each species to point-based estimates of landscape connectivity (current density) derived from circuit theory. To our knowledge, we are the first to evaluate current density as a measure of genetic connectivity. Our results depended on landscape context: habitat amount was more important than current density in explaining multi-species genetic connectivity in the northern part of our study area, where habitat was abundant and fragmentation was low. In the south however, where fragmentation was prevalent, genetic connectivity was correlated with current density. Contrary to our expectations however, locations with a high probability of movement as reflected by high current density were negatively associated with gene flow. Subsequent analyses of circuit theory outputs showed that high current density was also associated with high effective resistance, underscoring that the presence of pinch points is not necessarily indicative of gene flow. Conclusions: Overall, our study appears to provide support for the hypothesis that landscape pattern is important when habitat amount is low. We also conclude that while current density is proportional to the probability of movement per unit area, this does not imply increased gene flow, since high current density tends to be a result of neighbouring pixels with high cost of movement (e.g., low habitat amount). In other words, pinch points with high current density appear to constrict gene flow.
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Wheeldon, Tyler J.; Rutledge, Linda Y.; Patterson, Brent R.; White, Bradley N.; Wilson, Paul J. 2013-07-31 Hybridization has played an important role in the evolutionary history of Canis species in eastern North America. Genetic evidence of coyote–dog hybridization based on mitochondrial DNA (mtDNA) is lacking compared to that based on autosomal markers. This discordance suggests dog introgression into coyotes has potentially been male biased, but this hypothesis has not been formally tested. Therefore, we investigated biparentally, maternally, and paternally inherited genetic markers in a sample of coyotes and dogs from southeastern Ontario to assess potential asymmetric dog introgression into coyotes. Analysis of autosomal microsatellite genotypes revealed minimal historical and contemporary admixture between coyotes and dogs. We observed only mutually exclusive mtDNA haplotypes in coyotes and dogs, but we observed Y-chromosome haplotypes (Y-haplotypes) in both historical and contemporary coyotes that were also common in dogs. Species-specific Zfy intron sequences of Y-haplotypes shared between coyotes and dogs confirmed their homology and indicated a putative origin from dogs. We compared Y-haplotypes observed in coyotes, wolves, and dogs profiled in multiple studies, and observed that the Y-haplotypes shared between coyotes and dogs were either absent or rare in North American wolves, present in eastern coyotes, but absent in western coyotes. We suggest the eastern coyote has experienced asymmetric genetic introgression from dogs, resulting from predominantly historical hybridization with male dogs and subsequent backcrossing of hybrid offspring with coyotes. We discuss the temporal and spatial dynamics of coyote–dog hybridization and the conditions that may have facilitated the introgression of dog Y-chromosomes into coyotes. Our findings clarify the evolutionary history of the eastern coyote.
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Marrotte, Robby R.; Bowman, Jeff; Wilson, Paul J. 2021-10-19 <p>The Great Lakes and the St. Lawrence River are imposing barriers for wildlife and the additive effect of urban and agricultural development that dominates the lower Great Lakes region likely further reduces functional connectivity for many terrestrial species. As the climate warms species will need to track climate across these barriers. It is important, therefore, to investigate land cover and bioclimatic hypotheses that may explain the northward expansion of species through the Great Lakes. We investigated the functional connectivity of a vagile generalist, the bobcat, as a representative generalist forest species common to the region. We genotyped tissue samples collected across the region at 14 microsatellite loci and compared different landscape hypotheses that might explain the observed gene flow or functional connectivity. We found that the Great Lakes and the additive influence of forest stands with either low or high canopy cover and deep lake-effect snow have disrupted gene flow, whereas intermediate forest cover has facilitated gene flow. Functional connectivity in southern Ontario is relatively low and was limited in part by the low amount of forest cover. Pathways across the Great Lakes were through the Niagara region and through the Lower Peninsula of Michigan over the Straits of Mackinac and the St. Mary’s River. These pathways are important routes for bobcat range expansion north of the Great Lakes and are also likely pathways that many other mobile habitat generalists must navigate to track the changing climate. The extent to which species can navigate these routes will be important for determining the future biodiversity of areas north of the Great Lakes.</p>
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McFarlane, Samantha; Manseau, Micheline; Wilson, Paul J. 2022-01-30 <p class="List1" style="margin-bottom:13px;">In social species, reproductive success and rates of dispersal vary among individuals resulting in spatially structured populations. Network analyses of familial relationships may provide insights on how these parameters influence population-level demographic patterns. These methods have however rarely been applied to genetically-derived pedigree data from wild populations.</p> <p class="List1" style="margin-bottom:13px;">Here we use parent-offspring relationships to construct familial networks from polygamous boreal woodland caribou (<i>Rangifer tarandus caribou</i>) in Saskatchewan, Canada, to inform recovery efforts. We collected samples from 933 individuals at 15 variable microsatellite loci along with caribou-specific primers for sex identification. Using network measures, we assess the contribution of individual caribou to the population with several centrality measures and then determine which measures are best suited to inform on the population demographic structure. We investigate the centrality of individuals from eighteen different local areas, along with the entire population.</p> <p class="List1" style="margin-bottom:13px;">We found substantial differences in centrality of individuals in different local areas, that in turn contributed differently to the full network, highlighting the importance of analyzing networks at different scales. The full network revealed that boreal caribou in Saskatchewan form a complex, interconnected familial network, as the removal of edges with high betweenness did not result in distinct subgroups. Alpha, betweenness, and eccentricity centrality were the most informative measures to characterize the population demographic structure and for spatially identifying areas of highest fitness levels and family cohesion across the range. We found varied levels of dispersal, fitness and cohesion in family groups.</p> <p class="List1" style="margin-bottom:13px;"><i>Synthesis and applications</i>: Our results demonstrate the value of different network measures in assessing genetically-derived familial networks. The spatial application of the familial networks identified individuals presenting different fitness levels, short and long-distance dispersing ability across the range in support of population monitoring and recovery efforts.</p>
