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Landscape Ecology

, Volume 21, Issue 6, pp 901–916 | Cite as

Landscape attributes and life history variability shape genetic structure of trout populations in a stream network

  • Helen M. NevilleEmail author
  • Jason B. Dunham
  • Mary M. Peacock
Research Article

Abstract

Spatial and temporal landscape patterns have long been recognized to influence biological processes, but these processes often operate at scales that are difficult to study by conventional means. Inferences from genetic markers can overcome some of these limitations. We used a landscape genetics approach to test hypotheses concerning landscape processes influencing the demography of Lahontan cutthroat trout in a complex stream network in the Great Basin desert of the western US. Predictions were tested with population- and individual-based analyses of microsatellite DNA variation, reflecting patterns of dispersal, population stability, and local effective population sizes. Complementary genetic inferences suggested samples from migratory corridors housed a mixture of fish from tributaries, as predicted based on assumed migratory life histories in those habitats. Also as predicted, populations presumed to have greater proportions of migratory fish or from physically connected, large, or high quality habitats had higher genetic variability and reduced genetic differentiation from other populations. Populations thought to contain largely non-migratory individuals generally showed the opposite pattern, suggesting behavioral isolation. Estimated effective sizes were small, and we identified significant and severe genetic bottlenecks in several populations that were isolated, recently founded, or that inhabit streams that desiccate frequently. Overall, this work suggested that Lahontan cutthroat trout populations in stream networks are affected by a combination of landscape and metapopulation processes. Results also demonstrated that genetic patterns can reveal unexpected processes, even within a system that is well studied from a conventional ecological perspective.

Keywords

Bottlenecks Connectivity Cutthroat trout Dispersal Effective population size Founder effects Habitat structure Landscape genetics Metapopulation Oncorhynchus  clarkii 

