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Jeffery, Nicholas W.; DiBacco, Claudio; Wringe, Brendan F.; Stanley, Ryan R.E.; Hamilton, Lorraine C.; Ravindran, Praveen N.; Bradbury, Ian R. — 2017-03-22 Invasive species have been associated with significant negative impacts in their introduced range often outcompeting native species, yet the long-term evolutionary dynamics of biological invasions are not well understood. Hybridization, either among waves of invasion or between native and introduced populations, could alter the ecological and evolutionary impacts of invasions yet has rarely been studied in marine invasive species. The European green crab (Carcinus maenas) invaded eastern North America twice from northern and southern locations in its native range. Here we examine the frequency of hybridization among these two distinct invasions at locations from New Jersey, USA to Newfoundland, Canada using restriction-site associated DNA sequencing (RAD-seq), microsatellite loci, and COI mtDNA sequences. We used Bayesian clustering and hybrid assignment analyses to investigate hybridization between the northern and southern populations. Of the samples analyzed, six locations contained at least one hybrid individual, while two locations were characterized by extensive hybridization, with 95% of individuals collected from Placentia Bay, Newfoundland being hybrids (mostly F2), and 90% of individuals from Kejimkujik, Nova Scotia being classified as hybrids, mostly backcrosses to the northern ecotype. The presence of both F2 hybrids and backcrossed individuals suggests that these hybrids are viable and introgression is occurring between invasions. Our results provide insight into the demographic and evolutionary consequences of hybridization between independent invasions, and will inform the management of green crabs in eastern North America.

Jeffery, Nicholas W.; Stanley, Ryan R. E.; Wringe, Brendan F.; Guijarro-Sabaniel, Javier; Bourret, Vincent; Bernatchez, Louis; Bentzen, Paul; Beiko, Robert G.; Gilbey, John; Clement, Marie; Bradbury, Ian R. — 2017-10-13 Clinal variation across replicated environmental gradients can reveal evidence of local adaptation, providing insight into the demographic and evolutionary processes that shape intraspecific diversity. Using 1773 genome-wide single nucleotide polymorphisms we evaluated latitudinal variation in allele frequency for 134 populations of North American and European Atlantic salmon (Salmo salar). We detected 84 (4.74%) and 195 (11%) loci showing clinal patterns in North America and Europe respectively, with 12 clinal loci in common between continents. Clinal SNPs were evenly distributed across the salmon genome and logistic regression revealed significant associations with latitude and seasonal temperatures, particularly average spring temperature in both continents. Loci displaying parallel clines were associated with several metabolic and immune functions, suggesting a potential basis for climate associated adaptive differentiation. These climate-based clines collectively suggest evidence of large scale environmental associated differences on either side of the North Atlantic. Our results support patterns of parallel evolution on both sides of the North Atlantic, with evidence of both similar and divergent underlying genetic architecture. The identification of climate associated genomic clines illuminates the role of selection and demographic processes on intraspecific diversity in this species and provides a context in which to evaluate the impacts of climate change.

Jeffery, Nicholas W.; DiBacco, Claudio; Van Wyngaarden, Mallory; Hamilton, Lorraine C.; Stanley, Ryan R. E.; Bernier, Renée; FitzGerald, Jennifer; Matheson, K.; McKenzie, C. H.; Nadukkalam Ravindran, Praveen; Beiko, Robert; Bradbury, Ian R. — 2017-03-22 Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction-site-associated DNA sequencing-derived SNPs to explore fine-scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise FST ~0.001 to 0.15) and spread across many loci, with a mean FST ~0.052 and 52% of loci examined characterized by FST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.

