The genomic architecture underlying ecological divergence and ecological speciation with gene flow is still largely unknown for most organisms. One central question is whether divergence is genome-wide or localized in 'genomic mosaics' during early stages when gene flow is still pronounced. Empirical work has so far been limited, and the relative impacts of gene flow and natural selection on genomic patterns have not been fully explored. Here, we use ecotypes of Atlantic cod to investigate genomic patterns of diversity and population differentiation in a natural system characterized by high gene flow and large effective population sizes, properties which theoretically could restrict divergence in local genomic regions. We identify a genomic region of strong population differentiation, extending over approximately 20 cM, between pairs of migratory and stationary ecotypes examined at two different localities. Furthermore, the region is characterized by markedly reduced levels of genetic diversity in migratory ecotype samples. The results highlight the genomic region, or 'genomic island', as potentially associated with ecological divergence and suggest the involvement of a selective sweep. Finally, we also confirm earlier findings of localized genomic differentiation in three other linkage groups associated with divergence among eastern Atlantic populations. Thus, although the underlying mechanisms are still unknown, the results suggest that 'genomic mosaics' of differentiation may even be found under high levels of gene flow and that marine fishes may provide insightful model systems for studying and identifying initial targets of selection during ecological divergence.

Accurate prediction of species distribution shifts in the face of climate change requires a sound understanding of population diversity and local adaptations. Previous modeling has suggested that global warming will lead to increased abundance of Atlantic cod (Gadus morhua) in the ocean around Greenland, but the dynamics of earlier abundance fluctuations are not well understood. We applied a retrospective spatiotemporal population genomics approach to examine the temporal stability of cod population structure in this region and to search for signatures of divergent selection over a 78-year period spanning major demographic changes. Analyzing >900 gene-associated single nucleotide polymorphisms in 847 individuals, we identified four genetically distinct groups that exhibited varying spatial distributions with considerable overlap and mixture. The genetic composition had remained stable over decades at some spawning grounds, whereas complete population replacement was evident at others. Observations of elevated differentiation in certain genomic regions are consistent with adaptive divergence between the groups, indicating that they may respond differently to environmental variation. Significantly increased temporal changes at a subset of loci also suggest that adaptation may be ongoing. These findings illustrate the power of spatiotemporal population genomics for revealing biocomplexity in both space and time and for informing future fisheries management and conservation efforts.

Little is known about how quickly natural populations adapt to changes in their environment and how temporal and spatial variation in selection pressures interact to shape patterns of genetic diversity. We here address these issues with a series of genome scans in four overfished populations of Atlantic cod (Gadus morhua) studied over an 80-year period. Screening of >1000 gene-associated single-nucleotide polymorphisms (SNPs) identified 77 loci that showed highly elevated levels of differentiation, likely as an effect of directional selection, in either time, space or both. Exploratory analysis suggested that temporal allele frequency shifts at certain loci may correlate with local temperature variation and with life history changes suggested to be fisheries induced. Interestingly, however, largely nonoverlapping sets of loci were temporal outliers in the different populations and outliers from the 1928 to 1960 period showed almost complete stability during later decades. The contrasting microevolutionary trajectories among populations resulted in sequential shifts in spatial outliers, with no locus maintaining elevated spatial differentiation throughout the study period. Simulations of migration coupled with observations of temporally stable spatial structure at neutral loci suggest that population replacement or gene flow alone could not explain all the observed allele frequency variation. Thus, the genetic changes are likely to at least partly be driven by highly dynamic temporally and spatially varying selection. These findings have important implications for our understanding of local adaptation and evolutionary potential in high gene flow organisms and underscore the need to carefully consider all dimensions of biocomplexity for evolutionarily sustainable management.

Genomic signatures associated with population divergence, speciation and the evolutionary mechanisms responsible for these are key research topics in evolutionary biology.Evolutionary radiations and parallel evolution have offered opportunities to study the role of the environment by providing replicates of ecologically driven speciation. Here, we apply an extension of the parallel evolution framework to study replicates of ecological speciation where multiple species went through a process of population divergence during the colonization of a common environmental gradient. We used the conditions offered by the North Sea -Baltic Sea environmental transition zone and found clear evidence of population structure linked to the Baltic Sea salinity gradient in four flatfish species. We found highly heterogeneous signatures of population divergence within and between species, and no evidence of parallel genomic architecture across species associated with the divergence.Analyses of demographic history suggest that Baltic Sea lineages are older than the age of the Baltic Sea itself. In most cases, divergence appears to involve reticulated demography through secondary contact, and our analyses revealed that genomic patterns of divergence were likely the result of a combination of effects from past isolation and subsequent adaptation to a new environment. In one case, we identified two large structural variants associated with the environmental gradient, where populations were inferred to have diverged in the presence of gene flow. Our results highlight the heterogeneous genomic effects associated with complex interplays of evolutionary forces, and stress the importance of genomic background for studies of parallel evolution. 2006), but so far the comparative framework has not been extended with the use of higher genome coverage.Here, we used a comparative population genomic approach to study the evolutionary processes involved during the colonization of the Baltic Sea. We studied population structure of four closely related (but genetically isolated) flatfish species: turbot (Scophthalmus maximus), common dab (Limanda limanda), European plaice (Pleuronectes platessa) andEuropean flounder (Platichthys flesus). These species were considered replicates of population divergence and were analysed independently. Our analyses showed heterogeneous genetic patterns of North Sea (NS) -Baltic Sea (BS) differentiation across species, both for magnitudes and genomic patterns of differentiation. Most of the genetic differences found were strongly associated with the environmental gradient of the NBTZ.However, the majority of the genomic regions underlying the NS-BS divergence were not shared between species. The timing of divergence between NS-BS populations was inferred to be five to ten times older than the age of the Baltic Sea. In three species, population divergence was inferred to involve past isolation followed by a secondary contact phase, and our analyses revealed that highly diverged genomic regions were likely the result of ...

Genetic data have great potential for improving fisheries management by identifying the fundamental management units—that is, the biological populations—and their mixing. However, so far, the number of practical cases of marine fisheries management using genetics has been limited. Here, we used Atlantic cod in the Baltic Sea to demonstrate the applicability of genetics to a complex management scenario involving mixing of two genetically divergent populations. Specifically, we addressed several assumptions used in the current assessment of the two populations. Through analysis of 483 single nucleotide polymorphisms (SNPs) distributed across the Atlantic cod genome, we confirmed that a model of mechanical mixing, rather than hybridization and introgression, best explained the pattern of genetic differentiation. Thus, the fishery is best monitored as a mixed‐stock fishery. Next, we developed a targeted panel of 39 SNPs with high statistical power for identifying population of origin and analyzed more than 2,000 tissue samples collected between 2011 and 2015 as well as 260 otoliths collected in 2003/2004. These data provided high spatial resolution and allowed us to investigate geographical trends in mixing, to compare patterns for different life stages and to investigate temporal trends in mixing. We found similar geographical trends for the two time points represented by tissue and otolith samples and that a recently implemented geographical management separation of the two populations provided a relatively close match to their distributions. In contrast to the current assumption, we found that patterns of mixing differed between juveniles and adults, a signal likely linked to the different reproductive dynamics of the two populations. Collectively, our data confirm that genetics is an operational tool for complex fisheries management applications. We recommend focussing on developing population assessment models and fisheries management frameworks to capitalize fully on the additional information offered by genetically assisted fisheries monitoring.