Correction: Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon.

[This corrects the article DOI: 10.1371/journal.pgen.1008348.].

Ancestry and genetic structure of resident and anadromous rainbow trout (Oncorhynchus mykiss) in Argentina.

Since the first introduction from North America more than a century ago, rainbow trout (Oncorhynchus mykiss) have rapidly established self-sustaining populations in major river basins of Patagonia. Many generations later, only the freshwater resident life history is expressed in the Chubut and Negro rivers of northern Argentinian Patagonia, whereas both the resident and anadromous life histories are found in the Santa Cruz River of southern Argentina. Despite previous studies that have tried to identify the sources of these introduced populations, uncertainty still exists. Here we combined data from many single-nucleotide polymorphisms and microsatellite loci in O. mykiss populations from Argentina and North America to evaluate putative source populations, gene flow between Argentinian river basins, and genetic diversity differences between Argentinian and North American populations. We found that populations from northern and southern Patagonia are highly differentiated and have limited gene flow between them. Phylogeographic analysis also confirmed that they have separate origins, with the northern populations most closely related to the domesticated rainbow trout strains that are raised worldwide and the Santa Cruz River populations most closely related to North American populations from California and Oregon that have an anadromous component. In addition, fish with different life histories in the Santa Cruz River were found to constitute a single interbreeding population. No evidence was found of reduced genetic variation in introduced rainbow trout, suggesting multiple contributing sources. In spite of these advances in understanding, significant questions remain regarding the origins and evolution of the introduced O. mykiss in Patagonia.

Distinct patterns of inheritance shape life-history traits in steelhead trout.

Life-history variation is the raw material of adaptation, and understanding its genetic and environmental underpinnings is key to designing effective conservation strategies. We used large-scale genetic pedigree reconstruction of anadromous steelhead trout (Oncorhynchus mykiss) from the Russian River, CA, USA, to elucidate sex-specific patterns of life-history traits and their heritability. SNP data from adults returning from sea over a 14-year period were used to identify 13,474 parent-offspring trios. These pedigrees were used to determine age structure, size distributions and family sizes for these fish, as well as to estimate the heritability of two key life-history traits, spawn date and age at maturity (first reproduction). Spawn date was highly heritable (h2 = 0.73) and had a cross-sex genetic correlation near unity. We provide the first estimate of heritability for age at maturity in ocean-going fish from this species and found it to be highly heritable (h2 from 0.29 to 0.62, depending on sex and method), with a much lower genetic correlation across sexes. We also evaluated genotypes at a migration-associated inversion polymorphism and found sex-specific correlations with age at maturity. The significant heritability of these two key reproductive traits in these imperiled fish, and their patterns of inheritance in the two sexes, is consistent with predictions of both natural and sexually antagonistic selection (sexes experience opposing selection pressures). This emphasizes the importance of anthropogenic factors, including hatchery practices and ecosystem modifications, in shaping the fitness of this species, thus providing important guidance for management and conservation efforts.

Long-distance migration is a major factor driving local adaptation at continental scale in Coho salmon.

Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species' homing behaviour may promote the establishment of local adaptation. We genotyped 7829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. The results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidate single nucleotide polymorphisms associated with long-distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.

Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon.

A thorough reconstruction of historical processes is essential for a comprehensive understanding of the mechanisms shaping patterns of genetic diversity. Indeed, past and current conditions influencing effective population size have important evolutionary implications for the efficacy of selection, increased accumulation of deleterious mutations, and loss of adaptive potential. Here, we gather extensive genome-wide data that represent the extant diversity of the Coho salmon (Oncorhynchus kisutch) to address two objectives. We demonstrate that a single glacial refugium is the source of most of the present-day genetic diversity, with detectable inputs from a putative secondary micro-refugium. We found statistical support for a scenario whereby ancestral populations located south of the ice sheets expanded recently, swamping out most of the diversity from other putative micro-refugia. Demographic inferences revealed that genetic diversity was also affected by linked selection in large parts of the genome. Moreover, we demonstrate that the recent demographic history of this species generated regional differences in the load of deleterious mutations among populations, a finding that mirrors recent results from human populations and provides increased support for models of expansion load. We propose that insights from these historical inferences should be better integrated in conservation planning of wild organisms, which currently focuses largely on neutral genetic diversity and local adaptation, with the role of potentially maladaptive variation being generally ignored.

