Andrew P. Matala

Environmental adaptation in Chinook salmon (Oncorhynchus tshawytscha) throughout their North American range

Landscape genomics is a rapidly growing field with recent advances in both genotyping efficiency and statistical analyses that provide insight towards local adaptation of populations under varying environmental and selective pressure. Chinook salmon (Oncorhynchus tshawytscha) are a broadly distributed Pacific salmon species, occupying a diversity of habitats throughout the northeastern Pacific with pronounced variation in environmental and climate features but little is understood regarding local adaptation in this species. We used a multivariate method, redundancy analysis (RDA), to identify polygenic correlations between 19 703 SNP loci and a suite of environmental variables in 46 collections of Chinook salmon (1956 total individuals) distributed throughout much of its North American range. Models in RDA were conducted on both rangewide and regional scales by hierarchical partitioning of the populations into three distinct genetic lineages. Our results indicate that between 5.8 and 21.8% of genomic variation can be accounted for by environmental features, and 566 putatively adaptive loci were identified as targets of environmental adaptation. The most influential drivers of adaptive divergence included precipitation in the driest quarter of the year (Rangewide and North Coastal Lineage, anova P = 0.002 and 0.01, respectively), precipitation in the wettest quarter of the year (Interior Columbia River Stream‐Type Lineage, anova P = 0.03), variation in mean diurnal range in temperature (South Coastal Lineage, anova P = 0.005), and migration distance (Rangewide, anova P = 0.001). Our results indicate that environmental features are strong drivers of adaptive genomic divergence in this species, and provide a foundation to investigate how Chinook salmon might respond to global environmental change.

A centralized model for creating shared, standardized, microsatellite data that simplifies inter-laboratory collaboration

We demonstrate an efficient model for standardizing microsatellite DNA data among laboratories studying Oncorhynchus mykiss. Eight laboratories standardized 13 microsatellite loci following allele nomenclature of a central laboratory (average inter-laboratory genotyping concordance >98%). Following this central model, we have currently standardized 298 alleles from throughout the species native range. Although we focus here on O. mykiss, our experiences and recommendation apply equally to other broadly distributed species that may benefit from multi-laboratory collaborative data collection.

Major Lineages and Metapopulations in Columbia River Oncorhynchus mykiss Are Structured by Dynamic Landscape Features and Environments

Abstract It is widely recognized that genetic diversity within species is shaped by dynamic habitats. The quantitative and molecular genetic patterns observed are the result of demographics, mutation, migration, and adaptation. The populations of rainbow trout Oncorhynchus mykiss in the Columbia River basin (including both resident and anadromous forms and various subspecies) present a special challenge to understanding the relative roles of those factors. Standardized microsatellite data were compiled for 226 collections (15,658 individuals) from throughout the Columbia and Snake River basins to evaluate the genetic patterns of structure and adaptation. The data were primarily from fish of the anadromous life history form, and we used a population grouping procedure based on principal components and hierarchical k-means clustering to cluster populations into eight aggregates or groups with similar allele frequencies. These aggregates approximated geographic regions, and the two largest principal componen...

Resolving Adaptive and Demographic Divergence among Chinook Salmon Populations in the Columbia River Basin

Abstract Chinook salmon Oncorhynchus tshawytscha in the Columbia River basin (CRB) comprise three lineages—lower Columbia River and sympatric interior ocean and stream types—each with distinct biological attributes. To evaluate the adaptive and neutral genetic variation of this species in the CRB, we genotyped 54 Chinook salmon populations using a panel of 96 single-nucleotide polymorphism (SNP) loci. All three lineages were represented among the collections and were widely distributed across locations, ranging from the upper Salmon River to near the Columbia River estuary. Our goal was to explore local adaptation as a process shaping the population structure and genetic variation among Chinook salmon beyond the inferences possible with neutral marker data. In our analyses with putatively neutral SNPs, the population structure of Chinook salmon throughout the CRB was generally concordant with that of previous studies using microsatellites. Regression analyses and outlier methods identified 28, 17, and 29 ...

Examining genetic lineages of Chinook salmon in the Columbia River basin.

Abstract We examined 13 microsatellite loci from 51 collections of Chinook salmon Oncorhynchus tshawytscha throughout the Columbia River basin to determine membership in one of three major genetic lineages, introgression of genetic lineages within specific populations, and genetic structure at the subbasin level. Results confirm those of previous studies that three major lineages of Chinook salmon persist in the drainage, representing two interior life histories (ocean and stream types) and one lineage in the lower Columbia River. Novel observations of introgression were noted in specific collections, including three from the lower Columbia River (Sandy River, Kalama Hatchery, and Lewis Hatchery) and one stream-type population (Klickitat River). Estimates of genetic distance were larger in comparisons between ocean- and stream-type populations (G′ST = 0.429) and among stream-type and lower Columbia River populations (G′ST = 0.418) than between ocean-type and lower Columbia River populations (G′ST = 0.271)...

