Population and seascape genomics of a critically endangered benthic elasmobranch, the blue skate Dipturus batis

Abstract

The blue skate (Dipturus batis) has a patchy distribution across the North-East Atlantic Ocean, largely restricted to occidental seas around the British Isles following fisheries-induced population declines and extirpations. The viability of remnant populations remains uncertain and could be impacted by continued fishing and by-catch pressure, and the projected impacts of climate change. We genotyped 503 samples of D. batis, obtained opportunistically from the widest available geographic range, across 6 350 single nucleotide polymorphisms (SNPs) using a reduced-representation sequencing approach. Genotypes were used to assess the species' contemporary population structure, estimate effective population sizes and identify putative signals of selection in relation to environmental variables using a seascape genomics approach. We identified genetic discontinuities between inshore (British Isles) and offshore (Rockall and Faroe Island) populations, with differentiation most pronounced across the deep waters of the Rockall Trough. Effective population sizes were largest in the Celtic Sea and Rockall, but low enough to be of potential conservation concern among Scottish and Faroese sites. Among the 21 candidate SNPs under positive selection was one significantly correlated with environmental variables predicted to be affected by climate change, including bottom temperature, salinity and pH. The paucity of well-annotated elasmobranch genomes precluded us from identifying a putative function for this SNP. Nevertheless, our findings suggest that climate change could inflict a strong selective force upon remnant populations of D. batis, further constraining its already-restricted habitat. Furthermore, the results provide fundamental insights on the distribution, behaviour and evolutionary biology of D. batis in the North-East Atlantic that will be useful for the establishment of conservation actions for this and other critically endangered elasmobranchs.

Keywords: Dipturus batis; blue skate; climate change; conservation; population genomics; seascape genomics.

FIGURE 1

Sampling locations across the North‐East Atlantic Ocean for 503 blue skate Dipturus batis that were used for population genomic analyses. Site names are abbreviated for the Celtic Sea (CS), West Coast Scotland (WCS), Northern Scotland (NS), Rockall (RK), the Faroe Bank (FB) and the Faroe Shelf (FS)

FIGURE 2

Results from the Bayesian clustering algorithm implemented in STRUCTURE, visualized using CLUMPAK for K = 2 (top) and K = 3 (bottom), for 57 Dipturus batis samples collected from the Celtic Sea (CS), West Coast Scotland (WCS), North Scotland (NS), Rockall (RK), the Faroe Shelf (FS) and the Faroe Bank (FB). Each individual is represented by a vertical line with the proportion of assignment to a cluster indicated by two or three colours

FIGURE 3

Discriminant analysis of principal component (DAPC, adegenet) plots depicting the variation among 493 Dipturus batis samples genotyped across 6 350 SNPs. Top: variation between two clusters inferred using find.clusters, where the blue (left) cluster contains all 69 samples from Rockall and the red (right) cluster contains the remaining 424 samples from the UK and Faroe Island sites. Bottom: variation among samples grouped by their sampling locations, with 95% inertia ellipses shown for each group. Site names are abbreviated for the Celtic Sea (CS), West Coast Scotland (WCS), Northern Scotland (NS), Rockall (RK), the Faroe Bank (FB) and the Faroe Shelf (FS)

FIGURE 4

Principal component analysis depicting the variation among sites based on 34 environmental variables. Site names are abbreviated for the Celtic Sea (CS), West Coast Scotland (WCS), Northern Scotland (NS), Rockall (RK), the Faroe Bank (FB) and the Faroe Shelf (FS)