Watershed‐level brook trout genetic structuring: Evaluation and application of riverscape genetics models

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Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream‐resident (fluvial), lake‐migrant (adfluvial) and ocean‐migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site‐associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.     

The influence of breeding phenology on the genetic structure of four pond‐breeding salamanders

Understanding metapopulation dynamics requires knowledge about local population dynamics and movement in both space and time. Most genetic metapopulation studies use one or two study species across the same landscape to infer population dynamics; however, using multiple co‐occurring species allows for testing of hypotheses related to different life history strategies. We used genetic data to study dispersal, as measured by gene flow, in three ambystomatid salamanders (Ambystoma annulatum , A. maculatum , and A. opacum ) and the Central Newt (Notophthalmus viridescens louisianensis ) on the same landscape in Missouri, USA . While all four salamander species are forest dependent organisms that require fishless ponds to reproduce, they differ in breeding phenology and spatial distribution on the landscape. We use these differences in life history and distribution to address the following questions: (1) Are there species‐level differences in the observed patterns of genetic diversity and genetic structure? and (2) Is dispersal influenced by landscape resistance? We detected two genetic clusters in A. annulatum and A. opacum on our landscape; both species breed in the fall and larvae overwinter in ponds. In contrast, no structure was evident in A. maculatum and N. v. louisianensis , species that breed during the spring. Tests for isolation by distance were significant for the three ambystomatids but not for N. v. louisianensis . Landscape resistance also contributed to genetic differentiation for all four species. Our results suggest species‐level differences in dispersal ability and breeding phenology are driving observed patterns of genetic differentiation. From an evolutionary standpoint, the observed differences in dispersal distances and genetic structure between fall breeding and spring breeding species may be a result of the trade‐off between larval period length and size at metamorphosis which in turn may influence the long‐term viability of the metapopulation. Thus, it is important to consider life history differences among closely related and ecologically similar species when making management decisions.     

Local habitat conditions explain the variation in the strength of self‐thinning in a stream salmonid

Self-thinning patterns are frequently used to describe density dependence in populations on timescales shorter than the organism''s life span and have been used to infer carrying capacity of the environment. Among mobile animals, this concept has been used to document density dependence in stream salmonids, which compete over access to food and space. The carrying capacity, growth conditions, and initial cohort sizes often vary between streams and stream sections, which would influence the onset and strength of the density dependence. Despite much effort in describing habitat relationships in stream fishes, few studies have explicitly tested how the physical environment affects the slope of the thinning curves. Here, we investigate the prevalence and strength of self-thinning in juvenile stages of a steelhead (Oncorhynchus mykiss) population in Idaho, USA. Further, we investigate the roles of local physical habitat and metabolic constraints in explaining the variation in thinning curves among study sites in the watershed. Only yearling steelhead exhibited an overall significant thinning trend, but the slope of the mass–density relationship (−0.53) was shallower than predicted by theory and reported from empirical studies. There was no detectable relationship in subyearling steelhead. Certain abiotic factors explained a relatively large portion of the variation in the strength of the self-thinning among the study reaches. For subyearling steelhead, the slopes were negatively associated with the average water depth and flow velocity in the study sites, whereas slopes in yearlings were steeper in sites that incurred a higher metabolic cost. Our results show that the prevalence and strength of density dependence in natural fish populations can vary across heterogeneous watersheds and can be more pronounced during certain stages of a species'' life history, and that environmental factors can mediate the extent to which density dependence is manifested in predictable ways.     

Climate‐associated genetic variation in Fagus sylvatica and potential responses to climate change in the French Alps

