Atlantic cod (Gadus morhua) is a large, cold-adapted teleost that sustains long-standing commercial fisheries and incipient aquaculture1,2. Here we present the genome sequence of Atlantic cod, showing evidence for complex thermal adaptations in its haemoglobin gene cluster and an unusual immune architecture compared to other sequenced vertebrates. The genome assembly was obtained exclusively by 454 sequencing of shotgun and paired-end libraries, and automated annotation identified 22,154 genes. The major histocompatibility complex (MHC) II is a conserved feature of the adaptive immune system of jawed vertebrates3,4, but we show that Atlantic cod has lost the genes for MHCII, CD4 and Ii that are essential for the function of this pathway. Nevertheless, Atlantic cod is not exceptionally susceptible to disease under natural conditions5. We find a highly expanded number of MHCI genes and a unique composition of its Toll-like receptor (TLR) families. This suggests how the Atlantic cod immune system has evolved compensatory mechanisms within both adaptive and innate immunity in the absence of MHCII. These observations affect fundamental assumptions about the evolution of the adaptive immune system and its components in vertebrates.

BackgroundThe Atlantic salmon genome is in the process of returning to a diploid state after undergoing a whole genome duplication (WGD) event between 25 and100 million years ago. Existing data on the proportion of paralogous sequence variants (PSVs), multisite variants (MSVs) and other types of complex sequence variation suggest that the rediplodization phase is far from over. The aims of this study were to construct a high density linkage map for Atlantic salmon, to characterize the extent of rediploidization and to improve our understanding of genetic differences between sexes in this species.ResultsA linkage map for Atlantic salmon comprising 29 chromosomes and 5650 single nucleotide polymorphisms (SNPs) was constructed using genotyping data from 3297 fish belonging to 143 families. Of these, 2696 SNPs were generated from ESTs or other gene associated sequences. Homeologous chromosomal regions were identified through the mapping of duplicated SNPs and through the investigation of syntenic relationships between Atlantic salmon and the reference genome sequence of the threespine stickleback (Gasterosteus aculeatus). The sex-specific linkage maps spanned a total of 2402.3 cM in females and 1746.2 cM in males, highlighting a difference in sex specific recombination rate (1.38:1) which is much lower than previously reported in Atlantic salmon. The sexes, however, displayed striking differences in the distribution of recombination sites within linkage groups, with males showing recombination strongly localized to telomeres.ConclusionThe map presented here represents a valuable resource for addressing important questions of interest to evolution (the process of re-diploidization), aquaculture and salmonid life history biology and not least as a resource to aid the assembly of the forthcoming Atlantic salmon reference genome sequence.

Identification of genome-wide patterns of divergence provides insight on how genomes are influenced by selection and can reveal the potential for local adaptation in spatially structured populations. In Atlantic cod – historically a major marine resource – Northeast-Arctic- and Norwegian coastal cod are recognized by fundamental differences in migratory and non-migratory behavior, respectively. However, the genomic architecture underlying such behavioral ecotypes is unclear. Here, we have analyzed more than 8.000 polymorphic SNPs distributed throughout all 23 linkage groups and show that loci putatively under selection are localized within three distinct genomic regions, each of several megabases long, covering approximately 4% of the Atlantic cod genome. These regions likely represent genomic inversions. The frequency of these distinct regions differ markedly between the ecotypes, spawning in the vicinity of each other, which contrasts with the low level of divergence in the rest of the genome. The observed patterns strongly suggest that these chromosomal rearrangements are instrumental in local adaptation and separation of Atlantic cod populations, leaving footprints of large genomic regions under selection. Our findings demonstrate the power of using genomic information in further understanding the population dynamics and defining management units in one of the world’s most economically important marine resources.

How genomic selection enables species to adapt to divergent environments is a fundamental question in ecology and evolution. We investigated the genomic signatures of local adaptation in Atlantic cod (Gadus morhua L.) along a natural salinity gradient, ranging from 35‰ in the North Sea to 7‰ within the Baltic Sea. By utilizing a 12 K SNPchip, we simultaneously assessed neutral and adaptive genetic divergence across the Atlantic cod genome. Combining outlier analyses with a landscape genomic approach, we identified a set of directionally selected loci that are strongly correlated with habitat differences in salinity, oxygen, and temperature. Our results show that discrete regions within the Atlantic cod genome are subject to directional selection and associated with adaptation to the local environmental conditions in the Baltic- and the North Sea, indicating divergence hitchhiking and the presence of genomic islands of divergence. We report a suite of outlier single nucleotide polymorphisms within or closely located to genes associated with osmoregulation, as well as genes known to play important roles in the hydration and development of oocytes. These genes are likely to have key functions within a general osmoregulatory framework and are important for the survival of eggs and larvae, contributing to the buildup of reproductive isolation between the low-salinity adapted Baltic cod and the adjacent cod populations. Hence, our data suggest that adaptive responses to the environmental conditions in the Baltic Sea may contribute to a strong and effective reproductive barrier, and that Baltic cod can be viewed as an example of ongoing speciation.

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Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and nonmigratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the >100 000-year-old trans-Atlantic separation of Atlantic cod. The long-term persistence of these inversions indicates that they are maintained by selection, possibly facilitated by coevolution of genes underlying complex traits. Our data suggest that migratory behaviour is derived from more stationary, ancestral ecotypes. Overall, we identify several large genomic regions—each containing hundreds of genes—likely involved in the maintenance of genomic divergence in Atlantic cod on both sides of the Atlantic Ocean.

In several species genetic differentiation across environmental gradients or between geographically separate populations has been reported to center at “genomic islands of divergence,” resulting in heterogeneous differentiation patterns across genomes. Here, genomic regions of elevated divergence were observed on three chromosomes of the highly mobile fish Atlantic cod (Gadus morhua) within geographically fine-scaled coastal areas. The “genomic islands” extended at least 5, 9.5, and 13 megabases on linkage groups 2, 7, and 12, respectively, and coincided with large blocks of linkage disequilibrium. For each of these three chromosomes, pairs of segregating, highly divergent alleles were identified, with little or no gene exchange between them. These patterns of recombination and divergence mirror genomic signatures previously described for large polymorphic inversions, which have been shown to repress recombination across extensive chromosomal segments. The lack of genetic exchange permits divergence between noninverted and inverted chromosomes in spite of gene flow. For the rearrangements on linkage groups 2 and 12, allelic frequency shifts between coastal and oceanic environments suggest a role in ecological adaptation, in agreement with recently reported associations between molecular variation within these genomic regions and temperature, oxygen, and salinity levels. Elevated genetic differentiation in these genomic regions has previously been described on both sides of the Atlantic Ocean, and we therefore suggest that these polymorphisms are involved in adaptive divergence across the species distributional range.

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. K E Y W O R D Schromosomal inversion, ecological adaptation, Gadus morhua, gene flow, population divergence ----------------------------------------------------------------------------------------------------------------------------------------------------------------------This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. | INTRODUCTIONLocal adaptation characterizes populations that experience higher inherited fitness in their native habitat compared to members of other populations transferred to the same environment (Kawecki & Ebert, 2004). The degree of such ecological adaptation depends on the directional selection of advantageous traits and is counteracted by high connectivity and resulting homogenizing gene flow, implicating a limited potential for local adaptation in populations experiencing high gene flow (Dobzhansky, 1937;Mayr, 1942;Wright, 1931).Although environmental adaptation can also involve gene expression-induced plastic responses such as morphological, physiological or behavioural changes, these occur without genotypic changes (Reusch, 2014;Via et al., 1995).Most marine fish populations have traditionally been regar...