Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s).

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.

SNP genotyping reveals substructuring in weakly differentiated populations of Atlantic cod (Gadus morhua) from diverse environments in the Baltic Sea.

Atlantic cod (Gadus morhua) is one of the most important fish species in northern Europe for several reasons including its predator status in marine ecosystems, its historical role in fisheries, its potential in aquaculture and its strong public profile. However, due to over-exploitation in the North Atlantic and changes in the ecosystem, many cod populations have been reduced in size and genetic diversity. Cod populations in the Baltic Proper, Kattegat and North Sea have been analyzed using a species specific single nucleotide polymorphism (SNP) array. Using a subset of 8,706 SNPs, moderate genetic differences were found between subdivisions in three traditionally delineated cod management stocks: Kattegat, western and eastern Baltic. However, an FST measure of population differentiation based on allele frequencies from 588 outlier loci for 2 population groups, one including 5 western and the other 4 eastern Baltic populations, indicated high genetic differentiation. In this paper, differentiation has been demonstrated not only between, but also within western and eastern Baltic cod stocks for the first time, with salinity appearing to be the most important environmental factor influencing the maintenance of cod population divergence between the western and eastern Baltic Sea.

Assessing SNP-markers to study population mixing and ecological adaptation in Baltic cod.

Atlantic cod (Gadus morhua) is a species of great ecological and economical importance in the Baltic Sea. Here, two genetically differentiated stocks, the western and the eastern Baltic cod, display substantial mechanical mixing, hampering our understanding of cod ecology and impeding stock assessments and management. Based on whole-genome re-sequencing data from reference samples obtained from the study area, we designed two different panels of Single Nucleotide Polymorphisms markers (SNPs), which take into account the exceptional genome architecture of cod. A minimum panel of 20 diagnostic SNPs and an extended panel (20 diagnostic and 18 biologically informative SNPs, 38 in total) were developed and validated to distinguish unambiguously between the western and the eastern Baltic cod stocks and to enable studies of local adaptation to the specific environment in the Baltic Sea, respectively. We tested both panels on cod sampled from the southern Baltic Sea (n = 603) caught in 2015 and 2016. Genotyping results showed that catches from the mixing zone in the Arkona Sea, were composed of similar proportions of individuals of the western and the eastern stock. Catches from adjacent areas to the east, the Bornholm Basin and Gdansk Deep, were exclusively composed of eastern Baltic cod, whereas catches from adjacent western areas (Belt Sea and Öresund) were composed of western Baltic cod. Interestingly, the two Baltic cod stocks showed strong genetic differences at loci associated with life-history trait candidate genes, highlighting the species' potential for ecological adaptation even at small geographical scales. The minimum and the extended panel of SNP markers presented in this study provide powerful tools for future applications in research and fisheries management to further illuminate the mixing dynamics of cod in the Baltic Sea and to better understand Baltic cod ecology.

Disentangling structural genomic and behavioural barriers in a sea of connectivity.

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

Ancient DNA reveals the Arctic origin of Viking Age cod from Haithabu, Germany.

Knowledge of the range and chronology of historic trade and long-distance transport of natural resources is essential for determining the impacts of past human activities on marine environments. However, the specific biological sources of imported fauna are often difficult to identify, in particular if species have a wide spatial distribution and lack clear osteological or isotopic differentiation between populations. Here, we report that ancient fish-bone remains, despite being porous, brittle, and light, provide an excellent source of endogenous DNA (15-46%) of sufficient quality for whole-genome reconstruction. By comparing ancient sequence data to that of modern specimens, we determine the biological origin of 15 Viking Age (800-1066 CE) and subsequent medieval (1066-1280 CE) Atlantic cod (Gadus morhua) specimens from excavation sites in Germany, Norway, and the United Kingdom. Archaeological context indicates that one of these sites was a fishing settlement for the procurement of local catches, whereas the other localities were centers of trade. Fish from the trade sites show a mixed ancestry and are statistically differentiated from local fish populations. Moreover, Viking Age samples from Haithabu, Germany, are traced back to the North East Arctic Atlantic cod population that has supported the Lofoten fisheries of Norway for centuries. Our results resolve a long-standing controversial hypothesis and indicate that the marine resources of the North Atlantic Ocean were used to sustain an international demand for protein as far back as the Viking Age.