Carl André

Protecting populations and genetic diversity within them is critical to conserving the resilience and adaptive potential of species. Fisheries management has long had the ambition of managing species at the population level, but mainly define “fish stocks” based on geographical limits, which can lead to overfishing of sensitive populations in areas where many different populations coexist. Modern genetic methods are now sufficiently cost-effective, fast, and accurate to be integrated into fisheries management, enabling genetic identification and monitoring of fish populations. Here, we establish a genetic baseline for the commercially important fish Atlantic cod ( Gadus morhua ) in the waters surrounding Sweden, by using standardised sampling procedures and developing a genetic panel of 4000 single nucleotide polymorphisms (SNPs) for cost-effective assignment of population-of-origin and inversion genotypes. Using the SNP panel, we resolve the geographical distribution of three genetically distinct cod populations in the region: offshore, coastal/Western Baltic, and Eastern Baltic cod. While there is considerable spatial overlap between the three populations, they are genetically differentiated across the entire genome, as well as in genomic regions associated with chromosomal inversions. In addition, heterozygosity and effective population size estimates suggest differences in genetic diversity and rates of genetic erosion, underscoring the need to monitor the genetic diversity within each population separately. Repeating this methodology across years provides a first suggestion for establishing spatiotemporally resolved genetic monitoring of Atlantic cod in Sweden – simultaneously accounting for both population structure within the species and the genetic diversity within populations.

The current biodiversity crisis calls for conservation measures that limit the negative human impact on important habitats and sensitive wild populations. To effectively protect biodiversity at all levels, including intraspecific diversity, conservation measures should be aligned with the connectivity and genetic structure of wild populations. In this review, we synthesise scientific literature on the connectivity and population structure of marine species in the Skagerrak – a marginal sea in the northeast Atlantic Ocean. We discuss the results in relation to the current management practices in the region, as well as the general transferability of our findings. The Skagerrak is one of the most intensively studied regions within this research field, and our findings show that the overall connectivity with adjacent seas is high, but asymmetric, for most species. Simultaneously, most species have populations in the Skagerrak distinct from both each other, and those in adjacent seas. Most of this population structure is associated with the convoluted Skagerrak coastline – population structure is common both among coastal populations and between coastal and offshore populations. In many mobile species, multiple populations are temporally sympatric in certain areas, but retain their genetic divergence through natal homing or other barriers to gene flow. The presence of population structure despite high connectivity is a challenge for area-based protection measures, and calls for temporally flexible management that also monitors intraspecific genetic diversity on multiple timescales.

Knowledge of functional dispersal barriers in the marine environment can be used to inform a wide variety of management actions, such as marine spatial planning, restoration efforts, fisheries regulations, and invasive species management. Locations and causes of dispersal barriers can be studied through various methods, including movement tracking, biophysical modeling, demographic models, and genetics. Combining methods illustrating potential dispersal, such as biophysical modeling, with realized dispersal through, e.g., genetic connectivity estimates, provides particularly useful information for teasing apart potential causes of observed barriers. In this study, we focus on blue mussels (Mytilus edulis) in the Skagerrak—a marginal sea connected to the North Sea in Northern Europe—and combine biophysical models of larval dispersal with genomic data to infer locations and causes of dispersal barriers in the area. Results from both methods agree; patterns of ocean currents are a major structuring factor in the area. We find a complex pattern of source‐sink dynamics with several dispersal barriers and show that some areas can be isolated despite an overall high dispersal capability. Finally, we translate our finding into management advice that can be used to sustainably manage this ecologically and economically important species in the future.

Range expansions can lead to increased contact of divergent populations, thus increasing the potential of hybridization events. Whether viable hybrids are produced will most likely depend on the level of genomic divergence and associated genomic incompatibilities between the different entities as well as environmental conditions. By taking advantage of historical Baltic cod (Gadus morhua) otolith samples combined with genotyping and whole genome sequencing, we here investigate the genetic impact of the increased spawning stock biomass of the eastern Baltic cod stock in the mid 1980s. The eastern Baltic cod is genetically highly differentiated from the adjacent western Baltic cod and locally adapted to the brackish environmental conditions in the deeper Eastern basins of the Baltic Sea unsuitable for its marine counterparts. Our genotyping results show an increased proportion of eastern Baltic cod in western Baltic areas (Mecklenburg Bay and Arkona Basin)-indicative of a range expansion westwards-during the peak population abundance in the 1980s. Additionally, we detect high frequencies of potential hybrids (including F1, F2 and backcrosses), verified by whole genome sequencing data for a subset of individuals. Analysis of mitochondrial genomes further indicates directional gene flow from eastern Baltic cod males to western Baltic cod females. Our findings unravel that increased overlap in distribution can promote hybridization between highly divergent populations and that the hybrids can be viable and survive under specific and favourable environmental conditions. However, the observed hybridization had seemingly no long-lasting impact on the continuous separation and genetic differentiation between the unique Baltic cod stocks.

