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Understanding how marine organisms adapt to local environments is crucial for predicting how populations will respond to global climate change. The genomic basis, environmental factors and evolutionary processes involved in local adaptation are however not well understood. Here we use Atlantic herring, an abundant, migratory and widely distributed marine fish with substantial genomic resources, as a model organism to evaluate local adaptation. We examined genomic variation and its correlation with environmental variables across a broad environmental gradient, for 15 spawning aggregations in Atlantic Canada and the United States. We then compared our results with available genomic data of northeast Atlantic populations. We confirmed that population structure lies in a fraction of the genome including likely adaptive genetic variants of functional importance. We discovered 10 highly differentiated genomic regions distributed across four chromosomes. Nine regions show strong association with seasonal reproduction. One region, corresponding to a known inversion on chromosome 12, underlies a latitudinal pattern discriminating populations north and south of a biogeographic transition zone on the Scotian Shelf. Genome–environment associations indicate that winter seawater temperature best correlates with the latitudinal pattern of this inversion. The variation at two so‐called 'islands of divergence' related to seasonal reproduction appear to be private to the northwest Atlantic. Populations in the northwest and northeast Atlantic share variation at four of these divergent regions, simultaneously displaying significant diversity in haplotype composition at another four regions, which includes an undescribed structural variant approximately 7.7 Mb long on chromosome 8. Our results suggest that the timing and geographic location of spawning and early development may be under diverse selective pressures related to allelic fitness across environments. Our study highlights the role of genomic architecture, ancestral haplotypes and selection in maintaining adaptive divergence in species with large population sizes and presumably high gene flow. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Atlantic herring (Clupea harengus) and Pacific herring (C. pallasii) are sister species that split from a common ancestor about 2 million years ago. Balsfjord, a subarctic fjord in Northern Norway, harbors an outpost population of Pacific herring within the range of the Atlantic herring. We used whole genome sequencing to show that gene flow from Atlantic herring into the Balsfjord population has generated a stable hybrid population that has persisted for thousands of generations. The Atlantic herring ancestry in Balsfjord was estimated in the range 25–26%. The old age and large proportion of introgressed regions suggest there are no obvious genetic incompatibilities between species. Introgressed regions were widespread in the genome and large, with some in excess of 1 Mb, and they were overrepresented in low-recombination regions. We show that the distribution of introgressed material is non-random; introgressed sequence blocks in different individuals are shared more often than expected by chance. Furthermore, introgressed regions tend to show elevated divergence (F ST) between Atlantic and Pacific herring. Together, our results suggest that introgression of genetic material has facilitated adaptation in the Balsfjord population. The Balsfjord population provides a rare example of a stable interspecies hybrid population that has persisted over thousands of years. [ABSTRACT FROM AUTHOR]

The timing of reproduction influences key evolutionary and ecological processes in wild populations. Variation in reproductive timing may be an especially important evolutionary driver in the marine environment, where the high mobility of many species and few physical barriers to migration provide limited opportunities for spatial divergence to arise. Using genomic data collected from spawning aggregations of Pacific herring (Clupea pallasii) across 1600 km of coastline, we show that reproductive timing drives population structure in these pelagic fish. Within a specific spawning season, we observed isolation by distance, indicating that gene flow is also geographically limited over our study area. These results emphasize the importance of considering both seasonal and spatial variation in spawning when delineating management units for herring. On several chromosomes, we detected linkage disequilibrium extending over multiple Mb, suggesting the presence of chromosomal rearrangements. Spawning phenology was highly correlated with polymorphisms in several genes, in particular SYNE2, which influences the development of retinal photoreceptors in vertebrates. SYNE2 is probably within a chromosomal rearrangement in Pacific herring and is also associated with spawn timing in Atlantic herring (Clupea harengus). The observed genetic diversity probably underlies resource waves provided by spawning herring. Given the ecological, economic and cultural significance of herring, our results support that conserving intraspecific genetic diversity is important for maintaining current and future ecosystem processes. [ABSTRACT FROM AUTHOR]

Atlantic herring (Clupea harengus), a vital ecosystem component and target of the largest Northwest Atlantic pelagic fishery, undergo seasonal spawning migrations that result in elusive sympatric population structure. Herring spawn mostly in fall or spring, and genomic differentiation was recently detected between these groups. Here we used a subset of this differentiation, 66 single nucleotide polymorphisms (SNPs) to analyze the temporal dynamics of this local adaptation and the applicability of SNP subsets in stock assessment. We showed remarkable temporal stability of genomic differentiation corresponding to spawning season, between samples taken a decade apart (2005 N = 90 vs. 2014 N = 71) in the Gulf of St. Lawrence, and new evidence of limited interbreeding between spawning components. We also examined an understudied and overexploited herring population in Bras d'Or lake (N = 97); using highly reduced SNP panels (NSNPs > 6), we verified little‐known sympatric spawning populations within this unique inland sea. These results describe consistent local adaptation, arising from asynchronous reproduction in a migratory and dynamic marine species. Our research demonstrates the efficiency and precision of SNP‐based assessments of sympatric subpopulations; and indeed, this temporally stable local adaptation underlines the importance of such fine‐scale management practices. Herring spawn mostly in fall or spring, and genomic differentiation was recently detected between these groups. Here, we used a subset of this differentiation, 66 single nucleotide polymorphisms (SNPs) to analyze the temporal dynamics of this local adaptation and the applicability of SNP subsets in stock assessment. We showed remarkable temporal stability of this genomic differentiation between samples taken a decade apart (2005 N = 90 vs. 2014 N = 71) in the Gulf of St. Lawrence, alongside new evidence of limited interbreeding. [ABSTRACT FROM AUTHOR]

