Comparative genomics of rainbow trout (Oncorhynchus mykiss): Is the genetic architecture of migratory behavior conserved among populations?

Rainbow trout (Oncorhynchus mykiss) are a partially migratory species wherein some individuals undergo long-distance anadromous migrations, and others stay as residents in their native freshwater streams. The decision to migrate is known to be highly heritable, and yet, the underlying genes and alleles associated with migration are not fully characterized. Here we used a pooled approach of whole-genome sequence data from migratory and resident trout of two native populations-Sashin Creek, Alaska and Little Sheep Creek, Oregon-to obtain a genome-wide perspective of the genetic architecture of resident and migratory life history. We calculated estimates of genetic differentiation, genetic diversity, and selection between the two phenotypes to locate regions of interest and then compared these associations between populations. We identified numerous genes and alleles associated with life history development in the Sashin Creek population with a notable area on chromosome 8 that may play a critical role in the development of the migratory phenotype. However, very few alleles appeared to be associated with life history development in the Little Sheep Creek system, suggesting population-specific genetic effects are likely important in the development of anadromy. Our results indicate that a migratory life history is not controlled by a singular gene or region but supports the idea that there are many independent ways for a migratory phenotype to emerge in a population. Therefore, conserving and promoting genetic diversity in migratory individuals is paramount to conserving these populations. Ultimately, our data add to a growing body of literature that suggests that population-specific genetic effects, likely mediated through environmental variation, contribute to life history development in rainbow trout.

Affordable de novo generation of fish mitogenomes using amplification-free enrichment of mitochondrial DNA and deep sequencing of long fragments.

Biomonitoring surveys make use of metabarcoding tools to describe the community composition. These studies match their sequencing results against public genomic databases to identify the species. However, mitochondrial genomic reference data are yet incomplete, only a few genes may be available, or the suitability of existing sequence data is suboptimal for species level resolution. Here, we present a dedicated and cost-effective workflow with no DNA amplification for generating complete fish mitogenomes for the purpose of strengthening fish mitochondrial databases. Two different strategies using long fragment sequencing with Oxford Nanopore technology coupled with mitochondrial DNA enrichment were used. One where the enrichment is achieved by preferential isolation of mitochondria followed by DNA extraction and nuclear DNA depletion ("mitoenrichment"). A second enrichment approach takes advantage of the CRISPR Cas9 targeted scission on previously dephosphorylated DNA ("targeted mitosequencing"). The sequencing results varied between tissue, species, and integrity of the DNA. The mitoenrichment method yielded 0.17%-12.33% of sequences on target and a mean coverage ranging from 74.9 to 805-fold. The targeted mitosequencing experiment from native genomic DNA yielded 1.83%-55% of sequences on target and a 38 to 2123-fold mean coverage. These produced complete mitogenomes of species with homopolymeric regions, tandem repeats, and gene rearrangements. We demonstrate that deep sequencing of long fragments of native fish DNA can be achieved with low computational resources in a cost-effective manner, opening the discovery of mitogenomes of nonmodel or understudied fish taxa to a broad range of laboratories worldwide.

Los estudios de biomonitoreo utilizan herramientas de caracterización genética (metabarcoding) para describir la composición de la comunidad. Estos estudios contrastan las secuencias obtenidas con bases de datos genómicas públicas para así identificar la especie. Sin embargo, las bases de datos mitocondriales de referencia distan mucho de estar completas. En la mayor parte de los casos solo hay unos pocos genes disponibles o los datos existentes no ofrecen resolución hasta el nivel de especie. En este estudio presentamos un método dedicado a generar mitogenomas de peces completos de forma rentable y sin necesidad de amplificación del ADN, con el objeto de ampliar las bases de datos mitocondriales de peces. Para ello se utilizaron dos enfoques diferentes de secuenciación de fragmentos largos utilizando secuenciación Oxford Nanopore y enriquecimiento de ADN mitocondrial. Uno en el que el enriquecimiento se logra mediante el aislamiento preferencial de mitocondrias seguido de extracción del ADN y la eliminación del ADN nuclear ("mitoenriquecimiento"). En el segundo enfoque se aprovecha la capacidad de escisión dirigida por la endonucleasa CRISPR-Cas9 sobre ADN previamente desfosforilado ("mitosecuenciación dirigida"). Los resultados difirieron con el tejido, la especie y la integridad del ADN. El método de mitoenriquecimiento produjo un 0,17%-12,33% de secuencias objetivo y una cobertura media entre 74,9 y 805 secuencias. El experimento de mitosecuenciación dirigida a partir de ADN genómico nativo produjo entre 1,83 y 55% de secuencias objetivo y una cobertura media de 38 a 2123 secuencias. Este estudio permitió completar mitogenomas de diferentes especies que incluyen regiones homopoliméricas, repeticiones en tándem y reorganización de genes. Demostramos que la secuenciación intensiva de fragmentos largos de ADN de peces es posible, se puede lograr con bajos recursos informáticos de una manera económica, superando el método generalizado de secuenciación genómica de baja cobertura y permitiendo el descubrimiento de mitogenomas de taxones de peces no modelo o poco estudiados a una amplia gama de laboratorios en todo el mundo.