Organochlorine and Metal Contaminants in the Blood Plasma of Green Sturgeon Caught in Washington Coastal Estuaries.

Non-invasive monitoring was used to evaluate the concentrations of 40 contaminants in the blood plasma of the North American Green Sturgeon Acipenser medirostris caught and released from three estuaries in Washington State. The highest contaminant concentrations were found in fish caught in the most urbanized sites. Few statistical differences were found when evaluating contaminant levels according to sex, maturation stage, or distinct population segments of Green Sturgeon. The results indicate that recent exposure to legacy contaminants was reflected in Green Sturgeon plasma. Aldrin, 4,4-DDE, α-HCH, copper, and selenium were the most frequently detected contaminants. This study also explored the challenges of assessing toxicity in threatened species using non-lethal approaches. There is currently a lack of environmental contaminant monitoring data in estuaries frequented by Green Sturgeon and limited plasma to tissue toxicity correlations.

Heterogeneous genetic basis of age at maturity in salmonid fishes.

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications in conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains underexplored. Here, we address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmonids (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait-Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46 × 10-9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

Polygenic Basis and the Role of Genome Duplication in Adaptation to Similar Selective Environments.

Genetic changes underlying adaptation vary greatly in terms of complexity and, within the same species, genetic responses to similar selective pressures may or may not be the same. We examine both complex (supergene) and simple (SNP) genetic variants occurring in populations of rainbow trout (Oncorhynchus mykiss) independently isolated from ocean access and compared them to each other and to an anadromous below-barrier population representing their ancestral source to search for signatures of both parallel and nonparallel adaptation. All landlocked populations displayed an increased frequency of a large inversion on chromosome Omy05, while 3 of the 4 populations exhibited elevated frequencies of another inversion located on chromosome Omy20. In addition, we identified numerous regions outside these 2 inversions that also show significant shifts in allele frequencies consistent with adaptive evolution. However, there was little concordance among above-barrier populations in these specific genomic regions under selection. In part, the lack of concordance appears to arise from ancestral autopolyploidy in rainbow trout that provides duplicate genomic regions of similar functional composition for selection to act upon. Thus, while selection acting on landlocked populations universally favors the resident ecotype, outside of the major chromosomal inversions, the resulting genetic changes are largely distinct among populations. Our results indicate that selection on standing genetic variation is likely the primary mode of rapid adaptation, and that both supergene complexes and individual loci contribute to adaptive evolution, further highlighting the diversity of adaptive genomic variation involved in complex phenotypic evolution.

Dispersal of a nearshore marine fish connects marine reserves and adjacent fished areas along an open coast.

Marine species with pelagic larvae typically exhibit little population structure, suggesting long-distance dispersal and high gene flow. Directly quantifying dispersal of marine fishes is challenging but important, particularly for the design of marine protected areas (MPAs). Here, we studied kelp rockfish (Sebastes atrovirens) sampled along ~25 km of coastline in a boundary current-dominated ecosystem and used genetic parentage analysis to identify dispersal events and characterize them, because the distance between sedentary parents and their settled offspring is the lifetime dispersal distance. Large sample sizes and intensive sampling are critical for increasing the likelihood of detecting parent-offspring matches in such systems and we sampled more than 6,000 kelp rockfish and analysed them with a powerful set of 96 microhaplotype markers. We identified eight parent-offspring pairs with high confidence, including two juvenile fish that were born inside MPAs and dispersed to areas outside MPAs, and four fish born in MPAs that dispersed to nearby MPAs. Additionally, we identified 25 full-sibling pairs, which occurred throughout the sampling area and included all possible combinations of inferred dispersal trajectories. Intriguingly, these included two pairs of young-of-the-year siblings with one member each sampled in consecutive years. These sibling pairs suggest monogamy, either intentional or accidental, which has not been previously demonstrated in rockfishes. This study provides the first direct observation of larval dispersal events in a current-dominated ecosystem and direct evidence that larvae produced within MPAs are exported both to neighbouring MPAs and to proximate areas where harvest is allowed.