The world’s oceans are currently facing major stressors in the form of overexploitation and anthropogenic climate change. The Baltic Sea was home to the first “industrial” fishery ∼800 y ago targeting the Baltic herring, a species that is still economically and culturally important today. Yet, the early origins of marine industries and the long-term ecological consequences of historical and contemporary fisheries remain debated. Here, we study long-term population dynamics of Baltic herring to evaluate the past impacts of humans on the marine environment. We combine modern whole-genome data with ancient DNA (aDNA) to identify the earliest-known long-distance herring trade in the region, illustrating that extensive fish trade began during the Viking Age. We further resolve population structure within the Baltic and observe demographic independence for four local herring stocks over at least 200 generations. It has been suggested that overfishing at Øresund in the 16th century resulted in a demographic shift from autumn-spawning to spring-spawning herring dominance in the Baltic. We show that while the Øresund fishery had a negative impact on the western Baltic herring stock, the demographic shift to spring-spawning dominance did not occur until the 20th century. Instead, demographic reconstructions reveal population trajectories consistent with expected impacts of environmental change and historical reports on shifting fishing targets over time. This study illustrates the joint impact of climate change and human exploitation on marine species as well as the role historical ecology can play in conservation and management policies.

Cryptic population structure in exploited fish species poses a major challenge for fisheries management. Atlantic cod ( Gadus morhua ) is a species in which the presence of sympatric ecotypes has been known for a long time, for instance off the coast of Northern Norway. More recently, two sympatric ecotypes of cod have also been documented in the Skagerrak and Kattegat; one ecotype is of an apparent offshore origin and undertakes spawning migrations to the North Sea, and the other is resident at the coast throughout its life. However, their relative contributions of juveniles to the Swedish west coast remain poorly understood. The lack of adult cod along the Skagerrak and Kattegat coasts in recent years has led to the hypothesis that the offshore ecotype is the main source of juveniles to the area, but recent studies have shown large proportions of coastal cod inside Norwegian Skagerrak fjords. In this study, juvenile cod were collected at a high spatial resolution along the Swedish west coast, and genetically assigned to each of the two ecotypes. The results reveal that there is a considerable proportion of juvenile coastal cod in the southern Kattegat, Öresund, and in inshore Swedish Skagerrak, but that the offshore ecotype dominates in offshore areas. Model selection suggests that differences in bottom depth, rather than distance from the open sea, may explain the heterogenous spatial distribution of the two ecotypes. In addition, the two ecotypes displayed differences at loci known to be associated with environmental adaptation, suggesting that their spatial distribution is maintained by natural selection in response to specific environmental conditions.

Marine resource consumption has been a key component in European diet and culture since the Middle Ages, when fish consumption increased dramatically. Yet, the early origins of marine industries and the long-term ecological consequences of historical and contemporary fisheries remain debated. The Baltic Sea was home to the first “industrial” fishery ∼800 years ago targeting the Baltic herring, a species that is still economically and culturally important today. We combine modern whole genome data with ancient DNA (aDNA) to identify the first known long-distance herring trade in the region, illustrating that large-scale fish trade began during the Viking Age. We resolve population structure within the Baltic and observe demographic independence for four local herring stocks over at least 200 generations. It has been suggested that overfishing at Øresund in the 16 ^th century resulted in a demographic shift from autumn-spawning to spring-spawning herring dominance in the Baltic. We show that while the Øresund fishery had a negative impact on the western Baltic herring stock, the existence of autumn-spawning refugia in other regions of the Baltic delayed the demographic shift to spring spawning dominance until the 20 ^th century. Importantly, modelling demographic trajectories over time, we identify a consistent pattern of serial depletion within the Baltic that is associated with changes in fishing pressure and climate, and conclude that herring exploitation at both historical and recent intensities is not sustainable. Our results highlight the complex and enduring impacts humans have had on the marine environment well before the industrial era.

1 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) 4393 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 targeted 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 displays natal homing and potentially local populations with adaptive differences. This fine-scale population structure calls for consideration when defining management units for lumpfish fishing stocks and in decisions related to sourcing and moving lumpfish for farming and cleaner fish use.

Gene flow shapes spatial genetic structure and the potential for local adaptation. Among marine animals with nonmigratory adults, the presence or absence of a pelagic larval stage is thought to be a key determinant in shaping gene flow and the genetic structure of populations. In addition, the spatial distribution of suitable habitats is expected to influence the distribution of biological populations and their connectivity patterns. We used whole genome sequencing to study demographic history and reduced representation (double‐digest restriction associated DNA) sequencing data to analyse spatial genetic structure in broadnosed pipefish (Syngnathus typhle). Its main habitat is eelgrass beds, which are patchily distributed along the study area in southern Norway. Demographic connectivity among populations was inferred from long‐term (~30‐year) population counts that uncovered a rapid decline in spatial correlations in abundance with distance as short as ~2 km. These findings were contrasted with data for two other fish species that have a pelagic larval stage (corkwing wrasse, Symphodus melops; black goby, Gobius niger). For these latter species, we found wider spatial scales of connectivity and weaker genetic isolation‐by‐distance patterns, except where both species experienced a strong barrier to gene flow, seemingly due to lack of suitable habitat. Our findings verify expectations that a fragmented habitat and absence of a pelagic larval stage promote genetic structure, while presence of a pelagic larvae stage increases demographic connectivity and gene flow, except perhaps over extensive habitat gaps.