Correction: Fraik et al. The Impacts of Dam Construction and Removal on the Genetics of Recovering Steelhead (Oncorhynchus mykiss) Populations across the Elwha River Watershed. Genes 2021, 12, 89.

In the original publication [...].

Environmental DNA provides quantitative estimates of Pacific hake abundance and distribution in the open ocean.

All species inevitably leave genetic traces in their environments, and the resulting environmental DNA (eDNA) reflects the species present in a given habitat. It remains unclear whether eDNA signals can provide quantitative metrics of abundance on which human livelihoods or conservation successes depend. Here, we report the results of a large eDNA ocean survey (spanning 86 000 km2 to depths of 500 m) to understand the abundance and distribution of Pacific hake (Merluccius productus), the target of the largest finfish fishery along the west coast of the USA. We sampled eDNA in parallel with a traditional acoustic-trawl survey to assess the value of eDNA surveys at a scale relevant to fisheries management. Despite local differences, the two methods yield comparable information about the broad-scale spatial distribution and abundance. Furthermore, we find depth and spatial patterns of eDNA closely correspond to acoustic-trawl estimates for hake. We demonstrate the power and efficacy of eDNA sampling for estimating abundance and distribution and move the analysis eDNA data beyond sample-to-sample comparisons to management relevant scales. We posit that eDNA methods are capable of providing general quantitative applications that will prove especially valuable in data- or resource-limited contexts.

Differential gene expression associated with behavioral variation in ecotypes of Lake Superior brook trout (Salvelinus fontinalis).

Associations between behaviors and the development of different life history tactics have been documented in several species of salmon, trout, and charr. While it is well known that such behaviors are heritable the genes and molecular pathways connected to these behaviors remain unknown. We used an RNA-seq approach to identify genes and molecular pathways differentially regulated in brain tissue between "shy" and "bold" brook trout (Salvelinus fontinalis). A small number of genes were differentially expressed between the behavioral types at several months after hatching and two years of age. Pathway analysis revealed that EIF2 signaling differed consistently between shy and bold individuals suggesting large-scale differences in protein synthesis between behavioral types in the brain. Additionally, the RNA-seq data were used to find polymorphisms within the brook trout genome and a GWAS approach was used to test for statistical associations between genetic variants and behavior type. One allele located in a transcription factor (TSHZ3) contained a protein-coding non-synonymous SNP suggesting that functional variation within TSHZ3 is connected to the development of different behaviors. These results suggest that the molecular basis of behavioral development is complex and due to the differential expression of many genes involved in a wide-range of different molecular pathways.

Allelic diversification after transposable element exaptation promoted gsdf as the master sex determining gene of sablefish.

Concepts of evolutionary biology suggest that morphological change may occur by rare punctual but rather large changes, or by more steady and gradual transformations. It can therefore be asked whether genetic changes underlying morphological, physiological, and/or behavioral innovations during evolution occur in a punctual manner, whereby a single mutational event has prominent phenotypic consequences, or if many consecutive alterations in the DNA over longer time periods lead to phenotypic divergence. In the marine teleost, sablefish (Anoplopoma fimbria), complementary genomic and genetic studies led to the identification of a sex locus on the Y Chromosome. Further characterization of this locus resulted in identification of the transforming growth factor, beta receptor 1a (tgfbr1a) gene, gonadal somatic cell derived factor (gsdf), as the main candidate for fulfilling the master sex determining (MSD) function. The presence of different X and Y Chromosome copies of this gene indicated that the male heterogametic (XY) system of sex determination in sablefish arose by allelic diversification. The gsdfY gene has a spatio-temporal expression profile characteristic of a male MSD gene. We provide experimental evidence demonstrating a pivotal role of a transposable element (TE) for the divergent function of gsdfY By insertion within the gsdfY promoter region, this TE generated allelic diversification by bringing cis-regulatory modules that led to transcriptional rewiring and thus creation of a new MSD gene. This points out, for the first time in the scenario of MSD gene evolution by allelic diversification, a single, punctual molecular event in the appearance of a new trigger for male development.

