Aquaculture-driven evolution of the salmon louse mtDNA genome.

Resistance toward the antiparasitic pyrethroid, deltamethrin, is reported in the Atlantic salmon louse (Lepeophtheirus salmonis salmonis), a persistent ectoparasite of farmed and wild salmonids. The resistance mechanism is linked to mitochondrial DNA (mtDNA), where genetic markers for resistance have been identified. Here, we investigated how widespread pyrethroid use in aquaculture may have influenced mtDNA variation in lice, and the dispersion of resistant haplotypes across the North Atlantic, using historical (2000-2002 "pre-resistance") and contemporary (2014-2017 "post-resistance") samples. To study this, we sequenced ATPase 6 and cytochrome b, genotyped two genetic markers for deltamethrin resistance, and genotyped microsatellites as "neutral" controls of potential population bottlenecks. Overall, we observed a modest reduction in mtDNA diversity in the period 2000-2017, but no reduction in microsatellite variation was observed. The reduction in mtDNA variation was especially distinct in two of the contemporary samples, fixed for one and two haplotypes, respectively. By contrast, all historical samples consisted of close to one mtDNA haplotype per individual. No population genetic structure was detected among the historical samples for mtDNA nor microsatellites. By contrast, significant population genetic differentiation was observed for mtDNA among some of the contemporary samples. However, the observed population genetic structure was tightly linked with the pattern of deltamethrin resistance, and we therefore conclude that it primarily reflects the transient mosaic of pyrethroid usage in time and space. Two historically undetected mtDNA haplotypes dominated in the contemporary samples, both of which were linked to deltamethrin resistance, demonstrating primarily two origins of deltamethrin resistance in the North Atlantic. Collectively, these data demonstrate that the widespread use of pyrethroids in commercial aquaculture has substantially altered the patterns of mtDNA diversity in lice across the North Atlantic, and that long-distance dispersion of resistance is rapid due to high level of genetic connectivity that is observed in this species.

Global, regional, and cryptic population structure in a high gene-flow transatlantic fish.

Lumpfish (Cyclopterus lumpus) is a transatlantic marine fish displaying large population sizes and a high potential for dispersal and gene-flow. These features are expected to result in weak population structure. Here, we investigated population genetic structure of lumpfish throughout its natural distribution in the North Atlantic using two approaches: I) 4,393 genome wide SNPs and 95 individuals from 10 locations, and II) 139 discriminatory SNPs and 1,669 individuals from 40 locations. Both approaches identified extensive population genetic structuring with a major split between the East and West Atlantic and a distinct Baltic Sea population, as well as further differentiation of lumpfish from the English Channel, Iceland, and Greenland. The discriminatory loci displayed ~2-5 times higher divergence than the genome wide approach, revealing further evidence of local population substructures. Lumpfish from Isfjorden in Svalbard were highly distinct but resembled most fish from Greenland. The Kattegat area in the Baltic transition zone, formed a previously undescribed distinct genetic group. Also, further subdivision was detected within North America, Iceland, West Greenland, Barents Sea, and Norway. Although lumpfish have considerable potential for dispersal and gene-flow, the observed high levels of population structuring throughout the Atlantic suggests that this species may have a natal homing behavior and local populations with adaptive differences. This fine-scale population structure calls for consideration when defining management units for exploitation of lumpfish stocks and in decisions related to sourcing and moving lumpfish for cleaner fish use in salmonid aquaculture.

Not that clean: Aquaculture-mediated translocation of cleaner fish has led to hybridization on the northern edge of the species' range.

Translocation and introduction of non-native organisms can have major impacts on local populations and ecosystems. Nevertheless, translocations are common practices in agri- and aquaculture. Each year, millions of wild-caught wrasses are transported large distances to be used as cleaner fish for parasite control in marine salmon farms. Recently, it was documented that translocated cleaner fish are able to escape and reproduce with local wild populations. This is especially a challenge in Norway, which is the world's largest salmon producer. Here, a panel of 84 informative SNPs was developed to identify the presence of nonlocal corkwing wrasse (Symphodus melops) escapees and admixed individuals in wild populations in western Norway. Applying this panel to ~2000 individuals, escapees and hybrids were found to constitute up to 20% of the local population at the northern edge of the species' distribution. The introduction of southern genetic material at the northern edge of the species distribution range has altered the local genetic composition and could obstruct local adaptation and further range expansion. Surprisingly, in other parts of the species distribution where salmon farming is also common, few escapees and hybrids were found. Why hybridization seems to be common only in the far north is discussed in the context of demographic and transport history. However, the current lack of reporting of escapes makes it difficult to evaluate possible causes for why some aquaculture-dense areas have more escapees and hybrids than others. The results obtained in this study, and the observed high genomic divergence between the main export and import regions, puts the sustainability of mass translocation of nonlocal wild wrasse into question and suggests that the current management regime needs re-evaluation.

