Consistent loss of genetic diversity in isolated cutthroat trout populations independent of habitat size and quality

Fragmentation and isolation of wildlife populations has reduced genetic diversity worldwide, leaving many populations vulnerable to inbreeding depression and local extinction. Nonetheless, isolation is protecting many native aquatic species from interactions with invasive species, often making reconnection an unrealistic conservation strategy. Isolation management is widely used to protect extant cutthroat trout (Oncorhynchus clarkii) populations from invasive species. Despite this, few studies have empirically examined how predictor variables including habitat length, population size, time since isolation and habitat quality, relate to levels of genetic diversity in isolated trout populations. We compared allelic richness of cutthroat trout across 14 microsatellite loci in two connected and 12 anthropogenically isolated populations of the Flathead River basin, Montana. Isolated populations in habitat fragments <8 km stream length had reduced genetic diversity, but diversity was not significantly related to any of our predictor variables. To broaden our scope, we analyzed seven geologically isolated populations from the same river basin occupying habitat fragments up to 18 km in length. These populations showed reduced diversity, regardless of fragment size. Furthermore, geologically isolated populations had significantly lower average allelic richness compared to streams recently isolated by anthropogenic activities. These results demonstrate a consistent loss of genetic diversity through time in isolated populations, emphasizing the need to explore strategies to minimize risks of inbreeding depression. Testing conservation theory and subsequent assumptions broadly across taxa is necessary to ensure efficacy of conservation efforts.     

Genetic variation in westslope cutthroat trout <Emphasis Type="Italic">Oncorhynchus clarkii lewisi</Emphasis>: implications for conservation

Twenty-five populations of westslope cutthroat trout from throughout their native range were genotyped at 20 microsatellite loci to describe the genetic structure of westslope cutthroat trout. The most genetic diversity (heterozygosity, allelic richness, and private alleles) existed in populations from the Snake River drainage, while populations from the Missouri River drainage had the least. Neighbor-joining trees grouped populations according to major river drainages. A great amount of genetic differentiation was present among and within all drainages. Based on Nei’s D _S , populations in the Snake River were the most differentiated, while populations in the Missouri River were the least. This pattern of differentiation is consistent with a history of sequential founding events through which westslope cutthroat trout may have experienced a genetic bottleneck as they colonized each river basin from the Snake to the Clark Fork to the Missouri river. These data should serve as a starting point for a discussion on management units and possible distinct population segments. Given the current threats to the persistence of westslope cutthroat trout, and the substantial genetic differentiation between populations, these topics warrant attention.     

A molecular analysis of hybridization between native westslope cutthroat trout and introduced rainbow trout in southeastern British Columbia, Canada

Restriction site variation in the Ikaros gene intron was used to assess the incidence of westslope cutthroat trout ( Oncorhynchus clarki lewisi ), rainbow trout ( O. mykiss ) and interspecific hybrids at 11 localities among eight streams tributary to the upper Kootenay River system in south-eastern British Columbia, Canada. Out of 356 fish assayed by this technique, hybrids ( n =16) were found at seven of the 11 sites across five different streams. Rainbow trout ( n =6) were found at two of the 11 sites. Analysis of hybrids with a second genetic marker (heat shock 71 intron) indicated that most represented either backcrosses to both westslope cutthroat and rainbow trout, or post F₁ hybrids. Mitochondrial DNA analysis indicated that hybrid matings occur between male rainbow trout and female westslope cutthroat trout and vice versa. Comparison of present hybridization in five tributaries relative to an allozyme-based analysis in the mid-1980s, that documented hybrids in only a single tributary of seven that were common to the two studies, suggests that hybridization and introgression has increased in upper Kootenay River tributaries. The present analysis is a conservative estimate of genetic interaction between the species because introgression was not tested in the majority of samples. Identification of genetically pure westslope cutthroat trout populations, and why they might be resistant to introgression from rainbow trout, are crucial conservation priorities for this unique subspecies of cutthroat trout.     