Local adaptation patterns have been found in many plants and animals, highlighting the genetic heterogeneity of species along their range of distribution. In the next decades, global warming is predicted to induce a change in the selective pressures that drive this adaptive variation, forcing a reshuffling of the underlying adaptive allele distributions. For species with low dispersion capacity and long generation time such as trees, the rapidity of the change could impede the migration of beneficial alleles and lower their capacity to track the changing environment. Identifying the main selective pressures driving the adaptive genetic variation is thus necessary when investigating species capacity to respond to global warming. In this study, we investigate the adaptive landscape of Fagus sylvatica along a gradient of populations in the French Alps. Using a double‐digest restriction‐site‐associated DNA (ddRAD) sequencing approach, we identified 7,000 SNPs from 570 individuals across 36 different sites. A redundancy analysis (RDA)‐derived method allowed us to identify several SNPs that were strongly associated with climatic gradients; moreover, we defined the primary selective gradients along the natural populations of F. sylvatica in the Alps. Strong effects of elevation and humidity, which contrast north‐western and south‐eastern site, were found and were believed to be important drivers of genetic adaptation. Finally, simulations of future genetic landscapes that used these findings allowed identifying populations at risk for F. sylvatica in the Alps, which could be helpful for future management plans.     

Node‐based measures of connectivity in genetic networks

At‐site environmental conditions can have strong influences on genetic connectivity, and in particular on the immigration and settlement phases of dispersal. However, at‐site processes are rarely explored in landscape genetic analyses. Networks can facilitate the study of at‐site processes, where network nodes are used to model site‐level effects. We used simulated genetic networks to compare and contrast the performance of 7 node‐based (as opposed to edge‐based) genetic connectivity metrics. We simulated increasing node connectivity by varying migration in two ways: we increased the number of migrants moving between a focal node and a set number of recipient nodes, and we increased the number of recipient nodes receiving a set number of migrants. We found that two metrics in particular, the average edge weight and the average inverse edge weight, varied linearly with simulated connectivity. Conversely, node degree was not a good measure of connectivity. We demonstrated the use of average inverse edge weight to describe the influence of at‐site habitat characteristics on genetic connectivity of 653 American martens (Martes americana) in Ontario, Canada. We found that highly connected nodes had high habitat quality for marten (deep snow and high proportions of coniferous and mature forest) and were farther from the range edge. We recommend the use of node‐based genetic connectivity metrics, in particular, average edge weight or average inverse edge weight, to model the influences of at‐site habitat conditions on the immigration and settlement phases of dispersal.     

Distribution of genetic variation underlying adult migration timing in steelhead of the Columbia River basin

Fish migrations are energetically costly, especially when moving between freshwater and saltwater, but are a viable strategy for Pacific salmon and trout (Oncorhynchus spp.) due to the advantageous resources available at various life stages. Anadromous steelhead (O. mykiss) migrate vast distances and exhibit variation for adult migration phenotypes that have a genetic basis at candidate genes known as greb1L and rock1. We examined the distribution of genetic variation at 13 candidate markers spanning greb1L, intergenic, and rock1 regions versus 226 neutral markers for 113 populations (n = 9,471) of steelhead from inland and coastal lineages in the Columbia River. Patterns of population structure with neutral markers reflected genetic similarity by geographic region as demonstrated in previous studies, but candidate markers clustered populations by genetic variation associated with adult migration timing. Mature alleles for late migration had the highest frequency overall in steelhead populations throughout the Columbia River, with only 9 of 113 populations that had a higher frequency of premature alleles for early migration. While a single haplotype block was evident for the coastal lineage, we identified multiple haplotype blocks for the inland lineage. The inland lineage had one haplotype block that corresponded to candidate markers within the greb1L gene and immediately upstream in the intergenic region, and the second block only contained candidate markers from the intergenic region. Haplotype frequencies had similar patterns of geographic distribution as single markers, but there were distinct differences in frequency between the two haplotype blocks for the inland lineage. This may represent multiple recombination events that differed between lineages where phenotypic differences exist between freshwater entry versus arrival timing as indicated by Micheletti et al. (2018a). Redundancy analyses were used to model environmental effects on allelic frequencies of candidate markers, and significant variables were migration distance, temperature, isothermality, and annual precipitation. This study improves our understanding of the spatial distribution of genetic variation underlying adult migration timing in steelhead as well as associated environmental factors and has direct conservation and management implications.     

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.     