Lehnert, Sarah J.; DiBacco, Claudio; Jeffery, Nicholas W.; Blakeslee, April M.H.; Isaksson, Jonatan; Roman, Joe; Wringe, Brendan F.; Stanley, Ryan R.E.; Matheson, Kyle; McKenzie, Cynthia H.; Hamilton, Lorraine C.; Bradbury, Ian R.; Stanley, Ryan R. E.; Blakeslee, April M. H. — 2018-06-05 Two genetically distinct lineages of European green crabs (Carcinus maenas) were independently introduced to eastern North America, the first in the early 19th century and the second in the late 20th century. These lineages first came into secondary contact in southeastern Nova Scotia, Canada (NS), where they hybridized, producing latitudinal genetic clines. Previous studies have documented a persistent southward shift in the clines of different marker types, consistent with existing dispersal and recruitment pathways. We evaluated current clinal structure by quantifying the distribution of lineages and fine-scale hybridization patterns across the eastern North American range (25 locations, ~39-49°N) using informative single nucleotide polymorphisms (SNPs; n=96). In addition, temporal changes in the genetic clines were evaluated using mitochondrial DNA and microsatellite loci (n=9-11) over a 15-year period (2000-2015). Clinal structure was consistent with prior work demonstrating the existence of both northern and southern lineages with a hybrid zone occurring between southern New Brunswick (NB) and southern NS. Extensive later generation hybrids were detected in this region and in southeastern Newfoundland. Temporal genetic analysis confirmed the southward progression of clines over time; however, the rate of this progression was slower than predicted by forecasting models, and current clines for all marker types deviated significantly from these predictions. Our results suggest that neutral and selective processes contribute to cline dynamics, and ultimately, highlight how selection, hybridization, and dispersal can collectively influence invasion success.

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>

Wringe, Brendan F.; Jeffery, Nicholas W.; Stanley, Ryan R.E.; Hamilton, Lorraine C.; Anderson, Eric C.; Fleming, Ian A.; Grant, Carole; Dempson, J. Brian; Veinott, Geoff; Duffy, Steven J.; Bradbury, Ian R. — 2019-07-18 [No abstract entered]

Jeffery, Nicholas W.; Bradbury, Ian R.; Stanley, Ryan R.E.; Wringe, Brendan F.; Van Wyngaarden, Mallory; Lowen, J. Ben; McKenzie, Cynthia H.; Matheson, Kyle; Sargent, Philip S.; DiBacco, Claudio; Stanley, Ryan R. E. — 2018-01-19 Genetic-environment associations are increasingly revealed through population genomic data and can occur through a number of processes, including secondary contact, divergent natural selection, or isolation-by-distance. Here we investigate the influence of the environment, including seasonal temperature and salinity, on the population structure of the invasive European green crab (Carcinus maenas) in eastern North America. Green crab populations in eastern North America are associated with two independent invasions, previously shown to consist of distinct northern and southern ecotypes, with a contact zone in southern Nova Scotia, Canada. Using a RAD-seq panel of 9137 genome-wide SNPs, we detected 41 SNPs (0.49%) whose allele frequencies were highly correlated with environmental data. A principal components analysis of 25 environmental variables differentiated populations into northern, southern, and admixed sites in concordance with the observed genomic spatial structure. Furthermore, a spatial principal components analysis conducted on genomic and geographic data revealed a high degree of global structure (p<0.0001) partitioning a northern and southern ecotype. Redundancy and partial redundancy analyses revealed that among the environmental variables tested, winter sea surface temperature had the strongest association with spatial structuring, suggesting that it is an important factor defining range and expansion limits of each ecotype. Understanding environmental thresholds associated with intraspecific diversity will facilitate the ability to manage current and predict future distributions of this aquatic invasive species.

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>

Van Wyngaarden, Mallory; Snelgrove, Paul V.R.; DiBacco, Claudio; Hamilton, Lorraine C.; Rodríguez-Ezpeleta, Naiara; Jeffery, Nicholas W.; Stanley, Ryan R.; Bradbury, Ian R.; Stanley, Ryan R. E.; Snelgrove, Paul V. R. — 2016-08-29 Understanding patterns of dispersal and connectivity among marine populations can directly inform fisheries conservation and management. Advances in high-throughput sequencing offer new opportunities for estimating marine connectivity. We used Restriction-site Associated DNA sequencing to examine dispersal and realized connectivity in the sea scallop Placopecten magellanicus, an economically important marine bivalve. Based on 245 individuals sampled range-wide at 12 locations from Newfoundland to the Mid-Atlantic Bight we identified and genotyped 7163 Single Nucleotide Polymorphisms; 112 (1.6%) were identified as outliers potentially under directional selection. Bayesian clustering revealed a discontinuity between northern and southern samples and latitudinal clines in allele frequencies were observed in 42.9% of the outlier loci and in 24.6% of neutral loci. Dispersal estimates derived using these clines and estimates of linkage disequilibrium imply limited dispersal; 373.1 ± 407.0 km (mean ± SD) for outlier loci and 641.0 ± 544.6 km (mean ± SD) for neutral loci. Our analysis suggests restricted dispersal compared to the species range (>2000 km) and that dispersal and effective connectivity differ. These observations support the hypothesis that limited effective dispersal structures scallop populations along eastern North America. These findings can help refine the appropriate scale of management and conservation in this commercially valuable species.