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Chromosomal inversions are associated with local adaptation in many species. However, questions regarding how they are formed, maintained and impact various other evolutionary processes remain elusive. Here, using a large genomic dataset of long-read and short-read sequencing, we ask these questions in one of the most abundant vertebrates on Earth, the Atlantic herring. This species has four megabase-sized inversions associated with ecological adaptation that correlate with water temperature. The S and N inversion alleles at these four loci dominate in the southern and northern parts, respectively, of the species distribution in the North Atlantic Ocean. By determining breakpoint coordinates of the four inversions and the structural variations surrounding them, we hypothesize that these inversions are formed by ectopic recombination between duplicated sequences immediately outside of the inversions. We show that these are old inversions (>1 MY), albeit formed after the split between the Atlantic herring and its sister species, the Pacific herring. There is evidence for extensive gene flux between inversion alleles at all four loci. The large Ne of herring combined with the common occurrence of opposite homozygotes across the species distribution has allowed effective purifying selection to prevent the accumulation of genetic load and repeats within the inversions. The Atlantic herring has four megabase-sized inversions associated with ecological adaptation. This study untangles their evolutionary history, showing that considerable genetic exchange between alleles has occurred and that effective purifying selection has prevented the accumulation of genetic load.

Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here, we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.

Sustainable fisheries management is important for the continued harvest of the world's marine resources, especially as they are increasingly challenged by a range of climatic and anthropogenic factors. One of the pillars of sustainable fisheries management is the accurate identification of the biological units, i.e., populations. Here, we developed and implemented a genetic baseline for Atlantic herring harvested in the Norwegian offshore fisheries to investigate the validity of the current management boundaries. This was achieved by genotyping > 15,000 herring from the northern European seas, including samples of all the known populations in the region, with a panel of population-informative SNPs mined from existing genomic resources. The final genetic baseline consisted of ~1000 herring from 12 genetically distinct populations. We thereafter used the baseline to investigate mixed catches from the North and Norwegian Seas, revealing that each management area consisted of multiple populations, as previously suspected. However, substantial numbers (up to 50% or more within a sample) of herring were found outside of their expected management areas, e.g., North Sea autumn-spawning herring north of 62° N (average = 19.2%), Norwegian spring-spawning herring south of 62° N (average = 13.5%), and western Baltic spring-spawning herring outside their assumed distribution area in the North Sea (average = 20.0%). Based upon these extensive observations, we conclude that the assessment and management areas currently in place for herring in this region need adjustments to reflect the populations present. Furthermore, we suggest that for migratory species, such as herring, a paradigm shift from using static geographic stock boundaries towards spatial dynamic boundaries is needed to meet the requirements of future sustainable management regimes.

Understanding how populations adapt to their environment is increasingly important to prevent biodiversity loss due to overexploitation and climate change. Here we studied the population structure and genetic basis of local adaptation of Atlantic horse mackerel, a commercially and ecologically important marine fish that has one of the widest distributions in the eastern Atlantic. We analyzed whole‐genome sequencing and environmental data of samples collected from the North Sea to North Africa and the western Mediterranean Sea. Our genomic approach indicated low population structure with a major split between the Mediterranean Sea and the Atlantic Ocean and between locations north and south of mid‐Portugal. Populations from the North Sea are the most genetically distinct in the Atlantic. We discovered that most population structure patterns are driven by a few highly differentiated putatively adaptive loci. Seven loci discriminate the North Sea, two the Mediterranean Sea, and a large putative inversion (9.9 Mb) on chromosome 21 underlines the north–south divide and distinguishes North Africa. A genome–environment association analysis indicates that mean seawater temperature and temperature range, or factors correlated to them, are likely the main environmental drivers of local adaptation. Our genomic data broadly support the current stock divisions, but highlight areas of potential mixing, which require further investigation. Moreover, we demonstrate that as few as 17 highly informative SNPs can genetically discriminate the North Sea and North African samples from neighboring populations. Our study highlights the importance of both, life history and climate‐related selective pressures in shaping population structure patterns in marine fish. It also supports that chromosomal rearrangements play a key role in local adaptation with gene flow. This study provides the basis for more accurate delineation of the horse mackerel stocks and paves the way for improving stock assessments.

