Rare, long-distance dispersal underpins genetic connectivity in the pink sea fan, Eunicella verrucosa

Abstract

Characterizing patterns of genetic connectivity in marine species is of critical importance given the anthropogenic pressures placed on the marine environment. For sessile species, population connectivity can be shaped by many processes, such as pelagic larval duration, oceanographic boundaries and currents. This study combines restriction-site associated DNA sequencing (RADseq) and passive particle dispersal modelling to delineate patterns of population connectivity in the pink sea fan, Eunicella verrucosa, a temperate octocoral. Individuals were sampled from 20 sites covering most of the species' northeast Atlantic range, and a site in the northwest Mediterranean Sea to inform on connectivity across the Atlantic-Mediterranean transition. Using 7510 neutral SNPs, a geographic cline of genetic clusters was detected, partitioning into Ireland, Britain, France, Spain (Atlantic), and Portugal and Spain (Mediterranean). Evidence of significant inbreeding was detected at all sites, a finding not detected in a previous study of this species based on microsatellite loci. Genetic connectivity was characterized by an isolation by distance pattern (IBD) (r ² = 0.78, p < 0.001), which persisted across the Mediterranean-Atlantic boundary. In contrast, exploration of ancestral population assignment using the program ADMIXTURE indicated genetic partitioning across the Bay of Biscay, which we suggest represents a natural break in the species' range, possibly linked to a lack of suitable habitat. As the pelagic larval duration (PLD) is unknown, passive particle dispersal simulations were run for 14 and 21 days. For both modelled PLDs, inter-annual variations in particle trajectories suggested that in a long-lived, sessile species, range-wide IBD is driven by rare, longer dispersal events that act to maintain gene flow. These results suggest that oceanographic patterns may facilitate range-wide stepping-stone genetic connectivity in E. verrucosa and highlight that both oceanography and natural breaks in a species' range should be considered in the designation of ecologically coherent MPA networks.

Keywords: RAD sequencing; genetic structure; oceanographic modelling; octocoral; single nucleotide polymorphism.

FIGURE 1

Map of the study area and sampling sites (n = 20) across the northeast Atlantic and Mediterranean. See Table 1 for detailed information about sites.

FIGURE 2

Discriminant analysis of principal components (DAPC): (a) LD 1 and LD 2, (b) LD 1 and LD 3. Each point represents an individual and colours denote from which region the individual originates.

FIGURE 3

Admixture analysis for K = 2 to K = 5. Each bar represents an individual and each colour denotes which genetic cluster that individual has been assigned to. The plots show clustering patterns with no prior on location (see Appendix S1 for further details).

FIGURE 4

Final particle displacement trajectories for a 14‐day PLD simulation (a) and a 21‐day simulation (b). Each release site is denoted by a triangle (see corresponding key).

FIGURE 5

Final trajectory plots showing interannual variation in the distance and direction of dispersal trajectories for a 14‐day (a–d) and a 21‐day (e–h) drift simulation length.

FIGURE 6

Final particle trajectory plots showing examples of infrequent, longer dispersal between years for a 14‐day (a–d) and a 21‐day (e–h) drift simulation length.

FIGURE 7

Isolation by distance (IBD) analysis of pairwise comparisons of geographic distances (km) and F _ST between all sampling sites.