Genome architecture enables local adaptation of Atlantic cod despite high connectivity.

Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation.

Historical DNA documents long-distance natal homing in marine fish.

The occurrence of natal homing in marine fish remains a fundamental question in fish ecology as its unequivocal demonstration requires tracking of individuals from fertilization to reproduction. Here, we provide evidence of long-distance natal homing (>1000 km) over more than 60 years in Atlantic cod (Gadus morhua), through genetic analysis of archived samples from marked and recaptured individuals. Using a high differentiation single-nucleotide polymorphism assay, we demonstrate that the vast majority of cod tagged in West Greenland and recaptured on Icelandic spawning grounds belonged to the Iceland offshore population, strongly supporting a hypothesis of homing. The high degree of natal fidelity observed provides the evolutionary settings for development of locally adapted populations in marine fish and emphasize the need to consider portfolio effects in marine fisheries management strategies.

A 14-year time series of marine megafauna bycatch in the Italian midwater pair trawl fishery.

Fisheries bycatch is recognised as a global threat to vulnerable marine megafauna and historical data can contribute to quantify the magnitude of the impact. Here, we present a collection of three datasets generated between 2006 and 2019 by a monitoring programme on marine megafauna bycatch in one of the main Italian fisheries, the northern central Adriatic midwater pair trawl fishery. The three datasets consist of: (i) monitored fishing effort; (ii) bycatch and biological data of dolphins, sea turtles and elasmobranchs; (iii) and dolphin sightings. Some information included in these datasets has already proved to provide a unique opportunity to estimate total incidental capture of species of conservation concern and trends of their relative abundance over time in the northern - central Adriatic Sea. These datasets are expected to be considered by different end users to improve the conservation of species and fishery management approaches to assess the impact of a fishery on species of conservation concern.

Elasmobranch bycatch in the Italian Adriatic pelagic trawl fishery.

Elasmobranchs are among the most threatened long-lived marine species worldwide, and incidental capture is a major source of mortality. The northern central Adriatic Sea, though one of the most overfished basins of the Mediterranean Sea, supports a very valuable marine biodiversity, including elasmobranchs. This study assesses the impact of the northern central Adriatic pelagic trawl fishery on common smooth-hound (Mustelus mustelus), spiny dogfish (Squalus acanthias), common eagle ray (Myliobatis aquila), and pelagic stingray (Pteroplatytrygon violacea) by examining incidental catches recorded between 2006 and 2015. The distribution of bycatch events was evaluated using geo-referenced data. Generalized Linear Models were computed to standardize the catch of the four species and to predict the relative abundance of bycatch events. Data analysis shows that most bycatch events involving all four species occurred in the northern Adriatic Sea. The models predicted significant, distinct temporal patterns of standardized catches in line with previous investigations. Water depth, season, and fishing region were the best predictors to explain bycatch events. The present data suggest that the northern Adriatic may be an important nursery area for several elasmobranchs. They also highlight the urgent need for a better understanding of the interactions between elasmobranchs and fisheries to develop and apply suitable, ad hoc management measures.

Archived DNA reveals fisheries and climate induced collapse of a major fishery.

Fishing and climate change impact the demography of marine fishes, but it is generally ignored that many species are made up of genetically distinct locally adapted populations that may show idiosyncratic responses to environmental and anthropogenic pressures. Here, we track 80 years of Atlantic cod (Gadus morhua) population dynamics in West Greenland using DNA from archived otoliths in combination with fish population and niche based modeling. We document how the interacting effects of climate change and high fishing pressure lead to dramatic spatiotemporal changes in the proportions and abundance of different genetic populations, and eventually drove the cod fishery to a collapse in the early 1970s. Our results highlight the relevance of fisheries management at the level of genetic populations under future scenarios of climate change.

The use of archived tags in retrospective genetic analysis of fish.

Collections of historical tissue samples from fish (e.g. scales and otoliths) stored in museums and fisheries institutions are precious sources of DNA for conducting retrospective genetic analysis. However, in some cases, only external tags used for documentation of spatial dynamics of fish populations have been preserved. Here, we test the usefulness of fish tags as a source of DNA for genetic analysis. We extract DNA from historical tags from cod collected in Greenlandic waters between 1950 and 1968. We show that the quantity and quality of DNA recovered from tags is comparable to DNA from archived otoliths from the same individuals. Surprisingly, levels of cross-contamination do not seem to be significantly higher in DNA from external (tag) than internal (otolith) sources. Our study therefore demonstrates that historical tags can be a highly valuable source of DNA for retrospective genetic analysis of fish.

Spatiotemporal SNP analysis reveals pronounced biocomplexity at the northern range margin of Atlantic cod Gadus morhua.

Accurate prediction of species distribution shifts in the face of climate change requires a sound understanding of population diversity and local adaptations. Previous modeling has suggested that global warming will lead to increased abundance of Atlantic cod (Gadus morhua) in the ocean around Greenland, but the dynamics of earlier abundance fluctuations are not well understood. We applied a retrospective spatiotemporal population genomics approach to examine the temporal stability of cod population structure in this region and to search for signatures of divergent selection over a 78-year period spanning major demographic changes. Analyzing >900 gene-associated single nucleotide polymorphisms in 847 individuals, we identified four genetically distinct groups that exhibited varying spatial distributions with considerable overlap and mixture. The genetic composition had remained stable over decades at some spawning grounds, whereas complete population replacement was evident at others. Observations of elevated differentiation in certain genomic regions are consistent with adaptive divergence between the groups, indicating that they may respond differently to environmental variation. Significantly increased temporal changes at a subset of loci also suggest that adaptation may be ongoing. These findings illustrate the power of spatiotemporal population genomics for revealing biocomplexity in both space and time and for informing future fisheries management and conservation efforts.