Relative contributions of neutral and non-neutral genetic differentiation to inform conservation of steelhead trout across highly variable landscapes

Mounting evidence of climatic effects on riverine environments and adaptive responses of fishes have elicited growing conservation concerns. Measures to rectify population declines include assessment of local extinction risk, population ecology, viability, and genetic differentiation. While conservation planning has been largely informed by neutral genetic structure, there has been a dearth of critical information regarding the role of non‐neutral or functional genetic variation. We evaluated genetic variation among steelhead trout of the Columbia River Basin, which supports diverse populations distributed among dynamic landscapes. We categorized 188 SNP loci as either putatively neutral or candidates for divergent selection (non‐neutral) using a multitest association approach. Neutral variation distinguished lineages and defined broad‐scale population structure consistent with previous studies, but fine‐scale resolution was also detected at levels not previously observed. Within distinct coastal and inland lineages, we identified nine and 22 candidate loci commonly associated with precipitation or temperature variables and putatively under divergent selection. Observed patterns of non‐neutral variation suggest overall climate is likely to shape local adaptation (e.g., potential rapid evolution) of steelhead trout in the Columbia River region. Broad geographic patterns of neutral and non‐neutral variation demonstrated here can be used to accommodate priorities for regional management and inform long‐term conservation of this species.

Candidate Genetic Markers Associated with Anadromy in Oncorhynchus mykiss of the Klickitat River

Abstract Both environmental and genetic factors influence anadromy in rainbow trout Oncorhynchus mykiss, but the genetic mechanisms that contribute to migratory selection are not well understood. In this study, we used a limited genome scan approach to identify candidate genetic markers associated with anadromy in 10 populations of O. mykiss from the Klickitat River, Washington. From an initial panel of 96 single-nucleotide polymorphism (SNP) markers, we identified 3 SNPs that were significantly associated with anadromy after accounting for underlying population structure and selective environmental conditions. Univariate logistic regression of allele frequencies and residency/anadromy were also significant, and thus three SNPs were considered candidate markers associated with anadromy (Omy_IL6–320, Omy_LDHB-2_i6, and Omy_ndk-152). A multivariate logistic model was developed from the allele frequencies of these three markers to predict the potential for anadromy in natural populations. This model was appl...

Climate variables explain neutral and adaptive variation within salmonid metapopulations: the importance of replication in landscape genetics

Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population‐specific and pairwise FST) within five metapopulations (79 populations, 4583 individuals) of steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin, USA. Using 151 putatively neutral and 29 candidate adaptive SNP loci, we found that climate‐related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables and FST across all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin‐wide to the metapopulation scale). Sensitivity analysis (leave‐one‐population‐out) revealed consistent relationships between climate variables and FST within three metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes (N = 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.

A genetically distinct wild redband trout (Oncorhynchus mykiss gairdneri) population in Crane Prairie Reservoir, Oregon, persists despite extensive stocking of hatchery rainbow trout (O. m. irideus)

Crane Prairie Reservoir in the upper Deschutes River Basin has historically supported a wild population of migratory Deschutes River redband trout. Owing to its status as a premier destination for recreational angling in Oregon, the reservoir has been stocked with domesticated hatchery rainbow trout since 1955. In recent years the wild redband trout population has experienced a substantial decline. Effects on productivity related to genetic interaction with naturally spawning hatchery-origin fish (fitness risks) have not been determined. The species Oncorhynchus mykiss has been characterized with substantial genetic diversity throughout the Deschutes River Basin that further heightens the challenge of identifying specific conservation needs of wild populations. A conservation plan for Crane Prairie wild redband trout requires a better understanding of the natural reproductive success of out-of-basin hatchery trout in the reservoir tributaries, and the similarity between Crane Prairie redband trout with other extant redband trout populations in the basin. Using a suite of 17 microsatellite nuclear DNA markers, we evaluated the genetic structure among Crane Prairie Reservoir redband trout, hatchery rainbow trout, and two adjacent populations of redband trout from within the Upper Deschutes River Basin. We observed significant heterogeneity between the hatchery and wild Crane Prairie populations that may reflect differences in life histories, differential productivity and assortative mating. The genetic distinctions observed among the three redband trout populations suggest restricted gene flow and genetic drift within the upper basin. Temporally stratified sampling and larger numbers of samples will be necessary to confirm these conclusions.

Influences of Hatchery Supplementation, Spawner Distribution, and Habitat on Genetic Structure of Chinook Salmon in the South Fork Salmon River, Idaho

Abstract We evaluated the genetic influence of hatchery supplementation on distinct naturally spawning populations of Chinook salmon Oncorhynchus tshawytscha in the South Fork Salmon River (SFSR), Idaho. Genetic tissue samples were collected from unmarked natural-origin and McCall Fish Hatchery (MFH)-reared Chinook salmon carcasses, and fish were identified by an adipose fin clip at five main-stem sites located both upstream and downstream of a seasonal exclusionary weir in the upper SFSR. We evaluated allele frequency data across 95 single-nucleotide polymorphism loci to determine the extent of genetic differentiation among collections. Genetic distance analyses and homogeneity tests indicated little subpopulation distinction in the upper SFSR. The weak overall genetic structure (global F ST = 0.010) is likely reflective of a population diversity similar to the historical structure with introgression by MFH stock in the naturally spawning population of the upper SFSR. Further analyses were conducted to e...