The rise and fall of the ancient northern pike master sex-determining gene.

The understanding of the evolution of variable sex determination mechanisms across taxa requires comparative studies among closely related species. Following the fate of a known master sex-determining gene, we traced the evolution of sex determination in an entire teleost order (Esociformes). We discovered that the northern pike (Esox lucius) master sex-determining gene originated from a 65 to 90 million-year-old gene duplication event and that it remained sex linked on undifferentiated sex chromosomes for at least 56 million years in multiple species. We identified several independent species- or population-specific sex determination transitions, including a recent loss of a Y chromosome. These findings highlight the diversity of evolutionary fates of master sex-determining genes and the importance of population demographic history in sex determination studies. We hypothesize that occasional sex reversals and genetic bottlenecks provide a non-adaptive explanation for sex determination transitions.

The Impacts of Dam Construction and Removal on the Genetics of Recovering Steelhead (Oncorhynchus mykiss) Populations across the Elwha River Watershed.

Dam construction and longitudinal river habitat fragmentation disrupt important life histories and movement of aquatic species. This is especially true for Oncorhynchus mykiss that exhibits both migratory (steelhead) and non-migratory (resident rainbow) forms. While the negative effects of dams on salmonids have been extensively documented, few studies have had the opportunity to compare population genetic diversity and structure prior to and following dam removal. Here we examine the impacts of the removal of two dams on the Elwha River on the population genetics of O. mykiss. Genetic data were produced from >1200 samples collected prior to dam removal from both life history forms, and post-dam removal from steelhead. We identified three genetic clusters prior to dam removal primarily explained by isolation due to dams and natural barriers. Following dam removal, genetic structure decreased and admixture increased. Despite large O. mykiss population declines after dam construction, we did not detect shifts in population genetic diversity or allele frequencies of loci putatively involved in migratory phenotypic variation. Steelhead descendants from formerly below and above dammed populations recolonized the river rapidly after dam removal, suggesting that dam construction did not significantly reduce genetic diversity underlying O. mykiss life history strategies. These results have significant evolutionary implications for the conservation of migratory adaptive potential in O. mykiss populations above current anthropogenic barriers.

A mobile sex-determining region, male-specific haplotypes and rearing environment influence age at maturity in Chinook salmon.

Variation in age at maturity is an important contributor to life history and demographic variation within and among species. The optimal age at maturity can vary by sex, and the ability of each sex to evolve towards its fitness optimum depends on the genetic architecture of maturation. Using GWAS of RAD sequencing data, we show that age at maturity in Chinook salmon exhibits sex-specific genetic architecture, with age at maturity in males influenced by large (up to 20 Mb) male-specific haplotypes. These regions showed no such effect in females. We also provide evidence for translocation of the sex-determining gene between two different chromosomes. This has important implications for sexually antagonistic selection, particularly that sex linkage of adaptive genes may differ within and among populations based on chromosomal location of the sex-determining gene. Our findings will facilitate research into the genetic causes of shifting demography in Chinook salmon as well as a better understanding of sex determination in this species and Pacific salmon in general.

Strong population differentiation in lingcod (Ophiodon elongatus) is driven by a small portion of the genome.

Delimiting intraspecific genetic variation in harvested species is crucial to the assessment of population status for natural resource management and conservation purposes. Here, we evaluated genetic population structure in lingcod (Ophiodon elongatus), a commercially and recreationally important fishery species along the west coast of North America. We used 16,749 restriction site-associated DNA sequencing (RADseq) markers, in 611 individuals collected from across the bulk of the species range from Southeast Alaska to Baja California, Mexico. In contrast to previous population genetic work on this species, we found strong evidence for two distinct genetic clusters. These groups separated latitudinally with a break near Point Reyes off Northern California, and there was a high frequency of admixed individuals in close proximity to the break. F-statistics corroborate this genetic break between northern and southern sampling sites, although most loci are characterized by low FST values, suggesting high gene flow throughout most of the genome. Outlier analyses identified 182 loci putatively under divergent selection, most of which mapped to a single genomic region. When individuals were grouped by cluster assignment (northern, southern, and admixed), 71 loci were fixed between the northern and southern cluster, all of which were identified in the outlier scans. All individuals identified as admixed exhibited near 50:50 assignment to northern and southern clusters and were heterozygous for most fixed loci. Alignments of RADseq loci to a draft lingcod genome assembly and three other teleost genomes with chromosome-level assemblies suggest that outlier and fixed loci are concentrated on a single chromosome. Similar genomic patterns have been attributed to chromosomal inversions in diverse taxonomic groups. Regardless of the evolutionary mechanism, these results represent novel observations of genetic structure in lingcod and designate clear evolutionary units that could be used to inform fisheries management.