Genetic Integrity and Microgeographic Population Structure of Westslope Cutthroat Trout, Oncorhynchus clarki lewisi, in the Pend Oreille Basin in Washington

Five microsatellite DNA loci (Ots-101 ^*,Ots-107 ^*,Oki-10 ^*, Ogo-3 ^*, and FGT-3 ^*) were screened to evaluate the genetic characteristics and population structure for cutthroat trout from eight tributaries of the Pend Oreille River in northeastern Washington and to compare these collections with two hatchery stocks of westslope cutthroat trout, Oncorhynchus clarki lewisi, Yellowstone cutthroat trout, Oncorhynchus clarki bouvieri and a hatchery rainbow trout, Oncorhynchus mykiss, strain that have been stocked in northeastern Washington. Relatively high levels of variation (numbers of alleles and heterozygosity) were observed in all collections and allele frequencies were quite variable among collections. Evidence of limited introgression by rainbow and/or Yellowstone cutthroat was found at several locations. Both F_ST values and tests of genetic differentiation indicated the existence of numerous, reproductively isolated populations. The population in Slate Creek was very similar to the Kings Lake Hatchery strain, and we conclude that this similarity is the result of historical introductions of this hatchery strain into what was presumably a stream without a native cutthroat population. In one stream, differences in introgression and allele frequencies were found above and below a barrier falls. Because of the substantial level of population differentiation observed among the various collections, we recommend that management and conservation actions be focused at the level of individual streams in order to maintain the productivity and genetic character of the existing populations of cutthroat trout.     

Population structure and gene flow in the Sheepnose mussel (Plethobasus cyphyus) and their implications for conservation

North American freshwater mussel species have experienced substantial range fragmentation and population reductions. These impacts have the potential to reduce genetic connectivity among populations and increase the risk of losing genetic diversity. Thirteen microsatellite loci and an 883 bp fragment of the mitochondrial ND1 gene were used to assess genetic diversity, population structure, contemporary migration rates, and population size changes across the range of the Sheepnose mussel (Plethobasus cyphyus). Population structure analyses reveal five populations, three in the Upper Mississippi River Basin and two in the Ohio River Basin. Sampling locations exhibit a high degree of genetic diversity and contemporary migration estimates indicate that migration within river basins is occurring, although at low rates, but there is no migration is occurring between the Ohio and Mississippi river basins. No evidence of bottlenecks was detected, and almost all locations exhibited the signature of population expansion. Our results indicate that although anthropogenic activity has altered the landscape across the range of the Sheepnose, these activities have yet to be reflected in losses of genetic diversity. Efforts to conserve Sheepnose populations should focus on maintaining existing habitats and fostering genetic connectivity between extant demes to conserve remaining genetic diversity for future viable populations.     

Patterns of hybridization among cutthroat trout and rainbow trout in northern Rocky Mountain streams

Introgressive hybridization between native and introduced species is a growing conservation concern. For native cutthroat trout and introduced rainbow trout in western North America, this process is thought to lead to the formation of hybrid swarms and the loss of monophyletic evolutionary lineages. Previous studies of this phenomenon, however, indicated that hybrid swarms were rare except when native and introduced forms of cutthroat trout co‐occurred. We used a panel of 86 diagnostic, single nucleotide polymorphisms to evaluate the genetic composition of 3865 fish captured in 188 locations on 129 streams distributed across western Montana and northern Idaho. Although introgression was common and only 37% of the sites were occupied solely by parental westslope cutthroat trout, levels of hybridization were generally low. Of the 188 sites sampled, 73% contained ≤5% rainbow trout alleles and 58% had ≤1% rainbow trout alleles. Overall, 72% of specimens were nonadmixed westslope cutthroat trout, and an additional 3.5% were nonadmixed rainbow trout. Samples from seven sites met our criteria for hybrid swarms, that is, an absence of nonadmixed individuals and a random distribution of alleles within the sample; most (6/7) were associated with introgression by Yellowstone cutthroat trout. In streams with multiple sites, upstream locations exhibited less introgression than downstream locations. We conclude that although the widespread introduction of nonnative trout within the historical range of westslope cutthroat trout has increased the incidence of introgression, sites containing nonadmixed populations of this taxon are common and broadly distributed.     