Genetic response to human-induced habitat changes in the marine environment: A century of evolution of European sprat in Landvikvannet, Norway.

Habitat changes represent one of the five most pervasive threats to biodiversity. However, anthropogenic activities also have the capacity to create novel niche spaces to which species respond differently. In 1880, one such habitat alterations occurred in Landvikvannet, a freshwater lake on the Norwegian coast of Skagerrak, which became brackish after being artificially connected to the sea. This lake is now home to the European sprat, a pelagic marine fish that managed to develop a self-recruiting population in barely few decades. Landvikvannet sprat proved to be genetically isolated from the three main populations described for this species; that is, Norwegian fjords, Baltic Sea, and the combination of North Sea, Kattegat, and Skagerrak. This distinctness was depicted by an accuracy self-assignment of 89% and a highly significant F ST between the lake sprat and each of the remaining samples (average of ≈0.105). The correlation between genetic and environmental variation indicated that salinity could be an important environmental driver of selection (3.3% of the 91 SNPs showed strong associations). Likewise, Isolation by Environment was detected for salinity, although not for temperature, in samples not adhering to an Isolation by Distance pattern. Neighbor-joining tree analysis suggested that the source of the lake sprat is in the Norwegian fjords, rather than in the Baltic Sea despite a similar salinity profile. Strongly drifted allele frequencies and lower genetic diversity in Landvikvannet compared with the Norwegian fjords concur with a founder effect potentially associated with local adaptation to low salinity. Genetic differentiation (F ST) between marine and brackish sprat is larger in the comparison Norway-Landvikvannet than in Norway-Baltic, which suggests that the observed divergence was achieved in Landvikvannet in some 65 generations, that is, 132 years, rather than gradually over thousands of years (the age of the Baltic Sea), thus highlighting the pace at which human-driven evolution can happen.

Genome wide analysis reveals genetic divergence between Goldsinny wrasse populations.

BACKGROUND: Marine fish populations are often characterized by high levels of gene flow and correspondingly low genetic divergence. This presents a challenge to define management units. Goldsinny wrasse (Ctenolabrus rupestris) is a heavily exploited species due to its importance as a cleaner-fish in commercial salmonid aquaculture. However, at the present, the population genetic structure of this species is still largely unresolved. Here, full-genome sequencing was used to produce the first genomic reference for this species, to study population-genomic divergence among four geographically distinct populations, and, to identify informative SNP markers for future studies. RESULTS: After construction of a de novo assembly, the genome was estimated to be highly polymorphic and of ~600Mbp in size. 33,235 SNPs were thereafter selected to assess genomic diversity and differentiation among four populations collected from Scandinavia, Scotland, and Spain. Global FST among these populations was 0.015-0.092. Approximately 4% of the investigated loci were identified as putative global outliers, and ~ 1% within Scandinavia. SNPs showing large divergence (FST > 0.15) were picked as candidate diagnostic markers for population assignment. One hundred seventy-three of the most diagnostic SNPs between the two Scandinavian populations were validated by genotyping 47 individuals from each end of the species' Scandinavian distribution range. Sixty-nine of these SNPs were significantly (p < 0.05) differentiated (mean FST_173_loci = 0.065, FST_69_loci = 0.140). Using these validated SNPs, individuals were assigned with high probability (≥ 94%) to their populations of origin. CONCLUSIONS: Goldsinny wrasse displays a highly polymorphic genome, and substantial population genomic structure. Diversifying selection likely affects population structuring globally and within Scandinavia. The diagnostic loci identified now provide a promising and cost-efficient tool to investigate goldsinny wrasse populations further.

Genetic analysis redraws the management boundaries for the European sprat.

Sustainable fisheries management requires detailed knowledge of population genetic structure. The European sprat is an important commercial fish distributed from Morocco to the Arctic circle, Baltic, Mediterranean, and Black seas. Prior to 2018, annual catch advice on sprat from the International Council for the Exploration of the Sea (ICES) was based on five putative stocks: (a) North Sea, (b) Kattegat-Skagerrak and Norwegian fjords, (c) Baltic Sea, (d) West of Scotland-southern Celtic Seas, and (e) English Channel. However, there were concerns that the sprat advice on stock size estimates management plan inadequately reflected the underlying biological units. Here, we used ddRAD sequencing to develop 91 SNPs that were thereafter used to genotype approximately 2,500 fish from 40 locations. Three highly distinct and relatively homogenous genetic groups were identified: (a) Norwegian fjords; (b) Northeast Atlantic including the North Sea, Kattegat-Skagerrak, Celtic Sea, and Bay of Biscay; and (c) Baltic Sea. Evidence of genetic admixture and possibly physical mixing was detected in samples collected from the transition zone between the North and Baltic seas, but not between any of the other groups. These results have already been implemented by ICES with the decision to merge the North Sea and the Kattegat-Skagerrak sprat to be assessed as a single unit, thus demonstrating that genetic data can be rapidly absorbed to align harvest regimes and biological units.