The common smoothhound, Mustelus mustelus, is an epibenthic species targeted by fisheries around the world driven by the increasing demand for shark products. Given the wide-spread occurrence of this species and corresponding lack of molecular data in many areas of said distribution, baseline molecular assessments of this commercially important shark may contribute to finer-scale analyses in areas in which this species is targeted. Therefore, population genetic analyses were conducted along the East Atlantic, from the Mediterranean Sea to the south-east coast of Africa, using microsatellite markers and the mitochondrial control region (mtCR). Overall, M. mustelus displayed low to moderate genetic diversity, with the Mediterranean populations appearing to exhibit the lowest mitochondrial diversity, and the west African populations displaying the lowest nuclear diversity. Microsatellite analysis indicated strong genetic differentiation between the three regions, with finer-scale population structure in each region, without correlation between genetic and geographical distance. For the mtCR sequences, a total of 18 haplotypes were identified, with a high degree of divergence discernable between the regions, largely in accordance with the microsatellite data. The study documents a remarkable level of population isolation across a vast area, suggesting little or no present-day connectivity among extant populations. The findings may serve as an essential baseline for global population management and commercial traceability of this threatened shark.

Europe has a long tradition of exploiting marine fishes and is promoting marine economic activity through its Blue Growth strategy. This increase in anthropogenic pressure, along with climate change, threatens the biodiversity of fishes and food security. Here, we examine the conservation status of 1,020 species of European marine fishes and identify factors that contribute to their extinction risk. Large fish species (greater than 1.5 m total length) are most at risk; half of these are threatened with extinction, predominantly sharks, rays and sturgeons. This analysis was based on the latest International Union for Conservation of Nature (IUCN) European regional Red List of marine fishes, which was coherent with assessments of the status of fish stocks carried out independently by fisheries management agencies: no species classified by IUCN as threatened were considered sustainable by these agencies. A remarkable geographic divergence in stock status was also evident: in northern Europe, most stocks were not overfished, whereas in the Mediterranean Sea, almost all stocks were overfished. As Europe proceeds with its sustainable Blue Growth agenda, two main issues stand out as needing priority actions in relation to its marine fishes: the conservation of marine fish megafauna and the sustainability of Mediterranean fish stocks. Assessing the conservation status of 1,020 European marine fishes reveals half of large (>1.5 m) fishes are threatened with extinction and stock status diverges geographically: almost all Mediterranean stock is overfished, most northern European stock is not.

To assess whether Mytilus edulis is selective in its secretion of byssus threads and entrapment of gastropods, experiments were conducted in laboratory aquaria and in the field. Exposure to dogwhelks (Nucella lapillus) or their effluent induced mussels to produce twice as many byssus threads as mussels exposed only to winkles (Littorina littorea) or those exposed only to seawater. There were no significant differences among treatments in the area over which byssus threads were secreted. Significantly more byssus threads were attached to the shells of dogwhelks than to winkles. Laboratory experiments produced broadly similar results to those in the field, but the level of response in the laboratory was greater. It is concluded that byssus threads were attached selectively to dogwhelks and that they may serve as a defence against predation.

Nature Ecology & Evolution 1, 0170 (2017); published 26 May 2017; corrected 12 June 2017. In the original version of this Article, the European Commission was mistakenly included as an affiliation for Christos D. Maravelias. His contribution to this work was exclusively completed while at the Hellenic Centre for Marine Research.

Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here, we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.

Understanding how populations adapt to local environments is increasingly important to prevent biodiversity loss due to climate change. Here we examined whole-genome variation of twelve Atlantic horse mackerel samples from the North Sea to North Africa, and the western Mediterranean Sea. This marine migratory benthopelagic fish is one of the most widely distributed and commercially important species in the eastern Atlantic. We found low population structure at neutral loci, but high differentiation at adaptive loci distinguishing the western Mediterranean and the North Sea populations from other Atlantic locations. Candidate genes distinctive of the Mediterranean include a green-sensitive-opsin harbouring two missense mutations that might fine-tune the spectral sensitivity to blue-green light conditions. Candidate genes characteristic of the North Sea could play a critical role in cold tolerance (energy metabolism and cell membrane structure) and increased sensitivity to odours, presumably to compensate reduced visibility in turbid waters. We also discovered a putative chromosomal inversion (9.9 Mb) that follows a climate-related latitudinal cline with a break near mid Portugal. Genome-environment association analysis indicated that seawater-dissolved oxygen concentration and temperature are likely the main environmental drivers of local adaptation. Our genomic data broadly supports the current stock divisions, but recommends revision of the western and southern stock boundaries. We developed a reduced SNP panel that genetically discriminate the North Sea and North Africa from neighbouring populations. Our study highlights the importance of life history and chromosomal inversions in adaptation with gene flow, and the complexity of evolutionary and ecological processes involved in local adaptation. Competing Interest Statement The authors have declared no competing interest. Footnotes * Typos, Supplementary Figures citation in text