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 (θ) 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.

[1]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[2]  A. Templeton,et al.  CORRELATION OF PAIRWISE GENETIC AND GEOGRAPHIC DISTANCE MEASURES: INFERRING THE RELATIVE INFLUENCES OF GENE FLOW AND DRIFT ON THE DISTRIBUTION OF GENETIC VARIABILITY , 1999, Evolution; international journal of organic evolution.

[3]  J. Lawton,et al.  Range, population abundance and conservation. , 1993, Trends in ecology & evolution.

[4]  CLINAL VARIATION AT MICROSATELLITE LOCI REVEALS HISTORICAL SECONDARY INTERGRADATION BETWEEN GLACIAL RACES OF COREGONUS ARTEDI (TELEOSTEI: COREGONINAE) , 2001, Evolution; international journal of organic evolution.

[5]  K. Scribner,et al.  Isolation and characterization of novel salmon microsatellite loci: cross-species amplification and population genetic applications , 1996 .

[6]  J. Kershner,et al.  Conserving Inland Cutthroat Trout in Small Streams: How Much Stream is Enough? , 2000 .

[7]  E. Wiley,et al.  The Zoogeography of North American Freshwater Fishes , 1987 .

[8]  F. Allendorf,et al.  Conservation and Distribution of Genetic Variation in a Polytypic Species, the Cutthroat Trout , 1988 .

[9]  M. Lynch,et al.  THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES , 1999, Evolution; international journal of organic evolution.

[10]  P. Hedrick PERSPECTIVE: HIGHLY VARIABLE LOCI AND THEIR INTERPRETATION IN EVOLUTION AND CONSERVATION , 1999, Evolution; international journal of organic evolution.

[11]  C. Bouza,et al.  Genetic structure of brown trout, Salmo trutta L., at the southern limit of the distribution range of the anadromous form , 1999, Molecular ecology.

[12]  J. Goudet FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995) , 2001 .

[13]  D. Crawford,et al.  The evolutionary significance of genetic variation at enzyme synthesizing loci in the teleost Fundulus heteroclitus , 1991 .

[14]  P. Moran Current conservation genetics: building an ecological approach to the synthesis of molecular and quantitative genetic methods , 2002 .

[15]  I. Hanski,et al.  Inbreeding and extinction in a butterfly metapopulation , 1998, Nature.

[16]  H. G. Baker,et al.  Differentiation of populations. , 1970, Science.

[17]  M. Nei,et al.  THE BOTTLENECK EFFECT AND GENETIC VARIABILITY IN POPULATIONS , 1975, Evolution; international journal of organic evolution.

[18]  B. Rieman,et al.  Habitat Fragmentation and Extinction Risk of Lahontan Cutthroat Trout , 1997 .

[19]  P. Bentzen,et al.  Genetic and Behavioral Evidence for Restricted Gene Flow among Coastal Cutthroat Trout Populations , 2001 .

[20]  Mark V. Lomolino,et al.  Dynamic biogeography and conservation of endangered species , 2000, Nature.

[21]  V. Sork,et al.  Landscape approaches to historical and contemporary gene flow in plants. , 1999, Trends in ecology & evolution.

[22]  J. Rinne,et al.  Native trout of western North America , 1992, Reviews in Fish Biology and Fisheries.

[23]  J. Maienschein Growth of biological thought , 1994, Nature.

[24]  M. Nishida,et al.  Phylogeographic relationships within the Mediterranean turbot inferred by mitochondrial DNA haplotype variation , 2004 .

[25]  E. Taylor,et al.  A molecular analysis of hybridization between native westslope cutthroat trout and introduced rainbow trout in southeastern British Columbia, Canada , 2001 .

[26]  P. O’Reilly,et al.  Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites , 1996 .

[27]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[28]  Blouin,et al.  Isolation and inheritance of novel microsatellites in Chinook Salmon (Oncorhynchus tschawytscha) , 1999 .

[29]  R. Nichols,et al.  Spatial patterns of genetic variation generated by different forms of dispersal during range expansion , 1996, Heredity.

[30]  LANDSCAPE STRUCTURE AND HIERARCHICAL GENETIC DIVERSITY IN THE BROOK CHARR, SALVELINUS FONTINALIS , 2001 .

[31]  D. Hurwood,et al.  Phylogeography of the freshwater fish, Mogurnda adspersa, in streams of northeastern Queensland, Australia: evidence for altered drainage patterns , 1998, Molecular ecology.

