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.

A decade of progress in marine evolutionary biology.

This article summarizes the Evolutionary Applications Special Issue, "A decade of progress in Marine Evolutionary Biology." The globally connected ocean, from its pelagic depths to its highly varied coastlines, inspired Charles Darwin to develop the theory of evolution during the voyage of the Beagle. As technology has developed, there has been a dramatic increase in our knowledge about life on our blue planet. This Special Issue, composed of 19 original papers and seven reviews, represents a small contribution to the larger picture of recent research in evolutionary biology, and how such advancements come about through the connection of researchers, their fields, and their knowledge. The first European network for marine evolutionary biology, the Linnaeus Centre for Marine Evolutionary Biology (CeMEB), was developed to study evolutionary processes in the marine environment under global change. Though hosted by the University of Gothenburg in Sweden, the network quickly grew to encompass researchers throughout Europe and beyond. Today, more than a decade after its foundation, CeMEB's focus on the evolutionary consequences of global change is more relevant than ever, and knowledge gained from marine evolution research is urgently needed in management and conservation. This Special Issue, organized and developed through the CeMEB network, contains contributions from all over the world and provides a snapshot of the current state of the field, thus forming an important basis for future research directions.

Invader at the edge - Genomic origins and physiological differences of round gobies across a steep urban salinity gradient.

Species invasions are a global problem of increasing concern, especially in highly connected aquatic environments. Despite this, salinity conditions can pose physiological barriers to their spread, and understanding them is important for management. In Scandinavia's largest cargo port, the invasive round goby (Neogobius melanostomus) is established across a steep salinity gradient. We used 12,937 SNPs to identify the genetic origin and diversity of three sites along the salinity gradient and round goby from western, central and northern Baltic Sea, as well as north European rivers. Fish from two sites from the extreme ends of the gradient were also acclimated to freshwater and seawater, and tested for respiratory and osmoregulatory physiology. Fish from the high-salinity environment in the outer port showed higher genetic diversity, and closer relatedness to the other regions, compared to fish from lower salinity upstream the river. Fish from the high-salinity site also had higher maximum metabolic rate, fewer blood cells and lower blood Ca2+. Despite these genotypic and phenotypic differences, salinity acclimation affected fish from both sites in the same way: seawater increased the blood osmolality and Na+ levels, and freshwater increased the levels of the stress hormone cortisol. Our results show genotypic and phenotypic differences over short spatial scales across this steep salinity gradient. These patterns of the physiologically robust round goby are likely driven by multiple introductions into the high-salinity site, and a process of sorting, likely based on behaviour or selection, along the gradient. This euryhaline fish risks spreading from this area, and seascape genomics and phenotypic characterization can inform management strategies even within an area as small as a coastal harbour inlet.

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe.

For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salinity from a freshwater and a brackish population within their ancestral Ponto-Caspian region of the round goby, Neogobius melanostomus. These two ancestral populations were then compared to nine additional invaded sites across northern Europe, both in terms of their sperm traits and by using genomic SNP markers. Our results show clear patterns of ancestral adaptations to freshwater and brackish salinities in their sperm performance. Population genomic analyses show that the ancestral ecotypes have generally established themselves in environments that fit their sperm adaptations. Sites close to ports with intense shipping show that both outbreeding and admixture can affect the sperm performance of a population in a given salinity. Rapid adaptation to local conditions is also supported at some sites. Historical and contemporary evolution in the traits of the round goby sperm cells is tightly linked to the population and seascape genomics as well as biogeographic processes in these invasive fishes. Since the risk of a population establishing in an area is related to the genotype by environment match, port connectivity and the ancestry of the round goby population can likely be useful for predicting the species spread.

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.

"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.

Cleaner fish escape salmon farms and hybridize with local wrasse populations.

The genetic impact of farmed fish escaping aquaculture is a highly debated issue. However, non-target species, such as cleaner fish used to remove sea lice from farmed fish, are rarely considered. Here, we report that wild corkwing wrasse (Symphodus melops), which are transported long distances to be used as cleaner fish in salmon farms, escape and hybridize with local populations. Recently, increasing numbers of corkwing wrasse have been reported in Flatanger in Norway, north of its described distribution range, an area heavily relying on the import of cleaner fish from Skagerrak. Using genetic markers identified with 2bRAD sequencing, we show that, although the Flatanger population largely is a result of a northward range expansion, there is also evidence of considerable gene flow from southern populations in Skagerrak and Kattegat. Of the 40 corkwing wrasses sampled in Flatanger, we discovered two individuals with clear southern genotypes, one first-generation hybrid, and 12 potential second-generation hybrids. In summary, we provide evidence that corkwing wrasse escape from fish farms and hybridize with local populations at the leading edge of an ongoing range expansion. Although the magnitude and significance of escapees warrant further investigation, these results should be taken into consideration in the use of translocated cleaner fish.