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Koen, Erin L.; Bowman, Jeff; Wilson, Paul J. 2015-04-30 At-site environmental conditions can have strong influences on genetic connectivity, and in particular on the immigration and settlement phases of dispersal. However, at-site processes are rarely explored in landscape genetic analyses. Networks can facilitate the study of at-site processes, where network nodes are used to model site-level effects. We used simulated genetic networks to compare and contrast the performance of 7 node-based (as opposed to edge-based) genetic connectivity metrics. We simulated increasing node connectivity by varying migration in two ways: we increased the number of migrants moving between a focal node and a set number of recipient nodes, and we increased the number of recipient nodes receiving a set number of migrants. We found that two metrics in particular, the average edge weight and the average inverse edge weight, varied linearly with simulated connectivity. Conversely, node degree was not a good measure of connectivity. We demonstrated the use of average inverse edge weight to describe the influence of at-site habitat characteristics on genetic connectivity of 653 American martens (Martes americana) in Ontario, Canada. We found that highly connected nodes had high habitat quality for marten (deep snow and high proportions of coniferous and mature forest) and were farther from the range edge. We recommend the use of node-based genetic connectivity metrics, in particular, average edge weight or average inverse edge weight, to model the influences of at-site habitat conditions on the immigration and settlement phases of dispersal.
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Prentice, Melanie B.; Bowman, Jeff; Khidas, Kamal; Koen, Erin L.; Row, Jeffrey R.; Murray, Dennis L.; Wilson, Paul J. 2018-04-14 Island populations have long been important for understanding the dynamics and mechanisms of evolution in natural systems. While genetic drift is often strong on islands due to founder events and population bottlenecks, the strength of selection can also be strong enough to counteract the effects of drift. Here, we used several analyses to identify the roles of genetic drift and selection on genetic differentiation and diversity of Canada lynx (Lynx canadensis) across eastern Canada, including the islands of Cape Breton and Newfoundland. Specifically, we assessed whether we could identify a genetic component to the observed morphological differentiation that has been reported across insular and mainland lynx. We used a dinucleotide repeat within the promoter region of a functional gene that has been linked to mammalian body size, insulin-like growth factor-1 (IGF-1). We found high genetic differentiation at neutral molecular markers but convergence of allele frequencies at the IGF-1 locus. Thus, we showed that while genetic drift has influenced the observed genetic structure of lynx at neutral molecular markers, natural selection has also played a role in the observed patterns of genetic diversity at the IGF-1 locus of insular lynx.
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Bertrand, Philip; Bowman, Jeff; Dyer, Rodney; Manseau, Micheline; Wilson, Paul J.; Dyer, Rodney J. 2017-05-05 Sex-specific genetic structure is a commonly observed pattern among vertebrate species. Facing differential selective pressures, individuals may adopt sex-specific life history traits that ultimately shape genetic variation among populations. Although differential dispersal dynamics are commonly detected in the literature, few studies have used genetic structure to investigate sex-specific functional connectivity. The recent use of graph theoretic approaches in landscape genetics has demonstrated network capacities to describe complex system behaviours where network topology represents genetic interaction among subunits. Here, we partition the overall genetic structure into sex-specific graphs, revealing different male and female dispersal dynamics of a fisher (Pekania [Martes] pennanti) metapopulation in southern Ontario. Our analyses based on network topologies supported the hypothesis of male-biased dispersal. Furthermore, we demonstrated that the effect of the landscape, identified at the population level, could be partitioned among sex-specific strata. We found that female connectivity was negatively correlated with snow depth, whereas connectivity among males was not. Our findings underscore the potential of conducting sex-specific analysis by identifying landscape elements or configuration that differentially promotes or impedes functional connectivity between sexes, revealing processes that may otherwise remain cryptic. We propose that the sex-specific graph approach would be applicable to other vagile species where differential sex-specific processes are expected to occur.
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Morris, Kimberley Y.; Bowman, Jeff; Schulte-Hostedde, Albrecht; Wilson, Paul J. 2020-08-07 <p>The release of domestic organisms to the wild threatens biodiversity because the introduction of domestic genes through interbreeding can negatively impact wild conspecifics via outbreeding depression. In North America, farmed American mink (<i>Neovison vison</i>) frequently escape captivity, yet the impact of these events on functional genetic diversity of wild mink populations is unclear. We characterized domestic and wild mink in Ontario at 17 microsatellites located in functional genes and in a promoter region that is non-coding but thought to be associated with traits affected by domestication. We found low functional genetic diversity in both mink types, as only 4 of 17 genes were variable, and the number of alleles per locus were generally lower in captive mink than in wild mink. To determine if allele frequencies of wild populations were affected by domestic release events, we performed redundancy analysis and spatial analysis of principal components on four polymorphic loci (AR, ATN1, IGF-1, and TOB1). We found evidence to suggest domestic release events are affecting the functional genetic diversity of wild mink, as sPCA showed clear distinctions between wild individuals near mink farms and those located in areas without mink farms. This is further substantiated through RDA, where spatial location was associated with genetic variation of AR, ATN1, and IGF1.</p>

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