Comparing microsatellite variation in north-east Atlantic cod (Gadus morhua L.) to genetic structuring as revealed by the pantophysin (Pan I) locus

Variation at seven microsatellite loci was compared with variation observed at Pan I, a single copy nuclear DNA gene coding for pantophysin, in 14 samples of Atlantic cod ( Gadus morhua ) stretching from Spitsbergen to the North Sea. Population structuring indicated by the two types of markers was concordant and in agreement with the traditional grouping of cod in the study area into three main populations: north-east Arctic cod (NEAC), Norwegian coastal cod (NCC) and North Sea cod (NSC). Microsatellites, however, revealed genetic heterogeneity not only within NCC, as did Pan I, but also within NEAC and NSC, which appeared to be homogenous when analysed for Pan I. Moreover, microsatellites displayed lower levels of differentiation than Pan I between NEAC and two other groups. Differences in the magnitude of differentiation for the two types of markers may be attributable to higher levels of polymorphism and alleged selective neutrality of microsatellites. Isolation by distance was clearly apparent for microsatellites but was less evident for Pan I, indicating that environmentally induced selection appears to shape the patterns of genetic differentiation for this marker. Even though the population structure of north-east Atlantic cod, as revealed by microsatellites and Pan I, appears to be maintained largely by restricted gene flow, selection acting on a recent historical time scale probably contributes to the observed geographic pattern of Pan I frequencies.     

Pantophysin (Pan I) locus divergence between inshore v. offshore and northern v. southern populations of Atlantic cod in the north‐east Atlantic

More than 6000 cod Gadus morhua , sampled in coastal and offshore waters stretching from the Barents Sea down to the North Sea, were analysed for frequencies of alleles at the scnDNA pantophysin locus ( Pan I)[formerly called synaptophysin ( Syp I)]. The significant allele frequency difference between the two major stocks of cod in Norway, north‐east Arctic cod (NEAC) and Norwegian coastal cod (NCC), was upheld in all years of the investigation (1993 to 2001), and applied both to larval cod and post‐juveniles of various ages. On a north‐south axis, the appearance of a latitudinal cline of post‐juvenile (≥1 year) allele frequencies was exposed. The intermediate allele frequencies in coastal areas of northern Norway, seem to a large extent to be caused by intermingling of the two stocks, although the existence of populations of coastal cod with alternative Pan I frequencies could not be ruled out. The role of selection is yet unresolved. Depth of the sampling location seemed to have an effect on the allele frequencies and their temporal stability, while there was no indication of seasonal variation in the frequencies. Breeding structure was the most likely cause for upholding the extreme divergence in Pan I frequencies between NEAC and NCC.     

Climate-Driven Ichthyoplankton Drift Model Predicts Growth of Top Predator Young

Climate variability influences seabird population dynamics in several ways including access to prey near colonies during the critical chick-rearing period. This study addresses breeding success in a Barents Sea colony of common guillemots Uria aalge where trophic conditions vary according to changes in the northward transport of warm Atlantic Water. A drift model was used to simulate interannual variations in transport of cod Gadus morhua larvae along the Norwegian coast towards their nursery grounds in the Barents Sea. The results showed that the arrival of cod larvae from southern spawning grounds had a major effect on the size of common guillemot chicks at fledging. Furthermore, the fraction of larvae from the south was positively correlated to the inflow of Atlantic Water into the Barents Sea thus clearly demonstrating the mechanisms by which climate-driven bottom-up processes influence interannual variations in reproductive success in a marine top predator.     

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000–2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean.     

Genomic divergence between the migratory and stationary ecotypes of Atlantic cod

Atlantic cod displays a range of phenotypic and genotypic variations, which includes the differentiation into coastal stationary and offshore migratory types of cod that co‐occur in several parts of its distribution range and are often sympatric on the spawning grounds. Differentiation of these ecotypes may involve both historical separation and adaptation to ecologically distinct environments, the genetic basis of which is now beginning to be unravelled. Genomic analyses based on recent sequencing advances are able to document genomic divergence in more detail and may facilitate the exploration of causes and consequences of genome‐wide patterns. We examined genomic divergence between the stationary and migratory types of cod in the Northeast Atlantic, using next‐generation sequencing of pooled DNA from each of two population samples. Sequence data was mapped to the published cod genome sequence, arranged in more than 6000 scaffolds (611 Mb). We identified 25 divergent scaffolds (26 Mb) with a higher than average gene density, against a backdrop of overall moderate genomic differentiation. Previous findings of localized genomic divergence in three linkage groups were confirmed, including a large (15 Mb) genomic region, which seems to be uniquely involved in the divergence of migratory and stationary cod. The results of the pooled sequencing approach support and extend recent findings based on single‐nucleotide polymorphism markers and suggest a high degree of reproductive isolation between stationary and migratory cod in the North‐east Atlantic.     