A large-scale chromosomal inversion is not associated with life history development in rainbow trout from Southeast Alaska.

In studying the causative mechanisms behind migration and life history, the salmonids-salmon, trout, and charr-are an exemplary taxonomic group, as life history development is known to have a strong genetic component. A double inversion located on chromosome 5 in rainbow trout (Oncorhynchus mykiss) is associated with life history development in multiple populations, but the importance of this inversion has not been thoroughly tested in conjunction with other polymorphisms in the genome. To that end, we used a high-density SNP chip to genotype 192 F1 migratory and resident rainbow trout and focused our analyses to determine whether this inversion is important in life history development in a well-studied population of rainbow trout from Southeast Alaska. We identified 4,994 and 436 SNPs-predominantly outside of the inversion region-associated with life history development in the migrant and resident familial lines, respectively. Although F1 samples showed genomic patterns consistent with the double inversion on chromosome 5 (reduced observed and expected heterozygosity and an increase in linkage disequilibrium), we found no statistical association between the inversion and life history development. Progeny produced by crossing resident trout and progeny produced by crossing migrant trout both consisted of a mix of migrant and resident individuals, irrespective of the individuals' inversion haplotype on chromosome 5. This suggests that although the inversion is present at a low frequency, it is not strongly associated with migration as it is in populations of Oncorhynchus mykiss from lower latitudes.

Uncovering mechanisms of global ocean change effects on the Dungeness crab (Cancer magister) through metabolomics analysis.

The Dungeness crab is an economically and ecologically important species distributed along the North American Pacific coast. To predict how Dungeness crab may physiologically respond to future global ocean change on a molecular level, we performed untargeted metabolomic approaches on individual Dungeness crab juveniles reared in treatments that mimicked current and projected future pH and dissolved oxygen conditions. We found 94 metabolites and 127 lipids responded in a condition-specific manner, with a greater number of known compounds more strongly responding to low oxygen than low pH exposure. Pathway analysis of these compounds revealed that juveniles may respond to low oxygen through evolutionarily conserved processes including downregulating glutathione biosynthesis and upregulating glycogen storage, and may respond to low pH by increasing ATP production. Most interestingly, we found that the response of juveniles to combined low pH and low oxygen exposure was most similar to the low oxygen exposure response, indicating low oxygen may drive the physiology of juvenile crabs more than pH. Our study elucidates metabolic dynamics that expand our overall understanding of how the species might respond to future ocean conditions and provides a comprehensive dataset that could be used in future ocean acidification response studies.

Temporal Dynamics of DNA Methylation Patterns in Response to Rearing Juvenile Steelhead (Oncorhynchus mykiss) in a Hatchery versus Simulated Stream Environment.

Genetic selection is often implicated as the underlying cause of heritable phenotypic differences between hatchery and wild populations of steelhead trout (Oncorhynchus mykiss) that also differ in lifetime fitness. Developmental plasticity, which can also affect fitness, may be mediated by epigenetic mechanisms such as DNA methylation. Our previous study identified significant differences in DNA methylation between adult hatchery- and natural-origin steelhead from the same population that could not be distinguished by DNA sequence variation. In the current study, we tested whether hatchery-rearing conditions can influence patterns of DNA methylation in steelhead with known genetic backgrounds, and assessed the stability of these changes over time. Eyed-embryos from 22 families of Methow River steelhead were split across traditional hatchery tanks or a simulated stream-rearing environment for 8 months, followed by a second year in a common hatchery tank environment. Family assignments were made using a genetic parentage analysis to account for relatedness among individuals. DNA methylation patterns were examined in the liver, a relatively homogeneous organ that regulates metabolic processes and somatic growth, of juveniles at two time points: after eight months of rearing in either a tank or stream environment and after a subsequent year of rearing in a common tank environment. Further, we analyzed DNA methylation in the sperm of mature 2-year-old males from the earlier described treatments to assess the potential of environmentally-induced changes to be passed to offspring. Hepatic DNA methylation changes in response to hatchery versus stream-rearing in yearling fish were substantial, but few persisted after a second year in the tank environment. However, the early rearing environment appeared to affect how fish responded to developmental and environmental signals during the second year since novel DNA methylation differences were identified in the livers of hatchery versus stream-reared fish after a year of common tank rearing. Furthermore, we found profound differences in DNA methylation due to age, irrespective of rearing treatment. This could be due to smoltification associated changes in liver physiology after the second year of rearing. Although few rearing-treatment effects were observed in the sperm methylome, strong family effects were observed. These data suggest limited potential for intergenerational changes, but highlight the importance of understanding the effects of kinship among studied individuals in order to properly analyze and interpret DNA methylation data in natural populations. Our work is the first to study family effects and temporal dynamics of DNA methylation patterns in response to hatchery-rearing.