Genomic heritability estimation for the early life‐history transition related to propensity to migrate in wild rainbow and steelhead trout populations

A previous genomewide association study (GWAS) identified SNP markers associated with propensity to migrate of rainbow and steelhead trout (Oncorhynchus mykiss) in a connected population with free access to the ocean in Upper Yakima River (UYR) and a population in Upper Mann Creek (UMC) that has been sequestered from its access to the ocean for more than 50 years. Applying genomic heritability estimation using the same dataset, we found that smoltification in the UYR population were almost completely determined by additive effects, with 95.5% additive heritability and 4.5% dominance heritability, whereas smoltification in the UMC population had substantial dominance effects, with 0% additive heritability and 39.3% dominance heritability. Dominance test detected one SNP marker ({"type":"entrez-nucleotide","attrs":{"text":"R30393","term_id":"937054","term_text":"R30393"}}R30393) with significant dominance effect on smoltification (P = 1.98 × 10⁻⁷). Genomic-predicted additive effects completely separated migratory and nonmigratory fish in the UYR population, whereas genomic-predicted dominance effects achieved such complete separation in the UMC population. The UMC population had higher genomic additive and dominance correlations than the UYR population, and fish between these two populations had the least genomic correlations. These results suggested that blocking the free access to the ocean may have reduced genetic diversity and increased genomic similarity associated with the early life-history transition related to propensity to migrate.     

Dealing with uncertainty in landscape genetic resistance models: a case of three co‐occurring marsupials

Landscape genetics lacks explicit methods for dealing with the uncertainty in landscape resistance estimation, which is particularly problematic when sample sizes of individuals are small. Unless uncertainty can be quantified, valuable but small data sets may be rendered unusable for conservation purposes. We offer a method to quantify uncertainty in landscape resistance estimates using multimodel inference as an improvement over single model‐based inference. We illustrate the approach empirically using co‐occurring, woodland‐preferring Australian marsupials within a common study area: two arboreal gliders (Petaurus breviceps, and Petaurus norfolcensis) and one ground‐dwelling antechinus (Antechinus flavipes). First, we use maximum‐likelihood and a bootstrap procedure to identify the best‐supported isolation‐by‐resistance model out of 56 models defined by linear and non‐linear resistance functions. We then quantify uncertainty in resistance estimates by examining parameter selection probabilities from the bootstrapped data. The selection probabilities provide estimates of uncertainty in the parameters that drive the relationships between landscape features and resistance. We then validate our method for quantifying uncertainty using simulated genetic and landscape data showing that for most parameter combinations it provides sensible estimates of uncertainty. We conclude that small data sets can be informative in landscape genetic analyses provided uncertainty can be explicitly quantified. Being explicit about uncertainty in landscape genetic models will make results more interpretable and useful for conservation decision‐making, where dealing with uncertainty is critical.     

Relationship between effective population size,inbreeding and adult fitness‐related traits in a steelhead (Oncorhynchus mykiss) population released in the wild

Inbreeding is of concern in supportive breeding programmes in Pacific salmonids, Oncorhynchus spp, where the number of breeding adults is limited by rearing space or poor survival to adulthood, and large numbers are released to supplement wild stocks and fisheries. We reconstructed the pedigree of 6602 migratory hatchery steelhead (Oncorhynchus mykiss) over four generations, to determine the incidence and fitness consequences of inbreeding in a northwest USA programme. The hatchery maintained an effective population size,  = 107.9 from F₀ to F₂, despite an increasing census size (N), which resulted in a decreasing N_e/N ratio (0.35 in F₀ to 0.08 in F₂). The reduced ratio was attributed to a small broodstock size, nonrandom transfers and high variance in reproductive success (particularly in males). We observed accumulation of inbreeding from the founder generation (in F₄, percentage individuals with inbreeding coefficients Δf > 0 = 15.7%). Generalized linear mixed models showed that body length and weight decreased significantly with increasing Δf, and inbred fish returned later to spawn in a model that included father identity. However, there was no significant correlation between Δf and age at return, female fecundity or gonad weight. Similarly, there was no relationship between Δf and reproductive success of F₂ and F₃ individuals, which might be explained by the fact that reproductive success is partially controlled by hatchery mating protocols. This study is one of the first to show that small changes in inbreeding coefficient can affect some fitness‐related traits in a monitored population propagated and released to the wild.     