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References

  1. Allan D.J. 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu. Rev. Ecol. Evol. Syst. 35. Google Scholar
  2. Angers, B., Bernatchez, L., Angers, A., Desgroseillers, L. 1995Specific microsatellite loci for brook charr reveal strong population subdivision on a microgeographic scaleJournal of Fish Biology47177185CrossRefGoogle Scholar
  3. Angers, B., Magnan, P., Plante, M., Bernatchez, L. 1999Canonical correspondence analysis for estimating spatial and environmental effects on microsatellite gene diversity in brook charr (Salvelinus fontinalis)Mol. Ecol.810431053CrossRefGoogle Scholar
  4. Beerli, P., Felsenstein, J. 1999Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approachGenetics152763773PubMedGoogle Scholar
  5. Beerli, P., Felsenstein, J. 2001Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approachProc. Natl. Acad. Sci.9845634568PubMedCrossRefGoogle Scholar
  6. Behnke, R.J. 1992Native Trout of Western North AmericaAmerican Fisheries SocietyBethesdaGoogle Scholar
  7. Berry, O., Tocher, M.D., Gleeson, D.M., Sarre, S.D. 2005Effect of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinksConserv. Biol.19855864CrossRefGoogle Scholar
  8. Colyer, W. 2002Seasonal movements of fluvial Bonneville cutthroat trout in the Thomas fork of the Bear RiverIdaho-WyomingUtah State UniversityLogan, UtahMaster’s ThesisGoogle Scholar
  9. Cornuet, J.-M., Piry, S., Luikart, G., Estoup, A., Solignac, M. 1999New methods employing multilocus genotypes to select or exclude populations as origins of individualsGenetics15319892000PubMedGoogle Scholar
  10. Costello, A.B., Down, T.E., Pollard, S.M., Pacas, C.J., Taylor, E.B. 2003The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull troutSalvelinus confluentus (Pisces: Salmonidae)Evolution57328344PubMedCrossRefGoogle Scholar
  11. Couvet, D. 2002Deleterious effects of restricted gene flow in fragmented populationsConserv. Biol.16369376CrossRefGoogle Scholar
  12. Davies, N., Villablanca, F.X., Roderick, G.K. 1999Determining the source of individuals: multilocus genotyping in nonequilibrium population geneticsTrends Ecol. Evol.141721PubMedCrossRefGoogle Scholar
  13. Dunham, J.B. 1996The population ecology of stream-living Lahontan cutthroat trout (Oncorhynchus clarki henshawi). Doctoral DissertationUniversity of NevadaRenoGoogle Scholar
  14. Dunham, J.B., Peacock, M.M., Rieman, B.E., Schroeter, R.E., Vinyard, G.L. 1999Local and geographic variability in the distribution of stream-living Lahontan cutthroat troutTrans. Amer. Fish. Soc.128875889CrossRefGoogle Scholar
  15. Dunham, J.B., Rieman, B.E., Peterson, J.T. 2002Patch-based models of species occurrence: lessons from salmonid fishes in streamsScott, J.M.Heglund, P.J.Morrison, M.Raphael, M.Haufler, J.Wall, B. eds. Predicting Species Occurrences: Issues of Scale and AccuracyIsland PressCovelo, CA327334Google Scholar
  16. Dunham, J.B., Vinyard, G.L., Rieman, B.E. 1997Habitat fragmentation and extinction risk of Lahontan cutthroat troutNorth American Journal of Fisheries Management1711261133CrossRefGoogle Scholar
  17. Dunham, J.B., Young, K.A., Gresswell, R.E., Rieman, B.E. 2003Effects of fire on fish populations: landscape perspectives on persistence of native fishes and nonnative fish invasionsFor. Ecol. Manage.178183196CrossRefGoogle Scholar
  18. Fausch, K.D., Torgersen, C.E., Baxter, C.V., Li, H.W. 2002Landscapes to riverscapes: bridging the gap between research and conservation of stream fishesBioscience52483498CrossRefGoogle Scholar
  19. Fleishman, E., Ray, C., Sjogren-Gulve, P., Boggs, C.L., Murphy, D.D. 2002Assessing the roles of patch quality, areaand isolation in predicting metapopulation dynamicsConserv. Biol.16706716CrossRefGoogle Scholar
  20. Funk, C.W., Blouin, M.S., Corn, P.S., Maxell, B.A., Pilliod, D.S., Amish, S., Allendorf, F.W. 2005Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscapeMol. Ecol.14483496PubMedCrossRefGoogle Scholar
  21. Garza, J.C., Williamson, E.G. 2001Detection of reduction in population size using data from microsatellite lociMol. Ecol.10305318PubMedCrossRefGoogle Scholar
  22. Gerlach, G., Musolf, K. 2000Fragmentation of landscape as a cause for genetic subdivision in bank volesConserv. Biol.1410661074CrossRefGoogle Scholar
