Interspecific hybridization represents a dynamic evolutionary phenomenon and major conservation problem in salmonid fishes. In this study we used amplified fragment length polymorphisms (AFLP) and mitochondrial DNA (mtDNA) markers to describe the extent and characterize the pattern of hybridization and introgression between coastal rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki). Hybrid individuals were initially identified using principle coordinate analysis of 133 polymorphic AFLP markers. Subsequent analysis using 23 diagnostic AFLP markers revealed the presence of F1, rainbow trout backcross, cutthroat trout backcross and later-generation hybrids. mtDNA analysis demonstrated equal numbers of F1 hybrids with rainbow and cutthroat trout mtDNA indicating reciprocal mating of the parental types. In contrast, rainbow and cutthroat trout backcross hybrids always exhibited the mtDNA from the recurrent parent, indicating a male hybrid mating with a pure female. This study illustrates the usefulness of the AFLP technique for generating large numbers of species diagnostic markers. The pattern of hybridization raises many questions concerning the existence and action of reproductive isolating mechanisms between these two species. Our findings are consistent with the hypothesis that introgression between anadromous populations of coastal rainbow and coastal cutthroat trout is limited by an environment-dependent reduction in hybrid fitness.
BackgroundIntrogressive hybridization is an important evolutionary process that can lead to the creation of novel genome structures and thus potentially new genetic variation for selection to act upon. On the other hand, hybridization with introduced species can threaten native species, such as cutthroat trout (Oncorhynchus clarkii) following the introduction of rainbow trout (O. mykiss). Neither the evolutionary consequences nor conservation implications of rainbow trout introgression in cutthroat trout is well understood. Therefore, we generated a genetic linkage map for rainbow-Yellowstone cutthroat trout (O. clarkii bouvieri) hybrids to evaluate genome processes that may help explain how introgression affects hybrid genome evolution.ResultsThe hybrid map closely aligned with the rainbow trout map (a cutthroat trout map does not exist), sharing all but one linkage group. This linkage group (RYHyb20) represented a fusion between an acrocentric (Omy28) and a metacentric chromosome (Omy20) in rainbow trout. Additional mapping in Yellowstone cutthroat trout indicated the two rainbow trout homologues were fused in the Yellowstone genome. Variation in the number of hybrid linkage groups (28 or 29) likely depended on a Robertsonian rearrangement polymorphism within the rainbow trout stock. Comparison between the female-merged F1 map and a female consensus rainbow trout map revealed that introgression suppressed recombination across large genomic regions in 5 hybrid linkage groups. Two of these linkage groups (RYHyb20 and RYHyb25_29) contained confirmed chromosome rearrangements between rainbow and Yellowstone cutthroat trout indicating that rearrangements may suppress recombination. The frequency of allelic and genotypic segregation distortion varied among parents and families, suggesting few incompatibilities exist between rainbow and Yellowstone cutthroat trout genomes.ConclusionsChromosome rearrangements suppressed recombination in the hybrids. This result supports several previous findings demonstrating that recombination suppression restricts gene flow between chromosomes that differ by arrangement. Conservation of synteny and map order between the hybrid and rainbow trout maps and minimal segregation distortion in the hybrids suggest rainbow and Yellowstone cutthroat trout genomes freely introgress across chromosomes with similar arrangement. Taken together, these results suggest that rearrangements impede introgression. Recombination suppression across rearrangements could enable large portions of non-recombined chromosomes to persist within admixed populations.
Spatial partitioning and asymmetric hybridization among sympatric coastal steelhead trout ( Oncorhynchus mykiss irideus ), coastal cutthroat trout ( O. clarki clarki ) and interspecific hybrids C A R AbstractHybridization between sympatric species provides unique opportunities to examine the contrast between mechanisms that promote hybridization and maintain species integrity. We surveyed hybridization between sympatric coastal steelhead ( Oncorhynchus mykiss irideus ) and coastal cutthroat trout ( O. clarki clarki ) from two streams in Washington State, Olsen Creek (256 individuals sampled) and Jansen Creek (431 individuals sampled), over a 3-year period. We applied 11 O. mykiss -specific nuclear markers, 11 O. c. clarki -specific nuclear markers and a mitochondrial DNA marker to assess spatial partitioning among species and hybrids and determine the directionality of hybridization. F 1 and post-F 1 hybrids, respectively, composed an average of 1.2% and 33.6% of the population sampled in Jansen Creek, and 5.9% and 30.4% of the population sampled in Olsen Creek. A modest level of habitat partitioning among species and hybrids was detected. Mitochondrial DNA analysis indicated that all F 1 hybrids ( 15 from Olsen Creek and five from Jansen Creek) arose from matings between steelhead females and cutthroat males implicating a sneak spawning behaviour by cutthroat males. First-generation cutthroat backcrosses contained O. c. clarki mtDNA more often than expected suggesting natural selection against F 1 hybrids. More hybrids were backcrossed toward cutthroat than steelhead and our results indicate recurrent hybridization within these creeks. Age analysis demonstrated that hybrids were between 1 and 4 years old. These results suggest that within sympatric salmonid hybrid zones, exogenous processes (environmentally dependent factors) help to maintain the distinction between parental types through reduced fitness of hybrids within parental environments while divergent natural selection promotes parental types through distinct adaptive advantages of parental phenotypes.