Population genetics of steelhead (<Emphasis Type="Italic">Oncorhynchus mykiss</Emphasis>) in the Klamath River

An analysis of population structure and genetic diversity was conducted on samples of Oncorhynchus mykiss (steelhead/rainbow trout) from 33 sites in the Klamath–Trinity River basin. Genotype data from 16 microsatellite loci in almost 1,700 fish revealed genetic differentiation between most sampled locations. Two pairs of samples from the same sites in different years were not significantly different, indicating stability of population structure, at least on a short time scale. Most sampling sites were genetically distinct from all other sampling sites, and there was an evidence of geographic structure within the Klamath–Trinity River basin, although populations from tributaries within the watershed (e.g. Salmon River, Scott River, Clear Creek) did not always constitute distinct genetic lineages. Population structure was evident using phylogeographic trees, isolation by distance analyses and individual assignment tests, which all found a relationship between geographic and genetic distance. Populations in the lower Klamath region, below the confluence with the Trinity River, consistently clustered together in phylogeographic analyses and had patterns of genetic diversity that suggest reduced gene flow between these sites and sites above the confluence. Finally, in an analysis that included data from other coastal California rivers, the populations closest to the mouth of the Klamath River appeared intermediate between populations from adjacent watersheds and the lineage formed by the other populations in the Klamath–Trinity basin.     

Population subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications

Westslope cutthroat trout (Oncorhynchus clarki lewisi, Salmonidae) are native to the upper Columbia, Missouri, and South Saskatchewan river drainages of western North America and are at the northern periphery of their range in southeastern British Columbia, Canada. We examined geographical variation in allele frequencies at eight microsatellite loci in 36 samples of westslope cutthroat trout from British Columbia to assess levels of population subdivision and to test the hypothesis that different habitat types (principally mainstem vs. above migration barrier habitats) would influence levels of genetic diversity, genetic divergence among populations, and attainment of equilibrium between gene flow and genetic drift. Across all samples, the mean number of alleles per locus was 3.9 and mean expected heterozygosity was 0.56. Population subdivision was extensive with an overall Fst (theta) of 0.32. Populations sampled above migration barriers had significantly fewer alleles, lower expected heterozygosity, but greater average pairwise Fst than populations sampled from mainstem localities. We found evidence for isolation-by-distance from a significant correlation between genetic distance and geographical distance (r = 0.31), but the pattern was much stronger (r = 0.51) when above barrier populations and a population that may have been involved in headwater exchanges were removed. By contrast, isolation-by-distance was not observed when only above barrier populations were tested among themselves. Our data support the maintenance of separate demographic management strategies for westslope cutthroat trout inhabiting different river systems and illustrate how differing habitat structure (e.g. presence of migration barriers) may influence patterns of biodiversity and gene flow-drift equilibrium.     

Hybridization dynamics between Colorado's native cutthroat trout and introduced rainbow trout

Newly formed hybrid populations provide an opportunity to examine the initial consequences of secondary contact between species and identify genetic patterns that may be important early in the evolution of hybrid inviability. Widespread introductions of rainbow trout (Oncorhynchus mykiss) into watersheds with native cutthroat trout (Oncorhynchus clarkii) have resulted in hybridization. These introductions have contributed to the decline of native cutthroat trout populations. Here, we examine the pattern of hybridization between introduced rainbow trout and 2 populations of cutthroat trout native to Colorado. For this study, we utilized 7 diagnostic, codominant nuclear markers and a diagnostic mitochondrial marker to investigate hybridization in a population of greenback cutthroat trout (Oncorhynchus clarkii stomias) and a population of Colorado River cutthroat trout (Oncorhynchus clarkii pleuriticus). We infer that cutthroat-rainbow trout hybrid swarms have formed in both populations. Although a mixture of hybrid genotypes was present, not all genotype combinations were detected at expected frequencies. We found evidence that mitochondrial DNA introgression in hybrids is asymmetric and more likely from rainbow trout than from cutthroat trout. A difference in spawning time of the 2 species or differences in the fitness between the reciprocal crosses may explain the asymmetry. Additionally, the presence of intraspecific cytonuclear associations found in both populations is concordant with current hypotheses regarding coevolution of mitochondrial and nuclear genomes.     