  23. Goudet J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html.
  24. Gowan, C., Young, M.K., Fausch, K.D., Riley, S.C. 1994Restricted movement in resident stream salmonids: a paradigm lost?Can. J. Fish. Aquat. Sci.5126262637CrossRefGoogle Scholar
  25. Hale, M.L., Lurz, P.W.W., Shirley, M.D.F., Rushton, S., Fuller, R.M., Wolff, K. 2001Impact of landscape management on the genetic structure of red squirrel populationsScience29322462247PubMedCrossRefGoogle Scholar
  26. Hansen, M.M., Mensberg, K.-L. 1998Genetic differentiation and relationship between genetic and geographical distance in Danish sea trout (Salmo trutta L.) populationsHeredity81493504CrossRefGoogle Scholar
  27. Hansen, M.M., Nielsen, E.E., Mensberg, K.-L.D. 1997The problem of sampling families rather than populations: relatedness among individuals in samples of juvenile brown trout Salmo trutta LMol. Ecol.6469474CrossRefGoogle Scholar
  28. Hanski, I. 1994Patch-occupancy dynamics in fragmented landscapesTrends in Ecology & Evolution9131135CrossRefGoogle Scholar
  29. Hanski, I. 1999Metapopulation EcologyOxford University PressNew YorkGoogle Scholar
  30. Hanski, I., Breuker, C., Schops, K., Setchfield, R., Nieminen, M. 2002Population history and life history influence the migration rate of female Glanville fritillary butterfliesOikos988797CrossRefGoogle Scholar
  31. Hanski, I., Eralahti, C., Kankare, M., Ovaskainen, O., Sire, H. 2004Variation in migration propensity among individuals maintined by landscape structureEcol. Lett.7958966CrossRefGoogle Scholar
  32. Hanski, I., Simberloff, D. 1997The metapopulation approachits history, conceptual domain, and application to conservationHanski, I.Gilpin, M. eds. Metapopulation Biology: Ecology, Genetics, and EvolutionAcademic PressSan Diego126Google Scholar
  33. Hanski, I., Singer, M.C. 2001Extinction–colonization dynamics and host–plant choice in butterfly metapopulationsAm. Nat.158341353CrossRefPubMedGoogle Scholar
  34. Hartl, D.L., Clark, A.G. 1997Principles of Population GeneticsSinauer Associates, Inc.SunderlandGoogle Scholar
  35. Hedrick, P. 1999Perspective: highly variable loci and their interpretation in evolution and conservationEvolution53313318CrossRefGoogle Scholar
  36. Hedrick, P.W., Gilpin, M.E. 1997Genetic effective size of a metapopulationHanski, I.A.Gilpin, M.E. eds. Metapopulation Biology: Ecology, Genetics, and EvolutionAcademic PressSan Diego166181Google Scholar
  37. Hendry, A.P., Bohlin, T., Jonsson, B., Berg, O.K. 2004To sea or not to sea? Anadromy versus non-anadromy in SalmonidsHendry, A.P.Stearns, S.C. eds. Evolution Illuminated: Salmon and Their RelativesOxfordOxford University Press93125Google Scholar
  38. Ingram, K.K., Gordon, D.M. 2003Genetic analysis of dispersal dynamics in an invading population of argentine antsEcology8428322842Google Scholar
  39. Jonsson, B., Jonsson, N. 1993Partial migration – niche shift versus sexual-maturation in fishesRev. Fish Biol. Fish.3348365CrossRefGoogle Scholar
  40. Knutsen, H., Knutsen, J.A., Jorde, P.E. 2001Genetic evidence for mixed origin of recolonized sea trout populationsHeredity87207214PubMedCrossRefGoogle Scholar
  41. Levins, R. 1969Some demographic and genetic consequences of environmental heterogeneity for biological controlBull. Entomol. Soc. Am.15237240Google Scholar
  42. MacArthur, R.H., Wilson, E.O. 1967The Theory of Island BiogeographyPrinceton University PressPrincetonGoogle Scholar
  43. Manel, S., Schwartz, M.K., Luikart, G., Taberlet, P. 2003Landscape genetics: combining landscape ecology and population geneticsTrends Ecol. Evol.18189197CrossRefGoogle Scholar
  44. McConnell, S.K., O’Reilly, P.T., Hamilton, L., Wright, J.M., Bentzen, P. 1995Polymorphic microsatellite loci from Atlantic salmon (Salmo salar): genetic differentiation of North American and European populationsCan. J. Fish Aquat. Sci.5218631872Google Scholar
  45. Moilanen, A. 1999Patch occupancy models of metapopulation dynamics: efficient parameter estimation using implicit statistical inferenceEcology8010311043CrossRefGoogle Scholar
  46. Montgomery, D.R. 1999Process domains and the river continuumJ. Am. Water Resour. Ass.35397410Google Scholar