Whole-genome resequencing ( WGR) is a powerful method for addressing fundamental evolutionary biology questions that have not been fully resolved using traditional methods. WGR includes four approaches: the sequencing of individuals to a high depth of coverage with either unresolved or resolved haplotypes, the sequencing of population genomes to a high depth by mixing equimolar amounts of unlabelled-individual DNA (Pool-seq) and the sequencing of multiple individuals from a population to a low depth (lc WGR). These techniques require the availability of a reference genome. This, along with the still high cost of shotgun sequencing and the large demand for computing resources and storage, has limited their implementation in nonmodel species with scarce genomic resources and in fields such as conservation biology. Our goal here is to describe the various WGR methods, their pros and cons and potential applications in conservation biology. WGR offers an unprecedented marker density and surveys a wide diversity of genetic variations not limited to single nucleotide polymorphisms (e.g., structural variants and mutations in regulatory elements), increasing their power for the detection of signatures of selection and local adaptation as well as for the identification of the genetic basis of phenotypic traits and diseases. Currently, though, no single WGR approach fulfils all requirements of conservation genetics, and each method has its own limitations and sources of potential bias. We discuss proposed ways to minimize such biases. We envision a not distant future where the analysis of whole genomes becomes a routine task in many nonmodel species and fields including conservation biology. [ABSTRACT FROM AUTHOR]

Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroidstimulating hormone receptor (TSHR), the SOX11 transcription factor (SOX11), calmodulin (CALM), and estrogen receptor 2 (ESR2A), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5′ end of TSHR showed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations. [ABSTRACT FROM AUTHOR]

We developed and validated a mixed-stock analysis (MSA) method with 59 single-nucleotide polymorphisms selected from genome-wide data to assign individuals to populations in mixed-stock samples of Atlantic herring from the North and Baltic seas. We analysed 3734 herring from spawning locations and scientific catches of mixed feeding stocks to demonstrate a "one-fits-all" tool with unprecedented accuracy for monitoring spatio-temporal dynamics throughout a large geographical range with complex stock mixing. We re-analysed time-series data (2002–2021) and compared inferences about stock composition with estimates from morphological data. We show that contributions from the western Baltic spring-spawning stock complex, which is under management concern, have likely been overestimated. We also show that a genetically distinctive population of western Baltic autumn spawners, ascribed low fisheries importance, contributes non-negligible and potentially temporally increasing proportions to mixed-stock aggregations, calling for a re-evaluation of stock definitions. MSA data can be implemented in stock assessment and in a variety of applications, including marine ecosystem description, impact assessment of specific fleets, and stock-rebuilding plans. [ABSTRACT FROM AUTHOR]

We developed and validated a mixed-stock analysis (MSA) method with 59 single-nucleotide polymorphisms selected from genome-wide data to assign individuals to populations in mixed-stock samples of Atlantic herring from the North and Baltic seas. We analysed 3734 herring from spawning locations and scientific catches of mixed feeding stocks to demonstrate a "one-fits-all" tool with unprecedented accuracy for monitoring spatio-temporal dynamics throughout a large geographical range with complex stock mixing. We re-analysed time-series data (2002–2021) and compared inferences about stock composition with estimates from morphological data. We show that contributions from the western Baltic spring-spawning stock complex, which is under management concern, have likely been overestimated. We also show that a genetically distinctive population of western Baltic autumn spawners, ascribed low fisheries importance, contributes non-negligible and potentially temporally increasing proportions to mixed-stock aggregations, calling for a re-evaluation of stock definitions. MSA data can be implemented in stock assessment and in a variety of applications, including marine ecosystem description, impact assessment of specific fleets, and stock-rebuilding plans. [ABSTRACT FROM AUTHOR]

The underlying molecular mechanisms that determine long day versus short day breeders remain unknown in any organism. Atlantic herring provides a unique opportunity to examine the molecular mechanisms involved in reproduction timing, because both spring and autumn spawners exist within the same species. Although our previous whole genome comparisons revealed a strong association of TSHR alleles with spawning seasons, the functional consequences of these variants remain unknown. Here we examined the functional significance of six candidate TSHR mutations strongly associated with herring reproductive seasonality. We show that the L471M missense mutation in the spring-allele causes enhanced cAMP signaling. The best candidate non-coding mutation is a 5.2 kb retrotransposon insertion upstream of the TSHR transcription start site, near an open chromatin region, which is likely to affect TSHR expression. The insertion occurred prior to the split between Pacific and Atlantic herring and was lost in the autumn-allele. Our study shows that strongly associated coding and non-coding variants at the TSHR locus may both contribute to the regulation of seasonal reproduction in herring. Junfeng Chen et al. examine potential functional consequences of reproduction timing-associated TSHR alleles segregating in Atlantic herring. By comparing fish that spawn during the spring to those that spawn in the autumn, they find that the spring-allele is correlated with enhanced cAMP signaling and that both coding and non-coding variants in the TSHR locus contribute to seasonal reproduction. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]