Genetic and life-history consequences of extreme climate events.

Climate change is predicted to increase the frequency and intensity of extreme climate events. Tests on empirical data of theory-based predictions on the consequences of extreme climate events are thus necessary to understand the adaptive potential of species and the overarching risks associated with all aspects of climate change. We tested predictions on the genetic and life-history consequences of extreme climate events in two populations of marble trout Salmo marmoratus that have experienced severe demographic bottlenecks due to flash floods. We combined long-term field and genotyping data with pedigree reconstruction in a theory-based framework. Our results show that after flash floods, reproduction occurred at a younger age in one population. In both populations, we found the highest reproductive variance in the first cohort born after the floods due to a combination of fewer parents and higher early survival of offspring. A small number of parents allowed for demographic recovery after the floods, but the genetic bottleneck further reduced genetic diversity in both populations. Our results also elucidate some of the mechanisms responsible for a greater prevalence of faster life histories after the extreme event.

Molecular Population Genetics of the Northern Elephant Seal Mirounga angustirostris.

The northern elephant seal, Mirounga angustirostris, was heavily hunted and declared extinct in the 19th century. However, a colony remained on remote Guadalupe Island, Mexico and the species has since repopulated most of its historical distribution. Here, we present a comprehensive evaluation of genetic variation in the species. First, we assess the effect of the demographic bottleneck on microsatellite variability and compare it with that found in other pinnipeds, demonstrating levels of variation similar to that in species that continue to be threatened with extinction. Next, we use sequence data from these markers to demonstrate that some of the limited polymorphism predates the bottleneck. However, most contemporary variation appears to have arisen recently and persisted due to exponential growth. We also describe how we use the range in allele size of microsatellites to estimate ancestral effective population size before the bottleneck, demonstrating a large reduction in effective size. We then employ a classical method for bacteria to estimate the microsatellite mutation rate in the species, deriving an estimate that is extremely similar to that estimated for a similar set of loci in humans, indicating consistency of microsatellite mutation rates in mammals. Finally, we find slight significant structure between some geographically separated colonies, although its biological significance is unclear. This work demonstrates that genetic analysis can be useful for evaluating the population biology of the northern elephant seal, in spite of the bottleneck that removed most genetic variation from the species.

Shifting Thresholds: Rapid Evolution of Migratory Life Histories in Steelhead/Rainbow Trout, Oncorhynchus mykiss.

Expression of phenotypic plasticity depends on reaction norms adapted to historic selective regimes; anthropogenic changes in these selection regimes necessitate contemporary evolution or declines in productivity and possibly extinction. Adaptation of conditional strategies following a change in the selection regime requires evolution of either the environmentally influenced cue (e.g., size-at-age) or the state (e.g., size threshold) at which an individual switches between alternative tactics. Using a population of steelhead (Oncorhynchus mykiss) introduced above a barrier waterfall in 1910, we evaluate how the conditional strategy to migrate evolves in response to selection against migration. We created 9 families and 917 offspring from 14 parents collected from the above- and below-barrier populations. After 1 year of common garden-rearing above-barrier offspring were 11% smaller and 32% lighter than below-barrier offspring. Using a novel analytical approach, we estimate that the mean size at which above-barrier fish switch between the resident and migrant tactic is 43% larger than below-barrier fish. As a result, above-barrier fish were 26% less likely to express the migratory tactic. Our results demonstrate how rapid and opposing changes in size-at-age and threshold size contribute to the contemporary evolution of a conditional strategy and indicate that migratory barriers may elicit rapid evolution toward the resident life history on timescales relevant for conservation and management of conditionally migratory species.

Panmixia in a Critically Endangered Fish: The Totoaba (Totoaba macdonaldi) in the Gulf of California.

