Genomics for monitoring and understanding species responses to global climate change.

All life forms across the globe are experiencing drastic changes in environmental conditions as a result of global climate change. These environmental changes are happening rapidly, incur substantial socioeconomic costs, pose threats to biodiversity and diminish a species' potential to adapt to future environments. Understanding and monitoring how organisms respond to human-driven climate change is therefore a major priority for the conservation of biodiversity in a rapidly changing environment. Recent developments in genomic, transcriptomic and epigenomic technologies are enabling unprecedented insights into the evolutionary processes and molecular bases of adaptation. This Review summarizes methods that apply and integrate omics tools to experimentally investigate, monitor and predict how species and communities in the wild cope with global climate change, which is by genetically adapting to new environmental conditions, through range shifts or through phenotypic plasticity. We identify advantages and limitations of each method and discuss future research avenues that would improve our understanding of species' evolutionary responses to global climate change, highlighting the need for holistic, multi-omics approaches to ecosystem monitoring during global climate change.

Design and validation of a high-density single nucleotide polymorphism array for the Eastern oyster (Crassostrea virginica).

Dense single nucleotide polymorphism (SNP) arrays are essential tools for rapid high-throughput genotyping for many genetic analyses, including genomic selection and high-resolution population genomic assessments. We present a high-density (200 K) SNP array developed for the Eastern oyster (Crassostrea virginica), which is a species of significant aquaculture production and restoration efforts throughout its native range. SNP discovery was performed using low-coverage whole-genome sequencing of 435 F1 oysters from families from 11 founder populations in New Brunswick, Canada. An Affymetrix Axiom Custom array was created with 219,447 SNPs meeting stringent selection criteria and validated by genotyping more than 4,000 oysters across 2 generations. In total, 144,570 SNPs had a call rate >90%, most of which (96%) were polymorphic and were distributed across the Eastern oyster reference genome, with similar levels of genetic diversity observed in both generations. Linkage disequilibrium was low (maximum r2 ∼0.32) and decayed moderately with increasing distance between SNP pairs. Taking advantage of our intergenerational data set, we quantified Mendelian inheritance errors to validate SNP selection. Although most of SNPs exhibited low Mendelian inheritance error rates overall, with 72% of called SNPs having an error rate of <1%, many loci had elevated Mendelian inheritance error rates, potentially indicating the presence of null alleles. This SNP panel provides a necessary tool to enable routine application of genomic approaches, including genomic selection, in C. virginica selective breeding programs. As demand for production increases, this resource will be essential for accelerating production and sustaining the Canadian oyster aquaculture industry.

Long-distance migration is a major factor driving local adaptation at continental scale in Coho salmon.

Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species' homing behaviour may promote the establishment of local adaptation. We genotyped 7829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. The results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidate single nucleotide polymorphisms associated with long-distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.

Re-evaluating Coho salmon (Oncorhynchus kisutch) conservation units in Canada using genomic data.

Conservation units (CUs) are important tools for supporting the implementation of standardized management practices for exploited species. Following the adoption of the Wild Salmon Policy in Canada, CUs were defined for Pacific salmon based on characteristics related to ecotype, life history and genetic variation using microsatellite markers as indirect measures of local adaptation. Genomic data sets have the potential to improve the definition of CUs by reducing variance around estimates of population genetic parameters, thereby increasing the power to detect more subtle patterns of population genetic structure and by providing an opportunity to incorporate adaptive information more directly with the identification of variants putatively under selection. We used one of the largest genomic data sets recently published for a nonmodel species, comprising 5662 individual Coho salmon (Oncorhynchus kisutch) from 149 sampling locations and a total of 24,542 high-quality SNPs obtained using genotyping-by-sequencing and mapped to the Coho salmon reference genome to (1) evaluate the current delineation of CUs for Coho in Canada and (2) compare patterns of population structure observed using neutral and outlier loci from genotype-environment association analyses to determine whether separate CUs that capture adaptive diversity are needed. Our results reflected CU boundaries on the whole, with the majority of sampling locations managed in the same CU clustering together within genetic groups. However, additional groups that are not currently represented by CUs were also uncovered. We observed considerable overlap in the genetic clusters identified using neutral or candidate loci, indicating a general congruence in patterns of genetic variation driven by local adaptation and gene flow in this species. Consequently, we suggest that the current CU boundaries for Coho salmon are largely well-suited for meeting the Canadian Wild Salmon Policy's objective of defining biologically distinct groups, but we highlight specific areas where CU boundaries may be refined.

Evolving spatial conservation prioritization with intraspecific genetic data.

Spatial conservation prioritization (SCP) is a planning framework used to identify new conservation areas on the basis of the spatial distribution of species, ecosystems, and their services to human societies. The ongoing accumulation of intraspecific genetic data on a variety of species offers a way to gain knowledge of intraspecific genetic diversity and to estimate several population characteristics useful in conservation, such as dispersal and population size. Here, we review how intraspecific genetic data have been integrated into SCP and highlight their potential for identifying conservation area networks that represent intraspecific genetic diversity comprehensively and that ensure the long-term persistence of biodiversity in the face of global change.