Contrasting population genetic structure among freshwater‐resident and anadromous lampreys: the role of demographic history,differential dispersal and anthropogenic barriers to movement

The tendency of many species to abandon migration remains a poorly understood aspect of evolutionary biology that may play an important role in promoting species radiation by both allopatric and sympatric mechanisms. Anadromy inherently offers an opportunity for the colonization of freshwater environments, and the shift from an anadromous to a wholly freshwater life history has occurred in many families of fishes. Freshwater‐resident forms have arisen repeatedly among lampreys (within the Petromyzontidae and Mordaciidae), and there has been much debate as to whether anadromous lampreys, and their derived freshwater‐resident analogues, constitute distinct species or are divergent ecotypes of polymorphic species. Samples of 543 European river lamprey Lampetra fluviatilis (mostly from anadromous populations) and freshwater European brook lamprey Lampetra planeri from across 18 sites, primarily in the British Isles, were investigated for 13 polymorphic microsatellite DNA loci, and 108 samples from six of these sites were sequenced for 829 bp of mitochondrial DNA (mtDNA). We found contrasting patterns of population structure for mtDNA and microsatellite DNA markers, such that low diversity and little structure were seen for all populations for mtDNA (consistent with a recent founder expansion event), while fine‐scale structuring was evident for nuclear markers. Strong differentiation for microsatellite DNA loci was seen among freshwater‐resident L. planeri populations and between L. fluviatilis and L. planeri in most cases, but little structure was evident among anadromous L. fluviatilis populations. We conclude that postglacial colonization founded multiple freshwater‐resident populations with strong habitat fidelity and limited dispersal tendencies that became highly differentiated, a pattern that was likely intensified by anthropogenic barriers.     

Arms race co‐evolution of Magnaporthe oryzae AVR‐Pik and rice Pik genes driven by their physical interactions

Attack and counter‐attack impose strong reciprocal selection on pathogens and hosts, leading to development of arms race evolutionary dynamics. Here we show that Magnaporthe oryzae avirulence gene AVR‐Pik and the cognate rice resistance (R) gene Pik are highly variable, with multiple alleles in which DNA replacements cause amino acid changes. There is tight recognition specificity of the AVR‐Pik alleles by the various Pik alleles. We found that AVR‐Pik physically binds the N‐terminal coiled‐coil domain of Pik in a yeast two‐hybrid assay as well as in an in planta co‐immunoprecipitation assay. This binding specificity correlates with the recognition specificity between AVR and R genes. We propose that AVR‐Pik and Pik are locked into arms race co‐evolution driven by their direct physical interactions.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

Optimizing the trade‐off between spatial and genetic sampling efforts in patchy populations: towards a better assessment of functional connectivity using an individual‐based sampling scheme

Genetic data are increasingly used in landscape ecology for the indirect assessment of functional connectivity, that is, the permeability of landscape to movements of organisms. Among available tools, matrix correlation analyses (e.g. Mantel tests or mixed models) are commonly used to test for the relationship between pairwise genetic distances and movement costs incurred by dispersing individuals. When organisms are spatially clustered, a population‐based sampling scheme (PSS) is usually performed, so that a large number of genotypes can be used to compute pairwise genetic distances on the basis of allelic frequencies. Because of financial constraints, this kind of sampling scheme implies a drastic reduction in the number of sampled aggregates, thereby reducing sampling coverage at the landscape level. We used matrix correlation analyses on simulated and empirical genetic data sets to investigate the efficiency of an individual‐based sampling scheme (ISS) in detecting isolation‐by‐distance and isolation‐by‐barrier patterns. Provided that pseudo‐replication issues are taken into account (e.g. through restricted permutations in Mantel tests), we showed that the use of interindividual measures of genotypic dissimilarity may efficiently replace interpopulation measures of genetic differentiation: the sampling of only three or four individuals per aggregate may be sufficient to efficiently detect specific genetic patterns in most situations. The ISS proved to be a promising methodological alternative to the more conventional PSS, offering much flexibility in the spatial design of sampling schemes and ensuring an optimal representativeness of landscape heterogeneity in data, with few aggregates left unsampled. Each strategy offering specific advantages, a combined use of both sampling schemes is discussed.