[32]  THE INFLUENCE OF HISTORY AND CONTEMPORARY STREAM HYDROLOGY ON THE EVOLUTION OF GENETIC DIVERSITY WITHIN SPECIES: AN EXAMINATION OF MICROSATELLITE DNA VARIATION IN BULL TROUT, SALVELINUS CONFLUENTUS (PISCES: SALMONIDAE) , 2003, Evolution; international journal of organic evolution.

[33]  J. Carlsson,et al.  Effects of Geomorphological Structures on Genetic Differentiation among Brown Trout Populations in a Northern Boreal River Drainage , 2001 .

[34]  Richard Shine,et al.  Conservation biology: Restoration of an inbred adder population , 1999, Nature.

[35]  T. Northcote Juvenile current response, growth and maturity of above and below waterfall stocks of rainbow trout, Salmo gairdneri , 1981 .

[36]  L. Bernatchez,et al.  Canonical correspondence analysis for estimating spatial and environmental effects on microsatellite gene diversity in brook charr (Salvelinus fontinalis) , 1999 .

[37]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[38]  O. Gaggiotti,et al.  A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data , 1999, Molecular ecology.

[39]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[40]  J. Merilä,et al.  Comparison of genetic differentiation at marker loci and quantitative traits , 2001 .

[41]  F. Allendorf,et al.  Genetic Divergence and Identification of Seven Cutthroat Trout Subspecies and Rainbow Trout , 1987 .

[42]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[43]  Pierre Taberlet,et al.  Landscape genetics: combining landscape ecology and population genetics , 2003 .

[44]  E. C. Pielou,et al.  After the Ice Age : the return of life to glaciated North America , 1991 .

[45]  G Luikart,et al.  New methods employing multilocus genotypes to select or exclude populations as origins of individuals. , 1999, Genetics.

[46]  Peter Lesica,et al.  When Are Peripheral Populations Valuable for Conservation , 1995 .

[47]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[48]  Dianne B. Morris,et al.  Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids , 1996 .

[49]  D. Simberloff,et al.  Extinction by hybridization and introgression , 1996 .

[50]  T. Tammaru,et al.  Allozyme variability in central, peripheral and isolated populations of the scarce heath (Coenonympha hero: Lepidoptera, Nymphalidae); implications for conservation , 2004, Conservation Genetics.

[51]  G. Iwama,et al.  The Physiological Adaptations of the Lahontan Cutthroat Trout (Oncorhynchus clarki henshawi) following Transfer from Well Water to the Highly Alkaline Waters of Pyramid Lake, Nevada (pH 9.4) , 1994, Physiological Zoology.

[52]  J. Mitton,et al.  HISTORICAL SEPARATION AND PRESENT GENE FLOW THROUGH A ZONE OF SECONDARY CONTACT IN PONDEROSA PINE , 1999, Evolution; international journal of organic evolution.

[53]  D. Schmetterling Seasonal Movements of Fluvial Westslope Cutthroat Trout in the Blackfoot River Drainage, Montana , 2001 .

[54]  P. Bentzen,et al.  Microsatellite analysis of genetic population structure in an endangered salmonid: the coastal cutthroat trout (Oncorhynchus clarki clarki) , 1998 .

[55]  Eric J. Loudenslager,et al.  Geographic Patterns of Protein Variation and Subspeciation in Cutthroat Trout, Salmo Clarki , 1980 .

[56]  I. Olsaker,et al.  Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. , 1995, Animal genetics.

[57]  P. Grant Evolution on islands , 1998 .

[58]  J. Nielsen,et al.  Microsatellite diversity in sympatric reproductive ecotypes of Pacific steelhead (Oncorhynchus mykiss) from the Middle Fork Eel River, California , 1999 .

[59]  T. Beacham,et al.  Isolation and cross species amplification of microsatellite loci useful for study of Pacific salmon. , 1999, Animal genetics.

[60]  Einar Eg Nielsen,et al.  Assigning individual fish to populations using microsatellite DNA markers , 2001 .

[61]  Danny C. Lee,et al.  Status and Risk of Extinction for Westslope Cutthroat Trout in the Upper Missouri River Basin, Montana , 1997 .

[62]  A. Carr,et al.  Molecular analysis of , 1997 .

[63]  J. Waters,et al.  Across the Southern Alps by river capture? Freshwater fish phylogeography in South Island, New Zealand , 2000, Molecular ecology.

[64]  M Raymond,et al.  Testing differentiation in diploid populations. , 1996, Genetics.

[65]  L. Bernatchez,et al.  LANDSCAPE STRUCTURE AND HIERARCHICAL GENETIC DIVERSITY IN THE BROOK CHARR, SALVELINUS FONTINALIS , 2001, Evolution; international journal of organic evolution.