Conservation of the evolutionary legacy of endangered species is a key component for long-term persistence. Totoaba is a long-lived fish endemic to the Gulf of California and is considered critically endangered. There is currently a debate concerning its conservation status and whether it can be used as a fishery resource. Unfortunately, basic information on biological and genetic population structure of the species is lacking. We sampled 313 individuals and employed 16 microsatellite loci and 3 mitochondrial DNA markers (16S, 547 pb; COI, 619 pb; control region, 650 pb) to assess population structure and demography of totoaba in the Gulf of California, with samples from locations that encompass nearly all of its recognized geographic distribution. We could not reject a hypothesis of panmixia for totoaba, using nuclear or mitochondrial markers. Demographic analysis of mtDNA suggests a sudden population expansion model. The results have important implications for totoaba conservation because poaching is a significant conservation challenge and could have additive negative effects over the single population of totoaba in the Gulf of California.

Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout.

Rapid adaptation to novel environments may drive changes in genomic regions through natural selection. Such changes may be population-specific or, alternatively, may involve parallel evolution of the same genomic region in multiple populations, if that region contains genes or co-adapted gene complexes affecting the selected trait(s). Both quantitative and population genetic approaches have identified associations between specific genomic regions and the anadromous (steelhead) and resident (rainbow trout) life-history strategies of Oncorhynchus mykiss. Here, we use genotype data from 95 single nucleotide polymorphisms and show that the distribution of variation in a large region of one chromosome, Omy5, is strongly associated with life-history differentiation in multiple above-barrier populations of rainbow trout and their anadromous steelhead ancestors. The associated loci are in strong linkage disequilibrium, suggesting the presence of a chromosomal inversion or other rearrangement limiting recombination. These results provide the first evidence of a common genomic basis for life-history variation in O. mykiss in a geographically diverse set of populations and extend our knowledge of the heritable basis of rapid adaptation of complex traits in novel habitats.

Genetic parentage reveals the (un)natural history of Central Valley hatchery steelhead.

Populations composed of individuals descended from multiple distinct genetic lineages often feature significant differences in phenotypic frequencies. We considered hatchery production of steelhead, the migratory anadromous form of the salmonid species Oncorhynchus mykiss, and investigated how differences among genetic lineages and environmental variation impacted life history traits. We genotyped 23,670 steelhead returning to the four California Central Valley hatcheries over 9 years from 2011 to 2019, confidently assigning parentage to 13,576 individuals to determine age and date of spawning and rates of iteroparity and repeat spawning within each year. We found steelhead from different genetic lineages showed significant differences in adult life history traits despite inhabiting similar environments. Differences between coastal and Central Valley steelhead lineages contributed to significant differences in age at return, timing of spawning, and rates of iteroparity among programs. In addition, adaptive genomic variation associated with life history development in this species varied among hatchery programs and was associated with the age of steelhead spawners only in the coastal lineage population. Environmental variation likely contributed to variations in phenotypic patterns observed over time, as our study period spanned both a marine heatwave and a serious drought in California. Our results highlight evidence of a strong genetic component underlying known phenotypic differences in life history traits between two steelhead lineages.

Large-scale parentage analysis reveals reproductive patterns and heritability of spawn timing in a hatchery population of steelhead (Oncorhynchus mykiss).

Understanding life history traits is an important first step in formulating effective conservation and management strategies. The use of artificial propagation and supplementation as such a strategy can have numerous effects on the supplemented natural populations and minimizing life history divergence is crucial in minimizing these effects. Here, we use single nucleotide polymorphism (SNP) genotypes for large-scale parentage analysis and pedigree reconstruction in a hatchery population of steelhead, the anadromous form of rainbow trout. Nearly complete sampling of the broodstock for several consecutive years in two hatchery programmes allowed inference about multiple aspects of life history. Reconstruction of cohort age distribution revealed a strong component of fish that spawn at 2 years of age, in contrast to programme goals and distinct from naturally spawning steelhead in the region, which raises a significant conservation concern. The first estimates of variance in family size for steelhead in this region can be used to calculate effective population size and probabilities of inbreeding, and estimation of iteroparity rate indicates that it is reduced by hatchery production. Finally, correlations between family members in the day of spawning revealed for the first time a strongly heritable component to this important life history trait in steelhead and demonstrated the potential for selection to alter life history traits rapidly in response to changes in environmental conditions. Taken together, these results demonstrate the extraordinary promise of SNP-based pedigree reconstruction for providing biological inference in high-fecundity organisms that is not easily achievable with traditional physical tags.

