Diving into broad-scale and high-resolution population genomics to decipher drivers of structure and climatic vulnerability in a marine invertebrate.

Species with widespread distributions play a crucial role in our understanding of climate change impacts on population structure. In marine species, population structure is often governed by both high connectivity potential and selection across strong environmental gradients. Despite the complexity of factors influencing marine populations, studying species with broad distribution can provide valuable insights into the relative importance of these factors and the consequences of climate-induced alterations across environmental gradients. We used the northern shrimp Pandalus borealis and its wide latitudinal distribution to identify current drivers of population structure and predict the species' vulnerability to climate change. A total of 1514 individuals sampled across 24° latitude were genotyped at high geographic (54 stations) and genetic (14,331 SNPs) resolutions to assess genetic variation and environmental correlations. Four populations were identified in addition to finer substructure associated with local adaptation. Geographic patterns of neutral population structure reflected predominant oceanographic currents, while a significant proportion of the genetic variation was associated with gradients in salinity and temperature. Adaptive landscapes generated using climate projections suggest a larger genomic offset in the southern extent of the P. borealis range, where shrimp had the largest adaptive standing genetic variation. Our genomic results combined with recent observations point to further deterioration in southern regions and an impending vulnerable status in the regions at higher latitudes for P. borealis. They also provide rare insights into the drivers of population structure and climatic vulnerability of a widespread meroplanktonic species, which is crucial to understanding future challenges associated with invertebrates essential to ecosystem functioning.

Modeling demersal fish and benthic invertebrate assemblages in support of marine conservation planning.

Marine classification schemes based on abiotic surrogates often inform regional marine conservation planning in lieu of detailed biological data. However, these schemes may poorly represent ecologically relevant biological patterns required for effective design and management strategies. We used a community-level modeling approach to characterize and delineate representative mesoscale (tens to thousands of kilometers) assemblages of demersal fish and benthic invertebrates in the Northwest Atlantic. Hierarchical clustering of species occurrence data from four regional annual multispecies trawl surveys revealed three to six groupings (predominant assemblage types) in each survey region, broadly associated with geomorphic and oceanographic features. Indicator analyses identified 3-34 emblematic taxa of each assemblage type. Random forest classifications accurately predicted assemblage distributions from environmental covariates (AUC > 0.95) and identified thermal limits (annual minimum and maximum bottom temperatures) as important predictors of distribution in each region. Using forecasted oceanographic conditions for the year 2075 and a regional classification model, we projected assemblage distributions in the southernmost bioregion (Scotian Shelf-Bay of Fundy) under a high emissions climate scenario (RCP 8.5). Range expansions to the northeast are projected for assemblages associated with warmer and shallower waters of the Western Scotian Shelf over the 21st century as thermal habitat on the relatively cooler Eastern Scotian Shelf becomes more favorable. Community-level modeling provides a biotic-informed approach for identifying broadscale ecological structure required for the design and management of ecologically coherent, representative, well-connected networks of Marine Protected Areas. When combined with oceanographic forecasts, this modeling approach provides a spatial tool for assessing sensitivity and resilience to climate change, which can improve conservation planning, monitoring, and adaptive management.

Fine-scale temperature-associated genetic structure between inshore and offshore populations of sea scallop (Placopecten magellanicus).

