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.

Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well‐known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well‐mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco‐geographic features across which connectivity can be measured.

Summary: The European sea bass (Dicentrarchus labrax L.) is a marine fish of key economic and cultural importance in Europe. It is now more an aquaculture than a fisheries species (>96% of the production in 2016), although modern rearing techniques date back only from the late 1980s. It also has high interest for evolutionary studies, as it is composed of two semispecies (Atlantic and Mediterranean lineages) that have come into secondary contact following the last glaciation. Based on quantitative genetics studies of most traits of interest over the past 10–15 years, selective breeding programs are now applied to this species, which is at the beginning of its domestication process. The availability of a good quality reference genome has accelerated the development of new genomic resources, including SNP arrays that will enable genomic selection to improve genetic gain. There is a need to improve feed efficiency, both for economic and environmental reasons, but this will require novel phenotyping approaches. Further developments will likely focus on the understanding of genotype‐by‐environment interactions, which will be important both for efficient breeding of farmed stocks and for improving knowledge of the evolution of natural populations. At the interface between both, the domestication process must be better understood to improve production and also to fully evaluate the possible impact of aquaculture escapees on wild populations. The latter is an important question for all large‐scale aquaculture productions.

When incompletely isolated taxa coexist in a patchy environment (e.g. mosaic hybrid zones, host-race complexes), patterns of variation may differ between selected traits/genes and neutral markers. While the genetic structure of selected traits/loci tends to coincide with habitat variables (producing Genetic-Environment Association or GEA), genetic differentiation at neutral loci unlinked to any selected locus rather depends on geographic connectivity at a large scale (e.g. Isolation-By-Distance or IBD), although these loci often display GEA at a small scale. This discrepancy has been repeatedly taken as evidence for parallel primary divergence driven by local adaptation. We argue that this interpretation needs to be addressed more thoroughly by considering the alternative hypothesis that speciation was initiated in allopatry and secondary introgression has subsequently erased the signal of past differentiation at neutral loci. We present a model of neutral introgression after secondary contact in a mosaic hybrid zone, which describes how GEAs dissipate with time and how neutral variation self-organizes according to the environmental and geographic structures. We show that although neutral loci can be affected by environmental selection, they are often more affected by history and connectivity: the neutral structure retains the initial geographic separation more than it correlates with the environment during the colonization and introgression phases, and then converges to a migration-drift balance, the most frequent outcome of which is GEA at a local scale but IBD at a large scale. This is the exact pattern usually attributed to parallel ecological speciation. Introgression is heterogeneous in space and depends on the landscape structure (e.g. it is faster in small patches, which are more impacted by immigration). Furthermore, there is no directionality in the association and it is possible to observe reversed GEAs between distant regions. We argue that the history of differentiation should ideally be reconstructed with selected loci or neutral loci linked to them, not neutral ones, and review some case studies for which the hypothesis of a long co-existence of co-adapted genetic backgrounds might have been refuted too hastily.

Parallel divergence across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of replicate sympatric species pairs of Lake Whitefish (normal benthic and dwarf limnetic) characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared with the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3,000–4,000 generations) asymmetrical secondary contact between expanding postglacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation has emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.