Long-Term Conservation of Ohnologs Through Partial Tetrasomy Following Whole-Genome Duplication in Salmonidae.

Whole-genome duplications (WGDs) have occurred repeatedly and broadly throughout the evolutionary history of eukaryotes. However, the effects of WGD on genome function and evolution remain unclear. The salmonid WGD that occurred approximately 88 million years ago presents an excellent opportunity for studying the effects of WGD as ∼10-15% of each salmonid genome still exhibits tetrasomic inheritance. Herein, we utilized the rainbow trout (Oncorhynchus mykiss) genome assembly and brain transcriptome data to examine the fate of gene pairs (ohnologs) following the salmonid whole-genome duplication. We find higher sequence identity between ohnologs located within known tetrasomic regions than between ohnologs found in disomic regions, and that tetrasomically inherited ohnologs showed greater similarity in patterns of gene expression and per ohnolog were lower expressed, than disomically inherited ohnologs. Enrichment testing for Gene Ontology terms identified 49 over-represented terms in tetrasomically inherited ohnologs compared to disomic ohnologs. However, why these ohnologs are retained as tetrasomic is difficult to answer. It could be that we have identified salmonid specific "dangerous duplicates", that is, genes that cannot take on new roles following WGD. Alternatively, there may be adaptive advantages for retaining genes as functional duplicates in tetrasomic regions, as presumably, movement of these genes into disomic regions would affect both their sequence identity and their gene expression patterns.

Characterization of Genetic and Epigenetic Variation in Sperm and Red Blood Cells from Adult Hatchery and Natural-Origin Steelhead, Oncorhynchus mykiss.

While the goal of most conservation hatchery programs is to produce fish that are genetically and phenotypically indistinguishable from the wild stocks they aim to restore, there is considerable evidence that salmon and steelhead reared in hatcheries differ from wild fish in phenotypic traits related to fitness. Some evidence suggests that these phenotypic differences have a genetic basis (e.g., domestication selection) but another likely mechanism that remains largely unexplored is that differences between hatchery and wild populations arise as a result of environmentally-induced heritable epigenetic change. As a first step toward understanding the potential contribution of these two possible mechanisms, we describe genetic and epigenetic variation in hatchery and natural-origin adult steelhead, Oncorhynchus mykiss, from the Methow River, WA. Our main objectives were to determine if hatchery and natural-origin fish could be distinguished genetically and whether differences in epigenetic programming (DNA methylation) in somatic and germ cells could be detected between the two groups. Genetic analysis of 72 fish using 936 SNPs generated by Restriction Site Associated DNA Sequencing (RAD-Seq) did not reveal differentiation between hatchery and natural-origin fish at a population level. We performed Reduced Representation Bisulfite Sequencing (RRBS) on a subset of 10 hatchery and 10 natural-origin fish and report the first genome-wide characterization of somatic (red blood cells (RBCs)) and germ line (sperm) derived DNA methylomes in a salmonid, from which we identified considerable tissue-specific methylation. We identified 85 differentially methylated regions (DMRs) in RBCs and 108 DMRs in sperm of steelhead reared for their first year in a hatchery environment compared to those reared in the wild. This work provides support that epigenetic mechanisms may serve as a link between hatchery rearing and adult phenotype in steelhead; furthermore, DMRs identified in germ cells (sperm) highlight the potential for these changes to be passed on to future generations.

Evidence of sex-bias in gene expression in the brain transcriptome of two populations of rainbow trout (Oncorhynchus mykiss) with divergent life histories.