In the northwest Atlantic Ocean, sea scallop (Placopecten magellanicus) has been characterized by a latitudinal genetic cline with a breakpoint between northern and southern genetic clusters occurring at ~45°N along eastern Nova Scotia, Canada. Using 96 diagnostic single-nucleotide polymorphisms (SNPs) capable of discriminating between northern and southern clusters, we examined fine-scale genetic structure of scallops among 27 sample locations, spanning the largest geographic range evaluated in this species to date (~37-51°N). Here, we confirmed previous observations of northern and southern groups, but we show that the boundary between northern and southern clusters is not a discrete latitudinal break. Instead, at latitudes near the previously described boundary, we found unexpected patterns of fine-scale genetic structure occurring between inshore and offshore sites. Scallops from offshore sites, including St. Pierre Bank and the eastern Scotian Shelf, clustered with southern stocks, whereas inshore sites at similar latitudes clustered with northern stocks. Our analyses revealed significant genetic divergence across small spatial scales (i.e., 129-221 km distances), and that spatial structure over large and fine scales was strongly associated with temperature during seasonal periods of thermal minima. Clear temperature differences between inshore and offshore locations may explain the fine-scale structuring observed, such as why southern lineages of scallop occur at higher latitudes in deeper, warmer offshore waters. Our study supports growing evidence that fine-scale population structure in marine species is common, often environmentally associated, and that consideration of environmental and genomic data can significantly enhance the identification of marine diversity and management units.

Variation in genomic vulnerability to climate change across temperate populations of eelgrass (Zostera marina).

A global decline in seagrass populations has led to renewed calls for their conservation as important providers of biogenic and foraging habitat, shoreline stabilization 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 characterize 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 F ST 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 colonization 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 potentially 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.

Application of Omics Tools in Designing and Monitoring Marine Protected Areas For a Sustainable Blue Economy.

A key component of the global blue economy strategy is the sustainable extraction of marine resources and conservation of marine environments through networks of marine protected areas (MPAs). Connectivity and representativity are essential factors that underlie successful implementation of MPA networks, which can safeguard biological diversity and ecosystem function, and ultimately support the blue economy strategy by balancing ocean use with conservation. New "big data" omics approaches, including genomics and transcriptomics, are becoming essential tools for the development and maintenance of MPA networks. Current molecular omics techniques, including population-scale genome sequencing, have direct applications for assessing population connectivity and for evaluating how genetic variation is represented within and among MPAs. Effective baseline characterization and long-term, scalable, and comprehensive monitoring are essential for successful MPA management, and omics approaches hold great promise to characterize the full range of marine life, spanning the microbiome to megafauna across a range of environmental conditions (shallow sea to the deep ocean). Omics tools, such as eDNA metabarcoding can provide a cost-effective basis for biodiversity monitoring in large and remote conservation areas. Here we provide an overview of current omics applications for conservation planning and monitoring, with a focus on metabarcoding, metagenomics, and population genomics. Emerging approaches, including whole-genome sequencing, characterization of genomic architecture, epigenomics, and genomic vulnerability to climate change are also reviewed. We demonstrate that the operationalization of omics tools can enhance the design, monitoring, and management of MPAs and thus will play an important role in a modern and comprehensive blue economy strategy.

Integrating climate adaptation and biodiversity conservation in the global ocean.

The impacts of climate change and the socioecological challenges they present are ubiquitous and increasingly severe. Practical efforts to operationalize climate-responsive design and management in the global network of marine protected areas (MPAs) are required to ensure long-term effectiveness for safeguarding marine biodiversity and ecosystem services. Here, we review progress in integrating climate change adaptation into MPA design and management and provide eight recommendations to expedite this process. Climate-smart management objectives should become the default for all protected areas, and made into an explicit international policy target. Furthermore, incentives to use more dynamic management tools would increase the climate change responsiveness of the MPA network as a whole. Given ongoing negotiations on international conservation targets, now is the ideal time to proactively reform management of the global seascape for the dynamic climate-biodiversity reality.

Genomewide evidence of environmentally mediated secondary contact of European green crab (Carcinus maenas) lineages in eastern North America.

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 9,137 genomewide 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 < .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.

Temporal dynamics of genetic clines of invasive European green crab (Carcinus maenas) in eastern North America.

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 to 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.

Extensive hybridization following a large escape of domesticated Atlantic salmon in the Northwest Atlantic.

