Predicting the future of our oceans-Evaluating genomic forecasting approaches in marine species.

Climate change is restructuring biodiversity on multiple scales and there is a pressing need to understand the downstream ecological and genomic consequences of this change. Recent advancements in the field of eco-evolutionary genomics have sought to include evolutionary processes in forecasting species' responses to climate change (e.g., genomic offset), but to date, much of this work has focused on terrestrial species. Coastal and offshore species, and the fisheries they support, may be even more vulnerable to climate change than their terrestrial counterparts, warranting a critical appraisal of these approaches in marine systems. First, we synthesize knowledge about the genomic basis of adaptation in marine species, and then we discuss the few examples where genomic forecasting has been applied in marine systems. Next, we identify the key challenges in validating genomic offset estimates in marine species, and we advocate for the inclusion of historical sampling data and hindcasting in the validation phase. Lastly, we describe a workflow to guide marine managers in incorporating these predictions into the decision-making process.

Genomic signatures and correlates of widespread population declines in salmon.

Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified. Genomic data provide an opportunity to isolate drivers of change and even predict future vulnerabilities. Atlantic salmon (Salmo salar) populations have declined range-wide, but factors responsible are poorly understood. Here, we reconstruct changes in effective population size (Ne) in recent decades for 172 range-wide populations using a linkage-based method. Across the North Atlantic, Ne has significantly declined in >60% of populations and declines are consistently temperature-associated. We identify significant polygenic associations with decline, involving genomic regions related to metabolic, developmental, and physiological processes. These regions exhibit changes in presumably adaptive diversity in declining populations consistent with contemporary shifts in body size and phenology. Genomic signatures of widespread population decline and associated risk scores allow direct and potentially predictive links between population fitness and genotype, highlighting the power of genomic resources to assess population vulnerability.

Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions.

Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and nonmigratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the >100 000-year-old trans-Atlantic separation of Atlantic cod. The long-term persistence of these inversions indicates that they are maintained by selection, possibly facilitated by coevolution of genes underlying complex traits. Our data suggest that migratory behaviour is derived from more stationary, ancestral ecotypes. Overall, we identify several large genomic regions-each containing hundreds of genes-likely involved in the maintenance of genomic divergence in Atlantic cod on both sides of the Atlantic Ocean.

Genomic evidence of hybridization between two independent invasions of European green crab (Carcinus maenas) in the Northwest Atlantic.

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 cytochrome c oxidase subunit I mitochondrial DNA (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.

Structural and functional connectivity of marine fishes within a semi-enclosed Newfoundland fjord.

The interplay between structural connectivity (i.e. habitat continuity) and functional connectivity (i.e. dispersal probability) in marine fishes was examined in a coastal fjord (Holyrood Pond, Newfoundland, Canada) that is completely isolated from the North Atlantic Ocean for most of the year. Genetic differentiation was described in three species (rainbow smelt Osmerus mordax, white hake Urophycis tenuis and Atlantic cod Gadus morhua) with contrasting life histories using seven to 10 microsatellite loci and a protein-coding locus, PanI (G. morhua). Analysis of microsatellite differentiation indicated clear genetic differences between the fjord and coastal regions; however, the magnitude of difference was no more elevated than adjacent bays and was not enhanced by the fjord's isolation. Osmerus mordax was characterized by the highest structure overall with moderate differentiation between the fjord and St Mary's Bay (F(ST)c.0.047). In contrast, U. tenuis and G. morhua displayed weak differentiation (F(ST) < 0.01). Nonetheless, these populations did demonstrate high rates (< 75%) of Bayesian self-assignment. Furthermore, elevated differentiation was observed at the PanI locus in G. morhua between the fjord and other coastal locations. Interestingly, locus-specific genetic differentiation and expected heterozygosity were negatively associated in O. mordax, in contrast to the positive associations observed in U. tenuis and G. morhua. Gene flow in these species is apparently unencumbered by limited structural connectivity, yet the observed differentiation suggests that population structuring exists over small scales despite high dispersal potential.

Estimating contemporary early life-history dispersal in an estuarine fish: integrating molecular and otolith elemental approaches.

Dispersal during the early life history of the anadromous rainbow smelt, Osmerus mordax, was examined using assignment testing and mixture analysis of multilocus genotypes and otolith elemental composition. Six spawning areas and associated estuarine nurseries were sampled throughout southeastern Newfoundland. Samples of adults and juveniles isolated by > 25 km displayed moderate genetic differentiation (F(ST) ~ 0.05), whereas nearby (< 25 km) spawning and nursery samples displayed low differentiation (F(ST) < 0.01). Self-assignment and mixture analysis of adult spawning samples supported the hypothesis of independence of isolated spawning locations (> 80% self-assignment) with nearby runs self-assigning at rates between 50 % and 70%. Assignment and mixture analysis of juveniles using adult baselines indicated high local recruitment at several locations (70-90%). Nearby (< 25 km) estuaries at the head of St Mary's Bay showed mixtures of individuals (i.e. 20-40% assignment to adjacent spawning location). Laser ablation inductively coupled mass spectrometry transects across otoliths of spawning adults of unknown dispersal history were used to estimate dispersal among estuaries across the first year of life. Single-element trends and multivariate discriminant function analysis (Sr:Ca and Ba:Ca) classified the majority of samples as estuarine suggesting limited movement between estuaries (< 0.5%). The mixtures of juveniles evident in the genetic data at nearby sites and a lack of evidence of straying in the otolith data support a hypothesis of selective mortality of immigrants. If indeed selective mortality of immigrants reduces the survivorship of dispersers, estimates of dispersal in marine environments that neglect survival may significantly overestimate gene flow.