Identification of a single genomic region associated with seasonal river return timing in adult Scottish Atlantic salmon (<i>Salmo salar</i>), using a genome-wide association study

Cauwelier, Eef; Gilbey, John; Sampayo, James N.; Stradmeyer, Lee; Middlemas, Stuart J.

doi:10.1139/cjfas-2017-0293

Cited by 41 publications

(43 citation statements)

References 66 publications

(23 reference statements)

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“…Likewise, during their return migration, Atlantic salmon may be non-randomly distributed in relation to their life history, genotype, and population of origin (Svenning et al 2019). For example, relatively early run timing is linked to both later maturation (Jonsson and Jonsson 2011) and six6*L (Cauwelier et al 2018, Pritchard et al 2018), a pattern that concordantly holds in our dataset (Supp. Table 11).…”

Section: Discussionsupporting

confidence: 82%

Life history genomic regions explain differences in Atlantic salmon marine diet specialization

Aykanat

Rasmussen

Ozerov

et al. 2019

Preprint

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9An ecological consequence of climate change is the alteration of food-web structures. Species with 10 ontogenetic (age-dependent) diet variation, such as Atlantic salmon (Salmo salar), may exhibit an age-11 dependent response to food-web perturbations, which may subsequently influence the demographic structure. 12 We previously showed that age at maturity in Atlantic salmon is primarily influenced by few genomic regions 13 (vgll3 and six6), but whether these regions are linked to diet is unknown. We hypothesized that genetic 14 variation in these life history genomic regions govern age-dependent resource utilization efficiency, which 15 would subsequently influence age at maturity. To test this, we first performed stomach content analysis of 16 Atlantic salmon sampled at sea on their return migration to fresh water, followed by targeted genotyping by 17 sequencing. Here, we first showed that Atlantic salmon change their feeding strategies along their ontogeny. 18Consistent with the so-called feast and famine strategy, older age groups retained a heavier stomach content, 19 which however came at the expense of running on empty more often. Next, we presented evidence that 20 stomach fullness in Atlantic salmon is associated with six6, a gene previously shown to be potentially under 21 divergent selection and correlated with age at maturity among populations. There was no association with 22 vgll3, a gene with a large effect on sea age at maturity. Prey composition was marginally linked to both six6 23 and vgll3. Our results suggest that Atlantic salmon individuals are not as generalist as previously thought and 24 that genetic variation partly underlies resource utilization variation among individuals. Given that feeding 25 strategies differ ontogenetically, and a spatially divergent genomic region is associated with diet acquisition 26 variation, we predict populations with diverse maturation age will have diverse evolutionary responses to 27 future changes in marine food-web structures.

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Section: Discussionsupporting

confidence: 82%

Life history genomic regions explain differences in Atlantic salmon marine diet specialization

Aykanat

Rasmussen

Ozerov

et al. 2019

Preprint

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“…() also found a small but significant effect of genotype at this locus on length of returning adults. Recently, Cauwelier, Gilbey, Sampayo, Stradmeyer, and Middlemas () found that the locus was associated with intrapopulation variation in run timing of Atlantic salmon in Scotland. Further, Bourret, Dionne, et al.…”

Section: Discussionmentioning

confidence: 99%

Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence‐related genes

et al. 2018

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Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large-effect age-at-maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.

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“…Previous studies of salmonids have found genome-wide differences between populations and ecological morphs. Significant genetic differences were found between migratory and non-migratory Rainbow trout (Hale et al 2013), the lake, river and stream ecotypes of sockeye salmon (Larson et al 2017) and ecologically different subpopulations of salmon (Vincent et al 2013;Cauwelier et al 2017). Sympatric ecotypes are found in several salmonid species, e.g.…”

Section: Genome-wide Separation Of Sympatric Morphsmentioning

confidence: 99%

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

Guðbrandsson

Kapralova

Franzdóttir

et al. 2018

Preprint

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The availability of diverse ecological niches can promote adaptation of trophic specializations and related traits, as has been repeatedly observed in evolutionary radiations of freshwater fish. The role of genetics, environment and history in ecologically driven divergence and adaptation, can be studied on adaptive radiations or populations showing ecological polymorphism. Salmonids, especially the Salvelinus genus, are renowned for both phenotypic diversity and polymorphism. Arctic charr (Salvelinus alpinus) invaded Icelandic streams during the glacial retreat (about 10,000 years ago) and exhibits many instances of sympatric polymorphism. Particularly well studied are the four morphs in Lake Þingvallavatn in Iceland. The small benthic (SB), large benthic (LB), planktivorous (PL) and piscivorous (PI) charr differ in many regards, including size, form and life history traits. To investigate relatedness and genomic differentiation between morphs we identified variable sites from RNA-sequencing data from three of those morphs, and verified 22 variants in population samples. The data reveal genetic differences between the morphs, with the two benthic morphs being more similar and the PL-charr more genetically different. The markers with high differentiation map to all linkage groups, suggesting ancient and pervasive genetic separation of these three morphs. Furthermore, GO analyses suggest differences in collagen metabolism, odontogenesis and sensory systems between PL-charr and the benthic morphs. Genotyping in population samples from all four morphs confirms the genetic separation and indicates that the PI-charr are less genetically distinct than the other three morphs. The genetic separation of the other three morphs indicates certain degree of reproductive isolation. The extent of gene flow between the morphs and the nature of reproductive barriers between them remain to be elucidated.

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Identification of a single genomic region associated with seasonal river return timing in adult Scottish Atlantic salmon (Salmo salar), using a genome-wide association study

Cited by 41 publications

References 66 publications

Life history genomic regions explain differences in Atlantic salmon marine diet specialization

Life history genomic regions explain differences in Atlantic salmon marine diet specialization

Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence‐related genes

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

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