Individual-based eco-evolutionary models for understanding adaptation in changing seas.

As climate change threatens species' persistence, predicting the potential for species to adapt to rapidly changing environments is imperative for the development of effective conservation strategies. Eco-evolutionary individual-based models (IBMs) can be useful tools for achieving this objective. We performed a literature review to identify studies that apply these tools in marine systems. Our survey suggested that this is an emerging area of research fuelled in part by developments in modelling frameworks that allow simulation of increasingly complex ecological, genetic and demographic processes. The studies we identified illustrate the promise of this approach and advance our understanding of the capacity for adaptation to outpace climate change. These studies also identify limitations of current models and opportunities for further development. We discuss three main topics that emerged across studies: (i) effects of genetic architecture and non-genetic responses on adaptive potential; (ii) capacity for gene flow to facilitate rapid adaptation; and (iii) impacts of multiple stressors on persistence. Finally, we demonstrate the approach using simple simulations and provide a framework for users to explore eco-evolutionary IBMs as tools for understanding adaptation in changing seas.

Incorporating putatively neutral and adaptive genomic data into marine conservation planning.

The availability of genomic data for an increasing number of species makes it possible to incorporate evolutionary processes into conservation plans. Recent studies show how genetic data can inform spatial conservation prioritization (SCP), but they focus on metrics of diversity and distinctness derived primarily from neutral genetic data sets. Identifying adaptive genetic markers can provide important information regarding the capacity for populations to adapt to environmental change. Yet, the effect of including metrics based on adaptive genomic data into SCP in comparison to more widely used neutral genetic metrics has not been explored. We used existing genomic data on a commercially exploited species, the giant California sea cucumber (Parastichopus californicus), to perform SCP for the coastal region of British Columbia (BC), Canada. Using a RAD-seq data set for 717 P. californicus individuals across 24 sampling locations, we identified putatively adaptive (i.e., candidate) single nucleotide polymorphisms (SNPs) based on genotype-environment associations with seafloor temperature. We calculated various metrics for both neutral and candidate SNPs and compared SCP outcomes with independent metrics and combinations of metrics. Priority areas varied depending on whether neutral or candidate SNPs were used and on the specific metric used. For example, targeting sites with a high frequency of warm-temperature-associated alleles to support persistence under future warming prioritized areas in the southern coastal region. In contrast, targeting sites with high expected heterozygosity at candidate loci to support persistence under future environmental uncertainty prioritized areas in the north. When combining metrics, all scenarios generated intermediate solutions, protecting sites that span latitudinal and thermal gradients. Our results demonstrate that distinguishing between neutral and adaptive markers can affect conservation solutions and emphasize the importance of defining objectives when choosing among various genomic metrics for SCP.

Incorporación de Datos Genómicos Putativamente Neutros y Adaptativos dentro de la Planeación de la Conservación Marina Resumen La disponibilidad de los datos genómicos para un número creciente de especies posibilita la incorporación de los procesos evolutivos dentro de los planes de conservación. Los estudios recientes muestran cómo los datos genéticos pueden informar a la priorización de la conservación espacial (PCE) pero tienden a enfocarse más en las medidas de la diversidad y la distinción derivadas principalmente de los conjuntos de datos genéticos neutrales. La identificación de los marcadores genéticos adaptativos puede proporcionar información importante con respecto a la capacidad de las poblaciones para adaptarse al cambio ambiental. Aun así, no se ha explorado el efecto de la inclusión de las medidas basadas en los datos genéticos adaptativos dentro de la PCE y cómo se comparan con las medidas genéticas neutrales de uso más amplio. Usamos datos genómicos existentes sobre una especie de explotación comercial, el pepino de mar gigante de California (Parastichopus californicus), para realizar la PCE para la región costera de la Columbia Británica (BC) en Canadá. Usamos un conjunto de datos RAD-seq para 717 individuos de la especie P. californicus en 24 localidades de muestreo para identificar los polimorfismos de un solo nucleótido (PSNs) putativamente adaptativos (es decir, candidatos) con base en las asociaciones genotipo-ambiente manifestadas con la temperatura del fondo marino. Calculamos varias medidas para los PSNs neutrales y los PSNs candidatos y comparamos los resultados de la PCE con medidas independientes y con combinaciones de medidas. Las áreas prioritarias variaron dependiendo de si se usaron los SNP neutrales o los candidatos y de la medida específica que se utilizó. Por ejemplo, enfocarse en sitios con una frecuencia alta de alelos asociados con agua cálida para fortalecer la persistencia frente al futuro calentamiento prioriza las áreas en la región del sur de la costa. Al contrario, enfocarse en sitios con una alta heterocigosidad esperada en los loci de los candidatos para fortalecer la persistencia frente a la incertidumbre ambiental prioriza las áreas en la parte norte de la costa. Cuando combinamos las medidas, todos los escenarios generaron soluciones intermedias, protegiendo así los sitios que abarcan gradientes latitudinales y gradientes térmicos. Nuestros resultados demuestran que la distinción entre los marcadores neutrales y los adaptativos puede afectar las soluciones de conservación y también enfatizan la importancia de la definición de los objetivos cuando se elige entre varias medidas genómicas para la PCE.

