How Fish Population Genomics Can Promote Sustainable Fisheries: A Road Map.

Maintenance of genetic diversity in marine fishes targeted by commercial fishing is a grand challenge for the future. Most of these species are abundant and therefore important for marine ecosystems and food security. Here, we present a road map of how population genomics can promote sustainable fisheries. In these species, the development of reference genomes and whole genome sequencing is key, because genetic differentiation at neutral loci is usually low due to large population sizes and gene flow. First, baseline allele frequencies representing genetically differentiated populations within species must be established. These can then be used to accurately determine the composition of mixed samples, forming the basis for population demographic analysis to inform sustainably set fish quotas. SNP-chip analysis is a cost-effective method for determining baseline allele frequencies and for population identification in mixed samples. Finally, we describe how genetic marker analysis can transform stock identification and management.

The genomic basis and environmental correlates of local adaptation in the Atlantic horse mackerel (Trachurus trachurus).

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.

A baseline for the genetic stock identification of Atlantic herring, Clupea harengus, in ICES Divisions 6.a, 7.b-c.

Atlantic herring in International Council for Exploration of the Sea (ICES) Divisions 6.a, 7.b-c comprises at least three populations, distinguished by temporal and spatial differences in spawning, which have until recently been managed as two stocks defined by geographical delineators. Outside of spawning the populations form mixed aggregations, which are the subject of acoustic surveys. The inability to distinguish the populations has prevented the development of separate survey indices and separate stock assessments. A panel of 45 single-nucleotide polymorphisms, derived from whole-genome sequencing, were used to genotype 3480 baseline spawning samples (2014-2021). A temporally stable baseline comprising 2316 herring from populations known to inhabit Division 6.a was used to develop a genetic assignment method, with a self-assignment accuracy greater than 90%. The long-term temporal stability of the assignment model was validated by assigning archive (2003-2004) baseline samples (270 individuals) with a high level of accuracy. Assignment of non-baseline samples (1514 individuals) from Divisions 6.a, 7.b-c indicated previously unrecognized levels of mixing of populations outside of the spawning season. The genetic markers and assignment models presented constitute a 'toolbox' that can be used for the assignment of herring caught in mixed survey and commercial catches in Division 6.a into their population of origin with a high level of accuracy.

Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci.

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.

A novel method of microsatellite genotyping-by-sequencing using individual combinatorial barcoding.

This study examines the potential of next-generation sequencing based 'genotyping-by-sequencing' (GBS) of microsatellite loci for rapid and cost-effective genotyping in large-scale population genetic studies. The recovery of individual genotypes from large sequence pools was achieved by PCR-incorporated combinatorial barcoding using universal primers. Three experimental conditions were employed to explore the possibility of using this approach with existing and novel multiplex marker panels and weighted amplicon mixture. The GBS approach was validated against microsatellite data generated by capillary electrophoresis. GBS allows access to the underlying nucleotide sequences that can reveal homoplasy, even in large datasets and facilitates cross laboratory transfer. GBS of microsatellites, using individual combinatorial barcoding, is potentially faster and cheaper than current microsatellite approaches and offers better and more data.

Next Gen Pop Gen: implementing a high-throughput approach to population genetics in boarfish (Capros aper).

The recently developed approach for microsatellite genotyping by sequencing (GBS) using individual combinatorial barcoding was further improved and used to assess the genetic population structure of boarfish (Capros aper) across the species' range. Microsatellite loci were developed de novo and genotyped by next-generation sequencing. Genetic analyses of the samples indicated that boarfish can be subdivided into at least seven biological units (populations) across the species' range. Furthermore, the recent apparent increase in abundance in the northeast Atlantic is better explained by demographic changes within this area than by influx from southern or insular populations. This study clearly shows that the microsatellite GBS approach is a generic, cost-effective, rapid and powerful method suitable for full-scale population genetic studies-a crucial element for assessment, sustainable management and conservation of valuable biological resources.

New molecular tools for the identification of 2 endangered smooth-hound sharks, Mustelus mustelus and Mustelus punctulatus.

The smooth-hounds represent a significant proportion of the elasmobranch catch in the Adriatic basin of the Mediterranean Sea, where the common (Mustelus mustelus) and blackspotted (Mustelus punctulatus) smooth-hounds co-occur. The 2 species share several morphological and morphometric characters that lead to frequent misidentification. In order to provide information useful for their species identification, we performed a morphological identification of several Mustelus specimens to select individuals unambiguously attributed to 1 of the 2 species, and assayed these with 3 new molecular tests. First, we developed and validated a mitochondrial DNA assay based on species-specific amplification of the cytochrome c oxidase subunit 1 (COI). Second, a fragment analysis of 15 microsatellites cross-amplified from several triakid species was performed to identify diagnostic loci. Finally, a length difference was identified in the internal transcribed spacer 2 (ITS2) region and a diagnostic test based on its amplification was established. All the samples classified morphologically as M. mustelus and M. punctulatus showed a species-specific profile using all the 3 molecular tests. In addition, cross-amplification of microsatellites allowed identification of 9 highly polymorphic loci that will be useful for the study of the mating system and population differentiation of the 2 species.