Characterising genetic diversity and effective population size in one reservoir and two riverine populations of the threatened Macquarie perch

Nine polymorphic microsatellite loci have been used to infer population genetic diversity and structure of the threatened Australian freshwater fish, Macquarie perch, across three tributaries of the Murrumbidgee River in south-eastern Australia. This investigation has revealed a high level of divergence among all three populations, along with contrasting patterns of genetic diversity. The Cotter Reservoir, which is a stronghold population for the species, has typically higher diversity and effective population size than nearby riverine populations. This suggests that the reservoir population is unlikely to have undergone a genetic bottleneck during and following dam construction. Genetic diversity estimates were comparable with one riverine site but were significantly higher than a population sampled from the Queanbeyan River. This comparison revealed significantly less heterozygotes in the Queanbeyan River and lower estimates of effective population size. Options and considerations for stock replenishment of this population are discussed.     

Microsatellite analysis of genetic population structure in an endangered salmonid: the coastal cutthroat trout (Oncorhynchus clarki clarki)

The genetic population structure of coastal cutthroat trout ( Oncorhynchus clarki clarki ) in Washington state was investigated by analysis of variation in allele frequencies at six highly polymorphic microsatellite loci for 13 anadromous populations, along with one outgroup population from the Yellowstone subspecies ( O. clarki bouvieri) (mean heterozygosity = 67%; average number of alleles per locus = 24). Tests for genetic differentiation revealed highly significant differences in genotypic frequencies for pairwise comparisons between all populations within geographical regions and overall population subdivision was substantial ( F _ST = 0.121, R _ST = 0.093), with 44.6% and 55.4% of the among-population diversity being attributable to differences between streams ( F _SR = 0.054) and between regions ( F _RT = 0.067), respectively. Analysis of genetic distances and geographical distances did not support a simple model of isolation by distance for these populations. With one exception, neighbour-joining dendrograms from the Cavalli-Sforza and Edwards' chord distances and maximum likelihood algorithms clustered populations by physiogeographic region, although overall bootstrap support was relatively low (53%). Our results suggest that coastal cutthroat trout populations are ultimately structured genetically at the level of individual streams. It appears that the dynamic balance between gene flow and genetic drift in the subspecies favours a high degree of genetic differentiation and population subdivision with the simultaneous maintenance of high heterozygosity levels within local populations. Results are discussed in terms of coastal cutthroat trout ecology along with implications for the designation of evolutionarily significant units pursuant to the US Endangered Species Act of 1973 and analogous conservation units.     

Spatial extent of analysis influences observed patterns of population genetic structure in a widespread darter species (Percidae)

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Genetic structure in urban and rural populations of Apodemus agrarius in Poland

