Genomic survey of edible cockle (Cerastoderma edule) in the Northeast Atlantic: A baseline for sustainable management of its wild resources

Abstract

Knowledge on correlations between environmental factors and genome divergence between populations of marine species is crucial for sustainable management of fisheries and wild populations. The edible cockle (Cerastoderma edule) is a marine bivalve distributed along the Northeast Atlantic coast of Europe and is an important resource from both commercial and ecological perspectives. We performed a population genomics screening using 2b-RAD genotyping on 9309 SNPs localized in the cockle's genome on a sample of 536 specimens pertaining to 14 beds in the Northeast Atlantic Ocean to analyse the genetic structure with regard to environmental variables. Larval dispersal modelling considering species behaviour and interannual/interseasonal variation in ocean conditions was carried out as an essential background to which compare genetic information. Cockle populations in the Northeast Atlantic displayed low but significant geographical differentiation between populations (F _ST = 0.0240; p < 0.001), albeit not across generations. We identified 742 and 36 outlier SNPs related to divergent and balancing selection in all the geographical scenarios inspected, and sea temperature and salinity were the main environmental correlates suggested. Highly significant linkage disequilibrium was detected at specific genomic regions against the very low values observed across the whole genome. Two main genetic groups were identified, northwards and southwards of French Brittany. Larval dispersal modelling suggested a barrier for larval dispersal linked to the Ushant front that could explain these two genetic clusters. Further genetic subdivision was observed using outlier loci and considering larval advection. The northern group was divided into the Irish/Celtic Seas and the English Channel/North Sea, while the southern group was divided into three subgroups. This information represents the baseline for the management of cockles, designing conservation strategies, founding broodstock for depleted beds and producing suitable seed for aquaculture production.

Keywords: 2b‐RAD; adaptive variation; fisheries management; genetic structure; larval dispersal modelling.

FIGURE 1

Study area for Cerastoderma edule genetic analysis and larval dispersal modelling. Ocean bathymetry is shaded in blue. Summer surface currents are schematically represented by magenta‐coloured arrows (see section Study Area for a detailed description and references). Locations of fronts are depicted by purple dotted lines (CSF, Celtic Sea Front; UF, Ushant Front). Location of the C. edule beds for the genetic analysis are shown in dark red (see Table 1 for location codes) and particle release locations for larval dispersal modelling are shown in yellow and numbered from 1 to 51. Location codes in panel A are detailed in Table 1

FIGURE 2

Linkage disequilibrium (r ²) with regard to physical distance between pairs of markers in the Cerastoderma edule genome in a representative cockle bed (Noia) and using the whole data set from the Atlantic Area

FIGURE 3

Population structure of Cerastoderma edule in the studied region using fastSTRUCTURE for the complete data set (a) and the divergent outlier data set (b) taking into account all beds studied. Each vertical bar represents one individual, and the colour proportion for each bar represents the posterior probability of assignment of each individual to the different clusters (K) inferred by the programme (K = 2 and K = 9 for a and b respectively). Codes are shown in Table 1

FIGURE 4

Discriminant analysis of principal components plots of Cerastoderma edule. The weight of retained discriminant analysis (DA) eigenvalues representing >90% of variance are shown on right bottom box. Results using the complete data set (a), neutral data set (b) and divergent outlier data set (c) are shown. Codes are given in Table 1

FIGURE 5

Maximum‐likelihood trees inferred by TREEMIX without (left) and with (right) migration events included. Migration events are depicted as heatmap coloured arrows from yellow to red. Population code colours: northern region (red), southern region (blue)

FIGURE 6

Redundancy analyses (RDA) plots of Cerastoderma edule samples from the studied area using the different genetic data sets (complete: complete data set; neutral: neutral data set; divergent: divergent outlier data set) and seasons (reproductive period, winter and summer) taking into account all landscape variables (a) and only abiotic factors (b). BSS, bottom shear stress; SBS, sea bottom salinity; SSS, sea surface salinity; SST, sea surface temperature. Population code colours: northern region (red), southern region (blue)

FIGURE 7

Mean larval connectivity pathways for April to September from 2016 to 2018 releases at depths of 1, 15 and 30 m. The direction of the arrows indicates the direction of larval transport, and the colour and thickness of the connection display the strength of the connection