Domestication is rife with episodes of interbreeding between cultured and wild populations, potentially challenging adaptive variation in the wild. In Atlantic salmon, Salmo salar, the number of domesticated individuals far exceeds wild individuals, and escape events occur regularly, yet evidence of the magnitude and geographic scale of interbreeding resulting from individual escape events is lacking. We screened juvenile Atlantic salmon using 95 single nucleotide polymorphisms following a single, large aquaculture escape in the Northwest Atlantic and report the landscape-scale detection of hybrid and feral salmon (27.1%, 17/18 rivers). Hybrids were reproductively viable, and observed at higher frequency in smaller wild populations. Repeated annual sampling of this cohort revealed decreases in the presence of hybrid and feral offspring over time. These results link previous observations of escaped salmon in rivers with reports of population genetic change, and demonstrate the potential negative consequences of escapes from net-pen aquaculture on wild populations.

A climate-associated multispecies cryptic cline in the northwest Atlantic.

The spatial genetic structure of most species in the open marine environment remains largely unresolved. This information gap creates uncertainty in the sustainable management, recovery, and associated resilience of marine communities and our capacity to extrapolate beyond the few species for which such information exists. We document a previously unidentified multispecies biogeographic break aligned with a steep climatic gradient and driven by seasonal temperature minima in the northwest Atlantic. The coherence of this genetic break across our five study species with contrasting life histories suggests a pervasive macroecological phenomenon. The integration of this genetic structure with habitat suitability models and climate forecasts predicts significant variation in northward distributional shifts among populations and availability of suitable habitat in future oceans. The results of our integrated approach provide new perspective on how cryptic intraspecific diversity associated with climatic variation influences species and community response to climate change beyond simple poleward shifts.

hybriddetective: A workflow and package to facilitate the detection of hybridization using genomic data in r.

The ability to detect and characterize hybridization in nature has long been of interest to many fields of biology and often has direct implications for wildlife management and conservation. The capacity to identify the presence of hybridization, and quantify the numbers of individuals belonging to different hybrid classes, permits inference on the magnitude of, and timescale over which, hybridization has been or is occurring. Here, we present an r package and associated workflow developed for the detection, with estimates of efficiency and accuracy, of multigenerational hybrid individuals using genetic or genomic data in conjunction with the program newhybrids. This package includes functions for the identification and testing of diagnostic panels of markers, the simulation of multigenerational hybrids, and the quantification and visualization of the efficiency and accuracy with which hybrids can be detected. Overall, this package delivers a streamlined hybrid analysis platform, providing improvements in speed, ease of use and repeatability over current ad hoc approaches. The latest version of the package and associated documentation are available on GitHub (https://github.com/bwringe/hybriddetective).

parallelnewhybrid: an R package for the parallelization of hybrid detection using newhybrids.

Hybridization among populations and species is a central theme in many areas of biology, and the study of hybridization has direct applicability to testing hypotheses about evolution, speciation and genetic recombination, as well as having conservation, legal and regulatory implications. Yet, despite being a topic of considerable interest, the identification of hybrid individuals, and quantification of the (un)certainty surrounding the identifications, remains difficult. Unlike other programs that exist to identify hybrids based on genotypic information, newhybrids is able to assign individuals to specific hybrid classes (e.g. F1 , F2 ) because it makes use of patterns of gene inheritance within each locus, rather than just the proportions of gene inheritance within each individual. For each comparison and set of markers, multiple independent runs of each data set should be used to develop an estimate of the hybrid class assignment accuracy. The necessity of analysing multiple simulated data sets, constructed from large genomewide data sets, presents significant computational challenges. To address these challenges, we present parallelnewhybrid, an r package designed to decrease user burden when undertaking multiple newhybrids analyses. parallelnewhybrid does so by taking advantage of the parallel computational capabilities inherent in modern computers to efficiently and automatically execute separate newhybrids runs in parallel. We show that parallelization of analyses using this package affords users several-fold reductions in time over a traditional serial analysis. parallelnewhybrid consists of an example data set, a readme and three operating system-specific functions to execute parallel newhybrids analyses on each of a computer's c cores. parallelnewhybrid is freely available on the long-term software hosting site github (www.github.com/bwringe/parallelnewhybrid).

genepopedit: a simple and flexible tool for manipulating multilocus molecular data in R.