Seascape genomics of eastern oyster (Crassostrea virginica) along the Atlantic coast of Canada.

Interactions between environmental factors and complex life-history characteristics of marine organisms produce the genetic diversity and structure observed within species. Our main goal was to test for genetic differentiation among eastern oyster populations from the coastal region of Canadian Maritimes against expected genetic homogeneity caused by historical events, taking into account spatial and environmental (temperature, salinity, turbidity) variation. This was achieved by genotyping 486 individuals originating from 13 locations using RADSeq. A total of 11,321 filtered SNPs were used in a combination of population genomics and environmental association analyses. We revealed significant neutral genetic differentiation (mean F ST = 0.009) between sampling locations, and the occurrence of six major genetic clusters within the studied system. Redundancy analyses (RDAs) revealed that spatial and environmental variables explained 3.1% and 4.9% of the neutral genetic variation and 38.6% and 12.2% of the putatively adaptive genetic variation, respectively. These results indicate that these environmental factors play a role in the distribution of both neutral and putatively adaptive genetic diversity in the system. Moreover, polygenic selection was suggested by genotype-environment association analysis and significant correlations between additive polygenic scores and temperature and salinity. We discuss our results in the context of their conservation and management implications for the eastern oyster.

Putatively adaptive genetic variation in the giant California sea cucumber (Parastichopus californicus) as revealed by environmental association analysis of restriction-site associated DNA sequencing data.

Understanding the spatial scale of local adaptation and the factors associated with adaptive diversity are important objectives for ecology and evolutionary biology, and have significant implications for effective conservation and management of wild populations and natural resources. In this study, we used an environmental association analysis to identify important bioclimatic variables correlated with putatively adaptive genetic variation in a benthic marine invertebrate-the giant California sea cucumber (Parastichopus californicus)-spanning coastal British Columbia and southeastern Alaska. We used a redundancy analysis (RDA) with 3,699 single nucleotide polymorphisms (SNPs) obtained using RAD sequencing to detect candidate markers associated with 11 bioclimatic variables, including sea bottom and surface conditions, across two spatial scales (entire study area and within subregions). At the broadest scale, RDA revealed 59 candidate SNPs, 86% of which were associated with mean bottom temperature. Similar patterns were identified when population structure was accounted for. Additive polygenic scores, which provide a measure of the cumulative signal across all candidate SNPs, were strongly correlated with mean bottom temperature, consistent with spatially varying selection across a thermal gradient. At a finer scale, 23 candidate SNPs were detected, primarily associated with surface salinity (26%) and bottom current velocity (17%). Our findings suggest that environmental variables may play a role as drivers of spatially varying selection for P. californicus. These results provide context for future studies to evaluate the genetic basis of local adaptation in P. californicus and help inform the relevant scales and environmental variables for in situ field studies of putative adaptive variation in marine invertebrates.

Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus).

Marine populations are typically characterized by weak genetic differentiation due to the potential for long-distance dispersal favouring high levels of gene flow. However, strong directional advection of water masses or retentive hydrodynamic forces can influence the degree of genetic exchange among marine populations. To determine the oceanographic drivers of genetic structure in a highly dispersive marine invertebrate, the giant California sea cucumber (Parastichopus californicus), we first tested for the presence of genetic discontinuities along the coast of North America in the northeastern Pacific Ocean. Then, we tested two hypotheses regarding spatial processes influencing population structure: (i) isolation by distance (IBD: genetic structure is explained by geographic distance) and (ii) isolation by resistance (IBR: genetic structure is driven by ocean circulation). Using RADseq, we genotyped 717 individuals from 24 sampling locations across 2,719 neutral SNPs to assess the degree of population differentiation and integrated estimates of genetic variation with inferred connectivity probabilities from a biophysical model of larval dispersal mediated by ocean currents. We identified two clusters separating north and south regions, as well as significant, albeit weak, substructure within regions (FST  = 0.002, p = .001). After modelling the asymmetric nature of ocean currents, we demonstrated that local oceanography (IBR) was a better predictor of genetic variation (R2  = .49) than geographic distance (IBD) (R2  = .18), and directional processes played an important role in shaping fine-scale structure. Our study contributes to the growing body of literature identifying significant population structure in marine systems and has important implications for the spatial management of P. californicus and other exploited marine species.