Sex-bias in gene expression is a mechanism that can generate phenotypic variance between the sexes, however, relatively little is known about how patterns of sex-bias vary during development, and how variable sex-bias is between different populations. To that end, we measured sex-bias in gene expression in the brain transcriptome of rainbow trout (Oncorhynchus mykiss) during the first two years of development. Our sampling included from the fry stage through to when O. mykiss either migrate to the ocean or remain resident and undergo sexual maturation. Samples came from two F1 lines: One from migratory steelhead trout and one from resident rainbow trout. All samples were reared in a common garden environment and RNA sequencing (RNA-seq) was used to estimate patterns of gene expression. A total of 1,716 (4.6% of total) genes showed evidence of sex-bias in gene expression in at least one time point. The majority (96.7%) of sex-biased genes were differentially expressed during the second year of development, indicating that patterns of sex-bias in expression are tied to key developmental events, such as migration and sexual maturation. Mapping of differentially expressed genes to the O. mykiss genome revealed that the X chromosome is enriched for female upregulated genes, and this may indicate a lack of dosage compensation in rainbow trout. There were many more sex-biased genes in the migratory line than the resident line suggesting differences in patterns of gene expression in the brain between populations subjected to different forces of selection. Overall, our results suggest that there is considerable variation in the extent and identity of genes exhibiting sex-bias during the first two years of life. These differentially expressed genes may be connected to developmental differences between the sexes, and/or between adopting a resident or migratory life history.

Using Linkage Maps as a Tool To Determine Patterns of Chromosome Synteny in the Genus Salvelinus.

Next generation sequencing techniques have revolutionized the collection of genome and transcriptome data from nonmodel organisms. This manuscript details the application of restriction site-associated DNA sequencing (RADseq) to generate a marker-dense genetic map for Brook Trout (Salvelinus fontinalis). The consensus map was constructed from three full-sib families totaling 176 F1 individuals. The map consisted of 42 linkage groups with a total female map size of 2502.5 cM, and a total male map size of 1863.8 cM. Synteny was confirmed with Atlantic Salmon for 38 linkage groups, with Rainbow Trout for 37 linkage groups, Arctic Char for 36 linkage groups, and with a previously published Brook Trout linkage map for 39 linkage groups. Comparative mapping confirmed the presence of 8 metacentric and 34 acrocentric chromosomes in Brook Trout. Six metacentric chromosomes seem to be conserved with Arctic Char suggesting there have been at least two species-specific fusion and fission events within the genus Salvelinus In addition, the sex marker (sdY; sexually dimorphic on the Y chromosome) was mapped to Brook Trout BC35, which is homologous with Atlantic Salmon Ssa09qa, Rainbow Trout Omy25, and Arctic Char AC04q. Ultimately, this linkage map will be a useful resource for studies on the genome organization of Salvelinus, and facilitates comparisons of the Salvelinus genome with Salmo and Oncorhynchus.

Functional Annotation of All Salmonid Genomes (FAASG): an international initiative supporting future salmonid research, conservation and aquaculture.

We describe an emerging initiative - the 'Functional Annotation of All Salmonid Genomes' (FAASG), which will leverage the extensive trait diversity that has evolved since a whole genome duplication event in the salmonid ancestor, to develop an integrative understanding of the functional genomic basis of phenotypic variation. The outcomes of FAASG will have diverse applications, ranging from improved understanding of genome evolution, to improving the efficiency and sustainability of aquaculture production, supporting the future of fundamental and applied research in an iconic fish lineage of major societal importance.

Genomic signatures among Oncorhynchus nerka ecotypes to inform conservation and management of endangered Sockeye Salmon.

Conservation of life history variation is an important consideration for many species with trade-offs in migratory characteristics. Many salmonid species exhibit both resident and migratory strategies that capitalize on benefits in freshwater and marine environments. In this study, we investigated genomic signatures for migratory life history in collections of resident and anadromous Oncorhynchus nerka (Kokanee and Sockeye Salmon, respectively) from two lake systems, using ~2,600 SNPs from restriction-site-associated DNA sequencing (RAD-seq). Differing demographic histories were evident in the two systems where one pair was significantly differentiated (Redfish Lake, FST = 0.091 [95% confidence interval: 0.087 to 0.095]) but the other pair was not (Alturas Lake, FST = -0.007 [-0.008 to -0.006]). Outlier and association analyses identified several candidate markers in each population pair, but there was limited evidence for parallel signatures of genomic variation associated with migration. Despite lack of evidence for consistent markers associated with migratory life history in this species, candidate markers were mapped to functional genes and provide evidence for adaptive genetic variation within each lake system. Life history variation has been maintained in these nearly extirpated populations of O. nerka, and conservation efforts to preserve this diversity are important for long-term resiliency of this species.