Ancient chromosomal rearrangement associated with local adaptation of a postglacially colonized population of Atlantic Cod in the northwest Atlantic

Intraspecific diversity is central to the management and conservation of exploited species, yet knowledge of how this diversity is distributed and maintained in the genome of many marine species is lacking. Recent advances in genomic analyses allow for genome‐wide surveys of intraspecific diversity and offer new opportunities for exploring genomic patterns of divergence. Here, we analysed genome‐wide polymorphisms to measure genetic differentiation between an offshore migratory and a nonmigratory population and to define conservation units of Atlantic Cod (Gadus morhua) in coastal Labrador. A total of 141 individuals, collected from offshore sites and from a coastal site within Gilbert Bay, Labrador, were genotyped using an ~11k single nucleotide polymorphism array. Analyses of population structure revealed strong genetic differentiation between migratory offshore cod and nonmigratory Gilbert Bay cod. Genetic differentiation was elevated for loci within a chromosomal rearrangement found on linkage group 1 (LG1) that coincides with a previously found double inversion associated with migratory and nonmigratory ecotype divergence of cod in the northeast Atlantic. This inverted region includes several genes potentially associated with adaptation to differences in salinity and temperature, as well as influencing migratory behaviour. Our work provides evidence that a chromosomal rearrangement on LG1 is associated with parallel patterns of divergence between migratory and nonmigratory ecotypes on both sides of the Atlantic Ocean.     

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.     

Mitochondrial DNA polymorphism of atlantic cod of the Barents and White seas

High level of intraspecific polymorphism of the mtDNA cytochrome b gene in the Atlantic cod Gadus morhua L. from the northeastern part of the species range (Barents and White seas) is detected. The absence of genetic differentiation between the samples from different areas of the Norwegian and Barents seas is shown, and the fact that these samples belong to the same population of Northeast Arctic cod is confirmed. Significant differences in the frequences of mitochondrial DNA haplotypes between the cod from the Barents and White seas, as well as from the northwestern part of the range, are found. The cod Gadus morhua kildinensis Derjugin, 1920 from Mogilnoye Lake and Gadus morhua marisalbi Derjugin, 1920 from the White Sea were revealed to have common haplotypes with the cod from the Barents Sea, confirming the recent origin of these forms from the Atlantic cod G. morhua.     

Intraspecies structure of beaked redfish <Emphasis Type="Italic">Sebastes mentella</Emphasis> of the Atlantic and Arctic oceans

On the basis of the results of complex interdisciplinary investigations of the population composition and structure of the beaked redfish Sebastes mentella of the Atlantic and Arctic oceans, its three populations are discerned relatively isolated from each other by the system of permanent marine currents—North Atlantic, Flemish-Cape, and Norway-Barents Sea. The population structure of the species in the southern part of its area corresponds to the model of a local stock. Interaction of the North Atlantic and the Norway-Barents Sea populations well correspond to the model of fluctuating stocks. Redfish aggregations in different biotopes (mesobenthal and mesopelagial) are intrapopulational epigenetic groups. In the period of warm and anomalously warm years, a part of mature specimens from the pelagial of the North Irminger Sea make an irreversible migration to the southern part of the Norwegian Sea and form there mixed aggregations of fish from the North Atlantic and Norway-Barents Sea populations. With consideration of the effect of climatic–oceanological processes, a principally new scheme is elaborated describing the process of seasonal migrations of redfish in the mesobenthal and mesopelagial. The previous views on direction of return migrations of redfish of the Norway-Barents Sea population are reconsidered. Juveniles from the western part of the Barents Sea and Spitsbergen not only supplement the demersal aggregations but also migrate to the pelagial of the Norwegian Sea.     

Comparative analysis of genetic variability of white sea cod (Gadus morhua marisalbi) at allozyme and microsatellite markers

Variability of cod spawning and feeding schools from Kandalaksha Bay of the White Sea, was examined at six allozyme and eight microsatellite loci. The degree of genetic differentiation at allozyme loci constituted θ = 0.36% [95% bootstrap interval 0.0458; 0.6743]. The differentiation estimates obtained using microsatellite markers were higher, θ = 1.33% [0.057; 3.11]. It was demonstrated that the level of genetic diversity in the White Sea cod was lower than that established for the Atlantic cod from Barents Sea using the same set of allozyme and microsatellite markers. The genetic data obtained support the opinion that the White Sea cod is a reproductively independent group formed as a result of the Holocene dispersal of Atlantic cod.     