Advances in genetic sequencing technologies and techniques have made large, genome-wide data sets comprised of hundreds or even thousands of individuals and loci the norm rather than the exception even for nonmodel organisms. While such data present new opportunities for evaluating population structure and demographic processes, the large size of these genomic data sets brings new computational challenges for researchers needing to parse, convert and manipulate data often into a variety of software-specific formats required of genomic analyses. We developed genepopedit as a flexible tool for the manipulation of multilocus molecular data sets. Functionality can be divided among diagnostic-, manipulation-, sampling-, simulation-, and transformation-based tools. Metadata from large genomic data sets can be efficiently extracted, without the need to view data in a text-editing program. genepopedit provides tools to manipulate loci, individual samples and populations included in genomic data sets, in addition to the ability to convert directly to a variety of software formats. Functions are compiled as an R package, which can integrate into existing analysis workflows. Importantly, genepopedit provides a simple yet robust code-based tool for repeatable genomic data manipulation, which has been proven to be stable for data sets in excess of 200 000 SNPs. The latest version of the package and associated documentation are available on Github (github.com/rystanley/genepopedit).

Identifying patterns of dispersal, connectivity and selection in the sea scallop, Placopecten magellanicus, using RADseq-derived SNPs.

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 rangewide 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.

RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic.

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.

Range-wide parallel climate-associated genomic clines in Atlantic salmon.

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 single nucleotide polymorphisms 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.

Signatures of the collapse and incipient recovery of an overexploited marine ecosystem.

The Northwest Atlantic cod stocks collapsed in the early 1990s and have yet to recover, despite the subsequent establishment of a continuing fishing moratorium. Efforts to understand the collapse and lack of recovery have so far focused mainly on the dynamics of commercially harvested species. Here, we use data from a 33-year scientific trawl survey to determine to which degree the signatures of the collapse and recovery of the cod are apparent in the spatial and temporal dynamics of the broader groundfish community. Over this 33-year period, the groundfish community experienced four phases of change: (i) a period of rapid, synchronous biomass collapse in most species, (ii) followed by a regime shift in community composition with a concomitant loss of functional diversity, (iii) followed in turn by periods of slow compositional recovery, and (iv) slow biomass growth. Our results demonstrate how a community-wide perspective can reveal new aspects of the dynamics of collapse and recovery unavailable from the analysis of individual species or a combination of a small number of species. Overall, we found evidence that such community-level signals should be useful for designing more effective management strategies to ensure the persistence of exploited marine ecosystems.

Factors regulating early life history dispersal of Atlantic cod (Gadus morhua) from coastal Newfoundland.

To understand coastal dispersal dynamics of Atlantic cod (Gadus morhua), we examined spatiotemporal egg and larval abundance patterns in coastal Newfoundland. In recent decades, Smith Sound, Trinity Bay has supported the largest known overwintering spawning aggregation of Atlantic cod in the region. We estimated spawning and dispersal characteristics for the Smith Sound-Trinity Bay system by fitting ichthyoplankton abundance data to environmentally-driven, simplified box models. Results show protracted spawning, with sharply increased egg production in early July, and limited dispersal from the Sound. The model for the entire spawning season indicates egg export from Smith Sound is 13%•day(-1) with a net mortality of 27%•day(-1). Eggs and larvae are consistently found in western Trinity Bay with little advection from the system. These patterns mirror particle tracking models that suggest residence times of 10-20 days, and circulation models indicating local gyres in Trinity Bay that act in concert with upwelling dynamics to retain eggs and larvae. Our results are among the first quantitative dispersal estimates from Smith Sound, linking this spawning stock to the adjacent coastal waters. These results illustrate the biophysical interplay regulating dispersal and connectivity originating from inshore spawning of coastal northwest Atlantic.