The aims of this study were (i) to determine the genetic variability of the striped field mouse (Apodemus agrarius Pallas, 1771) population in the area of the Warsaw conurbation and the genetic differentiation among local populations of this species within the city, and (ii) to examine the influence of the degree of isolation on the appearance of such genetic structure. Comparison of the genetic structure of the urban population with that of populations inhabiting rural areas was intended to shed light on the depth of genetic changes in this species caused by life in an urban environment. Eight microsatellite loci were used for genotyping and these molecular analyses were successfully performed for 269 individuals. Genetic differentiation (F_ST) was much higher in the case of the urban population. STRUCTURE analysis indicated that this population was subdivided into several local populations, whereas for the rural locations, the highest likelihood was for a single genetic group (one genetically unstructured population). Moreover, in contrast to the rural population, we found no isolation by distance in the urban population. Despite clear subdivision of the urban population, the level of genetic variability was very similar in both analyzed groups. Our findings indicate the occurrence of an advanced process of differentiation of the urban population by microevolution, whereas populations from rural locations displayed very small and mainly insignificant genetic differentiation. Urban local populations, situated near the city borders or close to the natural ecological corridor (banks of the Vistula River), showed higher genetic variability and were less differentiated from populations inhabiting rural sites than from local populations in the city centre. These results provide support for the importance of ecological corridors in preserving the genetic variability of the urban striped field mouse population.     

A genetically distinct wild redband trout (<Emphasis Type="Italic">Oncorhynchus mykiss gairdneri</Emphasis>) population in Crane Prairie Reservoir,Oregon, persists despite extensive stocking of hatchery rainbow trout (<Emphasis Type="Italic">O. m. irideus</Emphasis>)

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.     

Summer and fall microhabitat utilization of juvenile bull trout and cutthroat trout in a wilderness stream, Idaho

Microhabitat use and availability were evaluated and compared between different size classes of juvenile resident bull trout (Salvelinus confluentus) and cutthroat trout (Oncorhynchus clarki) in a small wilderness stream within the South Fork Clearwater River basin, Idaho. The objective was to determine if utilization of measured habitat characteristics changed from summer to late fall. Sampling of fish was conducted with night snorkeling. During the summer, smaller juvenile bull trout (<66 mm) total length (TL) were associated with shallow stream margins over coarse substrates. In the fall, they moved to significantly deeper, lower velocity water, and closer to cover (p<0.05), but maintained their association with coarse substrates. During the summer, larger juvenile bull trout and larger juvenile cutthroat trout (66–130 mm TL) occupied significantly deeper water than smaller juvenile bull trout (p<0.05). Generally, larger juvenile bull trout were found closer to the bottom and in lower velocity water than larger juvenile cutthroat trout (p<0.05). In the fall, larger juvenile bull trout and larger juvenile cutthroat trout were associated with significantly deeper, lower velocity water located closer to cover than in summer (p<0.05). However, cutthroat trout occupied slightly deeper water over finer substrates than bull trout. Deep water with low velocities evidently provide important rearing areas for large bull trout and large cutthroat trout in the fall. Land management practices that maintain such environments will benefit these species.     

Modelling competition and hybridization between native cutthroat trout and nonnative rainbow and hybrid trout

Native salmonid fish have been displaced worldwide by nonnatives through hybridization, competition, and predation, but the dynamics of these factors are poorly understood. We apply stochastic Lotka-Volterra models to the displacement of cutthroat trout by rainbow/hybrid trout in the Snake River, Idaho, USA. Cutthroat trout are susceptible to hybridization in the river but are reproductively isolated in tributaries via removal of migratory rainbow/hybrid spawners at weirs. Based on information-theoretic analysis, population data provide evidence that hybridization was the primary mechanism for cutthroat trout displacement in the first 17 years of the invasion. However, under some parameter values, the data provide evidence for a model in which interaction occurs among fish from both river and tributary subpopulations. This situation is likely to occur when tributary-spawned cutthroat trout out-migrate to the river as fry. The resulting competition with rainbow/hybrid trout can result in the extinction of cutthroat trout even when reproductive segregation is maintained.     