Atlantic cod <Emphasis Type="Italic">Gadus morhua</Emphasis> (Gadiformes: Gadidae) from the Gulf of Ura: Morphobiological characteristic

Analysis of variation of biological and morphometric characteristics of cod Gadus morhua from the Gulf of Ura-a water area in the composition of Motovskii Bay of the Barents Sea was performed. The material was collected from 1999 to 2006 during spawning of the Atlantic cod. Parameters such as length, weight, sex composition, maturity stage, age, otolith structure, and variation of plastic characters were analyzed. It was shown that the Gulf of Ura, parallel to individuals of junior age groups, is inhabited by cod in the spawning state aged 5–6 months and older with coastal and Atlantic types of otolith.     

On the spatial relationship between the spawning and feeding parts of the range of lumpfish Cyclopterus lumpus (Cyclopteridae) in the Barents Sea and adjacent waters (according to results of analysis of the size composition similarity)

Results of analysis of similarity of size series of mature females of the lumpfish Cyclopterus lumpus collected on the spawning grounds in the Barents and Norwegian seas (Russian and Norwegian coasts), as well as in the areas of its feeding, are provided. The trajectories of feeding migrations of lumpfish in the southern part of the Barents Sea have been revealed. A clinal decrease in the average length of females in the range from west to east is shown. The area of feeding aggregations of lumpfish spawning off the Russian coast is distinguished. The boundaries of the census water area used to assess the commercial stock of lumpfish and to determine the values of its possible catch off the coast of Murmansk are specified.     

Recolonization history and large-scale dispersal in the open sea: the case study of the North Atlantic cod, Gadus morhua L.

Most studies of the genetic structure of Atlantic cod have focused on small geographical scales. In the present study, the genetic structure of cod sampled on spawning grounds in the North Atlantic was examined using eight microsatellite loci and the Pan I locus. A total of 954 cod was collected from nine different regions: the Baltic Sea, the North Sea, the Celtic Sea, the Irish Sea and Icelandic waters during spring 2002 and spring 2003, from Norwegian waters and the Faroe Islands (North and West spawning grounds) in spring 2003, and from Canadian waters in 1998. Temporal stability among spawning grounds was observed in Icelandic waters and the Celtic Sea, and no significant difference was observed between the samples from the Baltic Sea and between the samples from Faroese waters. F -statistics showed significant differences between most populations and a pattern of isolation-by-distance was described with microsatellite loci. The Pan I locus revealed the presence of two genetically distinguishable basins, the North-west Atlantic composed of the Icelandic and Canadian samples and the North-east Atlantic composed of all other samples. Permutation of allele sizes at each microsatellite locus among allelic states supported a mutational component to the genetic differentiation, indicating a historical origin of the observed variation. Estimation of the time of divergence was approximately 3000 generations, which places the origin of current genetic pattern of cod in the North Atlantic in the late Weichselian (Wisconsinian period), at last glacial maximum.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 315–329.     

Transport of North Sea cod larvae into the Skagerrak coastal populations

The Atlantic cod (Gadus morhua) is economically one of the world's most important marine species--a species presently suffering from heavy overexploitation throughout its range of distribution. Although not fully understood, the Atlantic cod is believed to be structured into populations in a rather complex manner, whereby both highly migratory and more confined ocean-spawning stocks coexist with stationary coastal populations. Owing to the complex population structure, little is presently known about how overexploitation of offshore stocks may affect other segments of the species. Here, we use microsatellite DNA analyses of coastal and offshore cod in combination with oceanographic modelling to investigate the population structure of Atlantic cod in the North Sea-Skagerrak area and evaluate the potential for larval transport into coastal populations. Our results suggest an extensive but temporally variable drift of offshore cod larvae into coastal populations. In a year (2001) with high inflow of North Sea waters into the Skagerrak we find that juvenile cod caught along the Skagerrak coast are predominantly of North Sea origin, whereas in a year (2000) with low inflow juveniles appear to be of local origin. These findings indicate that offshore cod may influence coastal cod populations over large distances.     