"A cleaner break": Genetic divergence between geographic groups and sympatric phenotypes revealed in ballan wrasse (Labrus bergylta).

Capture and long-distance translocation of cleaner fish to control lice infestations on marine salmonid farms has the potential to influence wild populations via overexploitation in source regions, and introgression in recipient regions. Knowledge of population genetic structure is therefore required. We studied the genetic structure of ballan wrasse, a phenotypically diverse and extensively used cleaner fish, from 18 locations in Norway and Sweden, and from Galicia, Spain, using 82 SNP markers. We detected two very distinct genetic groups in Scandinavia, northwestern and southeastern. These groups were split by a stretch of sandy beaches in southwest Norway, representing a habitat discontinuity for this rocky shore associated benthic egg-laying species. Wrasse from Galicia were highly differentiated from all Scandinavian locations, but more similar to northwestern than southeastern locations. Distinct genetic differences were observed between sympatric spotty and plain phenotypes in Galicia, but not in Scandinavia. The mechanisms underlying the geographic patterns between phenotypes are discussed, but not identified. We conclude that extensive aquaculture-mediated translocation of ballan wrasse from Sweden and southern Norway to western and middle Norway has the potential to mix genetically distinct populations. These results question the sustainability of the current cleaner fish practice.

Lack of recognition of genetic biodiversity: International policy and its implementation in Baltic Sea marine protected areas.

Genetic diversity is needed for species' adaptation to changing selective pressures and is particularly important in regions with rapid environmental change such as the Baltic Sea. Conservation measures should consider maintaining large gene pools to maximize species' adaptive potential for long-term survival. In this study, we explored concerns regarding genetic variation in international and national policies that governs biodiversity and evaluated if and how such policy is put into practice in management plans governing Baltic Sea Marine Protected Areas (MPAs) in Sweden, Finland, Estonia, and Germany. We performed qualitative and quantitative textual analysis of 240 documents and found that agreed international and national policies on genetic biodiversity are not reflected in management plans for Baltic Sea MPAs. Management plans in all countries are largely void of goals and strategies for genetic biodiversity, which can partly be explained by a general lack of conservation genetics in policies directed toward aquatic environments.

Living on the edge: reconstructing the genetic history of the Finnish wolf population.

BACKGROUND: Many western European carnivore populations became almost or completely eradicated during the last ~200 years, but are now recovering. Extirpation of wolves started in Finland in the 19th century, and for more than 150 years the population size of wolves has remained small. To investigate historical patterns of genetic variation, we extracted DNA from 114 wolf samples collected in zoological museums over the last ~150 years. Fifteen microsatellite loci were used to look at genotypic variation in this historical sample. Additionally, we amplified a 430 bp sequence of mtDNA control region from the same samples. Contemporary wolf samples (N = 298) obtained after the population recovery in the mid-1990s, were used as a reference. RESULTS: Our analyses of mtDNA revealed reduced variation in the mtDNA control region through the loss of historical haplotypes observed prior to wolf declines. Heterozygosity at autosomal microsatellite loci did not decrease significantly. However, almost 20% of microsatellite alleles were unique to wolves collected before the 1960s. The genetic composition of the population changed gradually with the largest changes occurring prior to 1920. Half of the oldest historical samples formed a distinguishable genetic cluster not detected in the modern-day Finnish or Russian samples, and might therefore represent northern genetic variation lost from today's gene pool. Point estimates of Ne were small (13.2 and 20.5) suggesting population fragmentation. Evidence of a genetic population bottleneck was also detected. CONCLUSIONS: Our genetic analyses confirm changes in the genetic composition of the Finnish wolf population through time, despite the geographic interconnectivity to a much larger population in Russia. Our results emphasize the need for restoration of the historical connectivity between the present wolf populations to secure long-term viability. This might be challenging, however, because the management policies between Western and Eastern Europe often differ greatly. Additionally, wolf conservation is still a rather controversial issue, and anthropogenic pressure towards wolves remains strong.