Genetic diversity is related to climatic variation and vulnerability in threatened bull trout

Understanding how climatic variation influences ecological and evolutionary processes is crucial for informed conservation decision‐making. Nevertheless, few studies have measured how climatic variation influences genetic diversity within populations or how genetic diversity is distributed across space relative to future climatic stress. Here, we tested whether patterns of genetic diversity (allelic richness) were related to climatic variation and habitat features in 130 bull trout (Salvelinus confluentus) populations from 24 watersheds (i.e., ~4–7th order river subbasins) across the Columbia River Basin, USA. We then determined whether bull trout genetic diversity was related to climate vulnerability at the watershed scale, which we quantified on the basis of exposure to future climatic conditions (projected scenarios for the 2040s) and existing habitat complexity. We found a strong gradient in genetic diversity in bull trout populations across the Columbia River Basin, where populations located in the most upstream headwater areas had the greatest genetic diversity. After accounting for spatial patterns with linear mixed models, allelic richness in bull trout populations was positively related to habitat patch size and complexity, and negatively related to maximum summer temperature and the frequency of winter flooding. These relationships strongly suggest that climatic variation influences evolutionary processes in this threatened species and that genetic diversity will likely decrease due to future climate change. Vulnerability at a watershed scale was negatively correlated with average genetic diversity (r = ?0.77; P < 0.001); watersheds containing populations with lower average genetic diversity generally had the lowest habitat complexity, warmest stream temperatures, and greatest frequency of winter flooding. Together, these findings have important conservation implications for bull trout and other imperiled species. Genetic diversity is already depressed where climatic vulnerability is highest; it will likely erode further in the very places where diversity may be most needed for future persistence.     

Modelling competition and hybridization between native cutthroat trout and nonnative rainbow and hybrid trout

Native salmonid fish have been displaced worldwide by nonnatives through hybridization, competition, and predation, but the dynamics of these factors are poorly understood. We apply stochastic Lotka–Volterra models to the displacement of cutthroat trout by rainbow/hybrid trout in the Snake River, Idaho, USA. Cutthroat trout are susceptible to hybridization in the river but are reproductively isolated in tributaries via removal of migratory rainbow/hybrid spawners at weirs. Based on information-theoretic analysis, population data provide evidence that hybridization was the primary mechanism for cutthroat trout displacement in the first 17 years of the invasion. However, under some parameter values, the data provide evidence for a model in which interaction occurs among fish from both river and tributary subpopulations. This situation is likely to occur when tributary-spawned cutthroat trout out-migrate to the river as fry. The resulting competition with rainbow/hybrid trout can result in the extinction of cutthroat trout even when reproductive segregation is maintained.     

Hierarchical population structure and genetic diversity of lake trout (Salvelinus namaycush) in a dendritic system in Northern Labrador

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Development and evaluation of 200 novel SNP assays for population genetic studies of westslope cutthroat trout and genetic identification of related taxa

DNA sequence data were collected and screened for single nucleotide polymorphisms (SNPs) in westslope cutthroat trout (Oncorhynchus clarki lewisi) and also for substitutions that could be used to genetically discriminate rainbow trout (O. mykiss) and cutthroat trout, as well as several cutthroat trout subspecies. In total, 260 expressed sequence tag‐derived loci were sequenced and allelic discrimination genotyping assays developed from 217 of the variable sites. Another 50 putative SNPs in westslope cutthroat trout were identified by restriction‐site‐associated DNA sequencing, and seven of these were developed into assays. Twelve O. mykiss SNP assays that were variable within westslope cutthroat trout and 12 previously published SNP assays were also included in downstream testing. A total of 241 assays were tested on six westslope cutthroat trout populations (N = 32 per population), as well as collections of four other cutthroat trout subspecies and a population of rainbow trout. All assays were evaluated for reliability and deviation from Hardy–Weinberg and linkage equilibria. Poorly performing and duplicate assays were removed from the data set, and the remaining 200 assays were used in tests of population differentiation. The remaining markers easily distinguished the various subspecies tested, as evidenced by mean G_ST of 0.74. A smaller subset of the markers (N = 86; average G_ST = 0.40) was useful for distinguishing the six populations of westslope cutthroat trout. This study increases by an order of magnitude the number of genetic markers available for the study of westslope cutthroat trout and closely related taxa and includes many markers in genes (developed from ESTs).