Structure and specific features of formation of aggregations of deepwater redfish <Emphasis Type="Italic">Sebastes mentella</Emphasis> (Scorpaenidae) in the Norwegian Sea pelagial

Results of studies of the structure and specific features of formation of aggregations of deepwater redfish Sebastes mentella in the Norwegian Sea pelagial are provided. Data on the biological characteristics of S. mentella from different regions of the Norwegian Sea pelagial do not allow us to consider its aggregations as separate populations. On the basis of comparative analysis of the structure of aggregations in the Norwegian Sea and of population parameters and specific features of the life cycle of S. mentella in different parts of the Atlantic Ocean, its complex intraspecies organization at sites of overlapping of two largest populations—North Atlantic and Norwegian-Barents Sea-was established. The formation of pelagic aggregations in the water area of the Norwegian Sea occurs due to migration of maturing and mature individuals from the adjoining water areas. In the southern areas of the Norwegian Sea, dominant recruitment comes from the pelagial of the northeastern part of the Irminger Sea, which is promoted by the direction of streams of the North-Atlantic Current; it is not excluded either that fish can migrate to the southern part of the sea from the slopes of the Faeroes, Faeroes-Icelandic threshold, and the western coast of Norway. Migration to the northern areas of the sea is mainly performed by rapidly maturing fish from the rearing region from the western slopes of the Barents Sea and Spitsbergen Archipelago. The presence of seasonal migrations hinders the formation in the pelagial of perch isolated groups and promotes their migration.     

Thermal growth potential of Atlantic cod by the end of the 21st century

Ocean warming may lead to smaller body sizes of marine ectotherms, because metabolic rates increase exponentially with temperature while the capacity of the cardiorespiratory system to match enhanced oxygen demands is limited. Here, we explore the impact of rising sea water temperatures on Atlantic cod (Gadus morhua), an economically important fish species. We focus on changes in the temperature‐dependent growth potential by a transfer function model combining growth observations with climate model ensemble temperatures. Growth potential is expressed in terms of asymptotic body weight and depends on water temperature. We consider changes between the periods 1985–2004 and 2081–2100, assuming that future sea water temperatures will evolve according to climate projections for IPCC AR5 scenario RCP8.5. Our model projects a response of Atlantic cod to future warming, differentiated according to ocean regions, leading to increases of asymptotic weight in the Barents Sea, while weights are projected to decline at the southern margin of the biogeographic range. Southern spawning areas will disappear due to thermal limitation of spawning stages. These projections match the currently observed biogeographic shifts and the temperature‐ and oxygen‐dependent decline in routine aerobic scope at southern distribution limits.     

Early Environmental Influences on Growth of Arcto-Norwegian Cod, Gadus Morhua, From The 0-group To Adults

A high growth rate for Arcto-Norwegian cod, Gadus morhua, in the Barents Sea and adjacent areas from the larva period to the 0-group enhances survival and ultimately recruitment to the fishery. However, it appeared that high growth rates for a cohort through the 0-group were not continued as the cohort ages. Based on survey data, there was a significant negative correlation between the average length at the 0-group and its average length at ages 2 through 8. We provided evidence suggesting that this phenomenon was caused by the inter-annual variability in inflow of warm, prey-rich Atlantic water into the Barents Sea from the Norwegian Sea. Enhanced inflow provided favorable conditions for cod growth during the larva and juvenile pelagic intervals. However, this same strong inflow carried a proportion of the cohort farther to the east in the Barents Sea, where the bottom water is colder than in the west. The colder conditions experienced by such cohorts, as compared to cohorts that have a more westerly settlement, led to slower growth prior to age 2. Slow growth during this interval appeared to be the reason for these cohorts' relatively smaller mean length at older ages.     

Population status of Greenland halibut <Emphasis Type="Italic">Reinhardtius hippoglossoides</Emphasis> (Walbaum, 1793) of the Laptev Sea

This is the first study to perform a comparative genetic analysis of Greenland halibut in the samples from the Atlantic (waters of west and east of Greenland), Arctic (Laptev Sea), and Pacific (the western part of the Bering Sea) ocean basins using seven microsatellite loci. The obtained data clearly demonstrate that the Greenland halibut population in the Laptev Sea belongs to the groups of the Atlantic Ocean basin. Apparently, the Greenland halibut of the Laptev Sea is represented by a dependent population, which is replenished due to the drift of immatures from the spawning grounds in the Barents Sea with the transformed Atlantic water flow along the continental slope. In addition, the Arctic population can be partially replenished due to the breeding of the halibut in local spawning grounds.     

Population genetic substructure in blue whiting based on allozyme data

The genetic population structure of the pelagic gadoid blue whiting Micromesistius poutassou throughout its east Atlantic distribution range was explored using polymorphisms at the tissue enzyme loci IDHP-2 * and PGM-1 *. The study included 5025 individuals from 65 locations in the east Atlantic and the Mediterranean. Significant geographic heterogeneity in allele frequencies was demonstrated at both loci ( IDHP-2 *: P=0·030, PGM-1 *: P=0·005). The degree of genetic differentiation ( F _ST= 1·1%) in blue whiting appears to be at the same level as for the demersal gadoids cod and haddock. Several separate reproductive units were indicated at the fringes of the distribution range, i.e. in the Barents Sea, and in one Norwegian fjord (Romsdalsfjord).