A suite of 26 PCR‐based markers was developed that differentiates rainbow (Oncorhynchus mykiss) and coastal cutthroat trout (O. clarki clarki). The markers also differentiated rainbow from other cutthroat trout subspecies (O. clarki), and several of the markers differentiated between cutthroat trout subspecies. This system has numerous positive attributes, including: nonlethal sampling, high species‐specificity and products that are easily identified and scored using agarose gel electrophoresis. The methodology described for developing the markers can be applied to virtually any system in which numerous markers are desired for identifying or differentiating species or subspecies.
Environmental DNA (eDNA) has emerged as a potentially powerful tool for use in conservation and resource management, including for tracking the recolonization dynamics of fish populations. We used eDNA to assess the effectiveness of dam removal to restore fish passage on the Elwha River in Washington State (USA). Using a suite of 11 species‐specific eDNA polymerase chain reaction (PCR) assays, we showed that most targeted anadromous species (five Pacific Salmon species and Pacific Lamprey) were able to pass upstream of both former dam sites. Multiscale occupancy modeling showed that the timing and spatial extent of recolonization differed among species during the four years of post‐dam removal monitoring. More abundant species like Chinook Salmon and Coho Salmon migrated farther into the upper portions of the watershed than less abundant species like Pink Salmon and Chum Salmon. Sampling also allowed assessment of potamodromous fish species. Bull Trout and Rainbow Trout, ubiquitous species in the watershed, were detected at all sampling locations. Environmental DNA from Brook Trout, a non‐native species isolated between the dams prior to dam removal, was detected downstream of Elwha dam but rarely upstream of the Glines Canyon Dam suggested that the species has not expanded its range appreciably in the watershed following dam removal. We found that eDNA was an effective tool to assess the response of fish populations to large‐scale dam removal on the Elwha River.
Historic introductions of nonnative rainbow trout Oncorhynchus mykiss into the native habitats of cutthroat trout O. clarkii have impacted cutthroat trout populations through introgressive hybridization, creating challenges and concerns for cutthroat trout conservation. We examined the effects of rainbow trout introductions on the native westslope cutthroat trout O. c. lewisii within the Stehekin River drainage, North Cascades National Park, Washington, by analyzing 1,763 salmonid DNA samples from 18 locations with nine diagnostic nuclear DNA markers and one diagnostic mitochondrial DNA (mtDNA) marker. Pure westslope cutthroat trout populations only occurred above upstream migration barriers in the Stehekin River and Park Creek. Two categories of rainbow trout admixture were observed: (1) less than 10% within the Stehekin River drainage above the Bridge Creek confluence and the middle and upper Bridge Creek drainage and (2) greater than 30% within the Stehekin River below the Bridge Creek confluence and in lower Bridge Creek. Hybrid indices and multilocus genotypes revealed an absence of rainbow trout and reduced hybrid diversity within the Stehekin River above the Bridge Creek confluence relative to hybrid diversity in the Stehekin River below the confluence and within lower Bridge Creek. Cytonuclear disequilibrium statistics revealed assortative mating between westslope cutthroat and rainbow trout but not among hybrids within the same locations. This suggests that a randomly mating hybrid swarm does not currently exist. However, continual migration of parental genotypes into the study location could also create significant cytonuclear disequilibria. The Stehekin River represents a novel and unique example of a dynamic hybridization zone where the invasion of rainbow trout alleles into the Stehekin River westslope cutthroat trout population above the Bridge Creek confluence appears to be impeded, suggesting that divergent ecological or evolutionary mechanisms promote the population structure within the Stehekin River drainage, depending upon location.
Eight polymerase chain reaction primer sets amplifying bi-parentally inherited speciesspecific markers were developed that differentiate between rainbow trout ( Oncorhynchus mykiss ) and various cutthroat trout ( O. clarki ) subspecies. The primers were tested within known F 1 and first generation hybrid backcrosses and were shown to amplify codominantly within hybrids. Heterozygous individuals also amplified a slower migrating band that was a heteroduplex, caused by the annealing of polymerase chain reaction products from both species. These primer sets have numerous advantages for native cutthroat trout conservation including statistical genetic analyses of known crosses and simple hybrid identification.
We investigated the evolutionary relationships among five sympatric morphs of Dolly Varden Salvelinus malma (white, Schmidti, longhead, river, and dwarf) inhabiting landlocked Kronotsky Lake on the Kamchatka Peninsula, Russia, and an anadromous population below the barrier waterfall on the outflowing Kronotsky River. Morphological analyses indicated phenotypic differentiation corresponding to preferred habitat, the longhead (a limnetic piscivorous morph) having a fusiform body, long jaw, and short fins and the Schmidti (a benthic morph) having a robust body, small jaw, and long fins. Analysis of molecular variance among the Kronotsky Lake morphs indicated that contemporary gene flow is restricted both among morphs within locations and among locations within morphs. Gene flow from Kronotsky Lake into the anadromous population also appears to be restricted. Our findings indicate that there are two divergent evolutionary lineages, one consisting of the white, Schmidti, river, and dwarf morphs and the other of the longhead morph and the anadromous population, which suggests that Kronotsky Lake was subject to separate waves of immigration. The Kronotsky Lake Dolly Varden morphs may represent an example of ecological speciation in progress, and we present a working hypothesis for the diversification of morphs within Kronotsky Lake.
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