Screening of duplicated loci reveals hidden divergence patterns in a complex salmonid genome

Limborg, Morten T.; Larson, Wesley A.; Seeb, Lisa W.; Seeb, James E.

doi:10.1111/mec.14201

Cited by 20 publications

(20 citation statements)

References 78 publications

(170 reference statements)

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“…The three outliers, which were located on chromosomes 4, 8 and 28, were associated with two different functions: metabolism and osmoregulation/acid–base balancing. Inclusion of reads that could have mapped to paralogous loci (i.e., salmonids have many paralogous loci due to a genome duplication event ~125 million years ago (Allendorf & Thorgaard, ; Macqueen & Johnston, )) changed the amplitude of the Z ( F ST ) estimates, but not the location of high Z ( F ST ) regions (Supporting Information Figure ; Limborg, Larson, Seeb & Seeb, ). Furthermore, we did not find any evidence that the location of transposable elements (Supporting Information Figure ) or copy number variation (Supporting Information Figure ) played a role in the adaptation of steelhead to Lake Michigan.…”

Section: Resultsmentioning

confidence: 99%

Rapid genetic adaptation to a novel environment despite a genome‐wide reduction in genetic diversity

et al. 2018

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Introduced species often colonize regions that have vastly different ecological and environmental conditions than those found in their native range. As such, species introductions can provide a deeper understanding into the process of adaptive evolution. In the 1880s, steelhead trout (Oncorhynchus mykiss) from California were introduced into Lake Michigan (Laurentian Great Lakes, North America) where they established naturally reproducing populations. In their native range, steelhead hatch in rivers, migrate to the ocean and return to freshwater to spawn. Steelhead in Lake Michigan continue to swim up rivers to spawn, but now treat the freshwater environment of the Great Lakes as a surrogate ocean. To examine the effects of this introduction, we sequenced the genomes of 264 fish. By comparing steelhead from Lake Michigan to steelhead from their ancestral range, we determined that the introduction led to consistent reductions in genetic diversity across all 29 chromosomes. Despite this reduction in genetic diversity, three chromosomal regions were associated with rapid genetic adaptation to the novel environment. The first region contained functional changes to ceramide kinase, which likely altered metabolic and wound-healing rates in Lake Michigan steelhead. The second and third regions encoded carbonic anhydrases and a solute carrier protein, both of which are critical for osmoregulation, and demonstrate how steelhead physiologically adapted to freshwater. Furthermore, the contemporary release of diverse hatchery strains into the lake increased genetic diversity but reduced the signature of genetic adaptation. This study illustrates that species can rapidly adapt to novel environments despite genome-wide reductions in genetic diversity.

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Section: Resultsmentioning

confidence: 99%

Rapid genetic adaptation to a novel environment despite a genome‐wide reduction in genetic diversity

et al. 2018

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“…Thus, duplicated genes disproportionately expand the adaptive capacity and potential phenotypic complexity of organisms with at least partially duplicated genomes (Freeling & Thomas, ). Initial investigations of duplicated loci in O. nerka identified outliers of putative adaptive significance among migratory phenotypes (anadromous sockeye salmon and non‐anadromous kokanee) and among reproductive ecotypes (stream‐, river‐ and beach‐spawning sockeye salmon) (Limborg, Larson, Seeb, & Seeb, ).…”

Section: Discussionmentioning

confidence: 99%

Reliance on lakes by salmon, trout and charr (Oncorhynchus,SalmoandSalvelinus): An evaluation of spawning habitats, rearing strategies and trophic polymorphisms

Arostegui

Quinn

2019

Fish and Fisheries

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Salmonid fishes may reside within or migrate between stream and lake habitats, or undergo anadromous migrations between freshwater and the ocean. While the degree of anadromy of salmonids has been thoroughly compared, no analogous review has examined the degree of lake use. To assess the extent of reliance on lake habitat in this family, we considered 16 species of salmon, trout and charr from the genera Oncorhynchus, Salmo and Salvelinus, comparing their (a) use of lakes as spawning habitat, (b) rearing strategies in lakes, and (c) occurrence and diversity of lacustrine trophic polymorphism. In identifying the primary life‐history patterns of each species and exploring the lesser‐known lacustrine behaviours, we found that the extent of reliance on lakes exhibits a negative association with the degree of anadromy. Oncorhynchus rely least on lakes, Salmo to an intermediate level and Salvelinus the most, opposite of the general prevalence of anadromy among these genera. Lakes are critical to adfluvial and lake‐resident salmonids, but they also support anadromous and fluvial life histories by providing spawning, rearing, overwintering and/or summer refuge habitat. Adfluviality, although a non‐anadromous life history, consists of similar migration‐related traits and behaviours as anadromy, including the parr–smolt transformation, sex‐biased patterns of migration and residency, and the presence of precocious males. Lakes support life‐history variants, reproductive ecotypes and trophic morphs unique to lacustrine habitat. Therefore, conservation of salmonids is dependent on maintaining the diversity and quality of their habitats, including lakes.

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“…Previous research in sockeye salmon has documented strong signals of selection in a number of drainages throughout the species range (e.g., Limborg, Larson, Seeb, & Seeb, ; Nichols, Kozfkay, & Narum, ). For example, multiple studies have found strong evidence of selection at major histocompatibility complex (MHC) genes (Gomez‐Uchida et al, ; McClelland et al, ; Miller, Kaukinen, Beacham, & Withler, ).…”

Section: Introductionmentioning

confidence: 99%

Parallel signatures of selection at genomic islands of divergence and the major histocompatibility complex in ecotypes of sockeye salmon across Alaska

et al. 2019

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Understanding the genetic mechanisms that facilitate adaptive radiation is an important component of evolutionary biology. Here, we genotyped 82 neutral SNPs, seven SNPs in islands of divergence identified in a previous study (island SNPs), and a region of the major histocompatibility complex (MHC) in 32 populations of sockeye salmon to investigate whether conserved genes and genomic regions are involved in adaptive radiation. Populations representing three ecotypes were sampled from seven drainages with differing habitats and colonization histories spanning a range of 2,000 km. We found strong signatures of parallel selection across drainages at the island SNPs and MHC, suggesting that the same loci undergo divergent selection during adaptive radiation. However, patterns of differentiation at most island SNPs and the MHC were not associated with ecotypes, suggesting that these loci are responding differently to a mosaic of selective pressures. Our study provides some of the first evidence that conserved genomic islands may be involved in adaptive divergence of salmon populations. Additionally, our data provide further support for the hypothesis that sockeye salmon inhabiting rivers unconnected to lakes harbour similar genetic diversity across large distances, are likely the ancestral form of the species, and have repeatedly recolonized lake systems as they have become available after glacial recession. Finally, our results highlight the value and importance of validating outlier loci by screening additional populations and regions, a practice that will hopefully become more common in the future.

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Screening of duplicated loci reveals hidden divergence patterns in a complex salmonid genome

Cited by 20 publications

References 78 publications

Rapid genetic adaptation to a novel environment despite a genome‐wide reduction in genetic diversity

Rapid genetic adaptation to a novel environment despite a genome‐wide reduction in genetic diversity

Reliance on lakes by salmon, trout and charr (Oncorhynchus,SalmoandSalvelinus): An evaluation of spawning habitats, rearing strategies and trophic polymorphisms

Parallel signatures of selection at genomic islands of divergence and the major histocompatibility complex in ecotypes of sockeye salmon across Alaska

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