Genetic structure and different color morphotypes suggest the occurrence and bathymetric segregation of two incipient species of Sebastes off Argentina.

Rockfishes of the genus Sebastes are extensively distributed in the Pacific and Atlantic oceans. Although the occurrence of two morphologically similar species in the Southern Hemisphere, Sebastes oculatus and Sebastes capensis, is now clearly established, the taxonomic status and phylogeographic patterns for the genus in the region have not yet been completely resolved. In this study, we provide new insights into the taxonomy and evolutionary relationships of rockfishes inhabiting the Southwestern Atlantic Ocean, off the coast of mainland Argentina, by combining mitochondrial DNA (mtDNA) control region sequences, microsatellite data, and color pattern analyses. Differences in coloration ("dark" and "light" fish) together with bathymetric segregation between color morphotypes were evident from fish collection and literature review. In addition, the mtDNA phylogenetic analysis and Bayesian clustering analysis using microsatellite data separated the fish into two distinct groups (F ST = 0.041), most likely representing incipient species. Our results suggest that speciation-by-depth in the absence of physical barriers could be a widespread mechanism of speciation in Sebastes from both the Northern and Southern Hemispheres. Nevertheless, the degree of genetic differentiation found, added to the large number of individuals displaying high levels of admixture, points to the occurrence of incomplete reproductive barriers between color morphotypes. Beyond the taxonomic and phylogeographic implications of our findings, the occurrence of distinct groups of Sebastes off the coast of Argentina being targeted by different fisheries (angling and trawling) has consequences for the design and implementation of appropriate fishery regulations to avoid overharvest of either group.

Rapid adaptive evolution of the diapause program during range expansion of an invasive mosquito.

In temperate climates, the recurring seasonal exigencies of winter represent a fundamental physiological challenge for a wide range of organisms. In response, many temperate insects enter diapause, an alternative developmental program, including developmental arrest, that allows organisms to synchronize their life cycle with seasonal environmental variation. Geographic variation in diapause phenology contributing to local climatic adaptation is well documented. However, few studies have examined how the rapid evolution of a suite of traits expressed across the diapause program may contribute to climatic adaptation on a contemporary timescale. Here, we investigate the evolution of the diapause program over the past 35 years by leveraging a "natural experiment" presented by the recent invasion of the Asian tiger mosquito, Aedes albopictus, across the eastern United States. We sampled populations from two distinct climatic regions separated by 6° of latitude (∼700 km). Using common-garden experiments, we identified regional genetic divergence in diapause-associated cold tolerance, diapause duration, and postdiapause starvation tolerance. We also found regional divergence in nondiapause thermal performance. In contrast, we observed minimal regional divergence in nondiapause larval growth traits and at neutral molecular marker loci. Our results demonstrate rapid evolution of the diapause program and imply strong selection caused by differences in winter conditions.

A complex phenotype in salmon controlled by a simple change in migratory timing.

Differentiation between ecotypes is usually presumed to be complex and polygenic. Seasonal patterns of life history in salmon are used to categorize them into ecotypes, which are often considered "distinct" animals. Using whole-genome sequencing and tribal fishery sampling of Chinook salmon, we show that a single, small genomic region is nearly perfectly associated with spawning migration timing but not with adiposity or sexual maturity, traits long perceived as central to salmon ecotypes. Distinct migration timing does not prevent interbreeding between ecotypes, which are the result of a simple, ancient polymorphism segregating within a diverse population. Our finding that a complex migratory phenotype results from a single gene region will facilitate conservation and restoration of this iconic fish.

Publisher Correction: Sex-dependent dominance maintains migration supergene in rainbow trout.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.