European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation

Abstract

The European sea bass (Dicentrarchus labrax) is a temperate-zone euryhaline teleost of prime importance for aquaculture and fisheries. This species is subdivided into two naturally hybridizing lineages, one inhabiting the north-eastern Atlantic Ocean and the other the Mediterranean and Black seas. Here we provide a high-quality chromosome-scale assembly of its genome that shows a high degree of synteny with the more highly derived teleosts. We find expansions of gene families specifically associated with ion and water regulation, highlighting adaptation to variation in salinity. We further generate a genome-wide variation map through RAD-sequencing of Atlantic and Mediterranean populations. We show that variation in local recombination rates strongly influences the genomic landscape of diversity within and differentiation between lineages. Comparing predictions of alternative demographic models to the joint allele-frequency spectrum indicates that genomic islands of differentiation between sea bass lineages were generated by varying rates of introgression across the genome following a period of geographical isolation.

Figure 1. Collinear blocks showing the overall degree of synteny between the European sea bass (D. labrax) genome and seven other publicly available teleost genomes represented outside the sea bass chromosomal ring.

From the inner to the outer layer: G. aculeatus, O. latipes, T. nigroviridis, D. rerio, O. niloticus, T. rubripes and G. morhua. Sea bass chromosomes (LGn) show conserved synteny with the assemblies of G. aculeatus, O. latipes, T. nigroviridis and D. rerio, while O. niloticus, T. rubripes and G. morhua are still scattered into many ungrouped scaffolds as reflected by tracks of different colours along the chromosomes. The colour code is species-specific. Blocks of collinearity between sea bass chromosomes are represented by grey inner links. Red inner links represent blocks of collinearity containing claudin genes.

Figure 2. Phylogenetic tree based on 621 1:1 high-quality orthologous protein-coding genes from 20 sequenced fish genomes, showing the relationships between European sea bass (D. labrax) and other fish species (half of which belong to the Series Percomorpha).

Node support is indicated by bootstrap values. The lancelet (Branchiostoma floridae) was used as the outgroup. The shaded box indicates the total number of gene copies across the five expanded gene families involved in euryhalinity for highly euryhaline (red), euryhaline (green) and stenohaline (blue) species.

Figure 3. Comparison of claudin gene synteny between sea bass LG 13 and 14 and other vertebrate chromosomes including human.

Chromosome blocks containing claudin genes (2) are blue coloured, other synteny blocks are coloured in red (1), yellow (3), orange (4M) and green (4F).

Figure 4. Distribution of population genetic parameters calculated in 150-kb windows across the different chromosomes of sea bass genome (x refers to LGx, and not to a sexual chromosome).

(a) Chromosomal patterns of nucleotide diversity (π) in the Atlantic (blue) and Mediterranean (red) lineages of D. labrax. (b) Genomic patterns of divergence between D. labrax and D. punctatus measured as the proportion of fixed differences per bp (d_f). (c) Chromosomal patterns of recombination (ρ/kb) in D. labrax, averaged across Atlantic and Mediterranean lineages, alternately coloured in grey and orange across chromosomes. (d) Genomic landscape of differentiation (F_ST) between Atlantic and Mediterranean lineages.

Figure 5. Population structure and demographic history of the European sea bass, D. labrax.

(a) Principal component analysis of the Atlantic (ATL) and Mediterranean (MED) sea bass lineages including the outgroup species D. punctatus. (b) The joint allele-frequency spectrum (AFS) for the ATL and MED populations, showing the count of derived allele for 109,300 oriented SNPs in 45 individuals from each population. (c) The secondary contact with two migration rate model (SC2m), including 10 parameters: the ancestral population size (N_a), the ATL and MED population sizes after splitting (N_ATL and N_MED), the splitting time (T_S) and the time since secondary contact (T_SC). Locus-effective migration rate from ATL into MED (m_ATL>MED) and in the opposite direction (m_MED>ATL) can take two free values in proportions p and 1−p. (d) The maximum-likelihood AFS obtained under the SC2m model.