  47. Morris, D.B., Richard, K.R., Wright, J.M. 1996Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonidsCan. J. Fish. Aquat. Sci.53120126CrossRefGoogle Scholar
  48. Nakano, S., Kitano, S., Maekawa, K. 1996Potential fragmentation and loss of thermal habitats for charrs in the Japanese archipelago due to climatic warmingFreshw. Biol.36711722CrossRefGoogle Scholar
  49. Näslund, I. 1993Migratory behavior of brown troutSalmo trutta L.: implications of genetic and environmental influencesEcology of Freshwater Fish25157CrossRefGoogle Scholar
  50. Nei, M. 1987Molecular Evolutionary GeneticsColumbia University PressNew YorkGoogle Scholar
  51. Neville Arsenault, H. 2003Genetic assessment of complex dynamics in an interior salmonid metapopulationUniversity of NevadaRenoDoctoral Dissertation. Ecology, Evolution and Conservation BiologyGoogle Scholar
  52. Neville H., Dunham J. and Peacock M. In press. Assessing connectivity in salmonid fishes with DNA microsatellite markers. In: Crooks K. and Sanjayan M.A. (eds), Connectivity Conservation. Cambridge University Press, Cambridge, UK.Google Scholar
  53. Nielsen, J.L., Sage, G.K. 2002Population genetic structure in Lahontan cutthroat troutTrans. Am. Fish. Soc.131376388CrossRefGoogle Scholar
  54. Northcote, T.G., Hartman, G.F. 1988The biology and significance of stream trout populations (Salmo spp.) living above and below waterfallsPolskie Archiuvum Hydrobiologii35409422Google Scholar
  55. O’Reilly, P.T., Hamilton, L.C., McConnell, S.K., Wright, J.M. 1996Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellitesCan. J. Fish. Aquat. Sci.5322922298CrossRefGoogle Scholar
  56. Ostergaard, S., Hansen, M.M., Loeschcke, V., Nielsen, E.E. 2003Long-term temporal changes of genetic composition in brown trout (Salmo trutta L.) populations inhabiting an unstable environmentMol. Ecol.1231233135PubMedCrossRefGoogle Scholar
  57. Parker, H.G., Kim, L.V., Sutter, N.B., Carlson, S., Lorentzen, T.D., Malek, T.B., Johnson, G.S., DeFrance, H.B., Ostrander, E.A., Kruglyak, L. 2004Genetic structure of the purebred domestic dogScience30411601164PubMedCrossRefGoogle Scholar
  58. Peacock, M.M., Neville, H., Kirchoff, V. 2004Ten species specific microsatellite loci for Lahontan cutthroat troutOncorhynchus clarki henshawi Mol. Ecol. Notes4557559CrossRefGoogle Scholar
  59. Pritchard, J.K., Stephens, M., Donnelly, P. 2000Inference of population structure using multilocus genotype dataGenetics155945959PubMedGoogle Scholar
  60. Pulliam, R.H. 1988Sources, sinks, and population regulationAm. Nat.132652661CrossRefGoogle Scholar
  61. Ray, C. 2001Maintaining genetic diversity despite local extinctions: a spatial scaling problemBiol. Conserv.100314CrossRefGoogle Scholar
  62. Rieman, B.E., Dunham, J.B. 2000Metapopulations of salmonids: a synthesis of life history patterns and empirical observationsEcol. Freshw. Fish.95164CrossRefGoogle Scholar
  63. Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelivs, W. , Hanski, I. 1998Inbreeding and extinction in a butterfly metapopulationsNature392491494CrossRefGoogle Scholar
  64. Schlosser, I.J. 1995Critical landscape attributes that influence fish population dynamics in headwater streamsHydrobiologia3037181Google Scholar
  65. Schlosser, I.J., Angermeier, P.L. 1995Spatial variation in demographic processes of lotic fishes: conceptual models, empirical evidenceand implications for conservationAmerican Fisheries Society Symposium17392401Google Scholar
  66. Schneider, S., Roessli, D., Excoffier, L. 2000Arlequin ver. 2.000: A software for population genetics data analysisGenetics and Biometry Laboratory, University of GenevaSwitzerlandGoogle Scholar
  67. Schrank, A.J., Rahel, F.J. 2004Movement patterns in inland cutthroat trout (Oncorhynchus clarki utah): management and conservation implicationsCan. J. Fish. Aquat. Sci.6115281537CrossRefGoogle Scholar
  68. Scribner, K.T., Gust, J.R., Fields, R.L. 1996Isolation and characterization of novel salmon microsatellite loci: cross-species amplification and population genetic applicationsCan. J. Fish. Aquat. Sci.53833841CrossRefGoogle Scholar
  69. Slatkin, M. 1985Gene flow in natural populationsAnn. Rev. Ecol. Syst.16393430CrossRefGoogle Scholar
  70. Smedbol, R.K., McPherson, A., Hansen, M.M., Kenchington, E. 2002Myths and moderation in marine ‘metapopulations’?Fish and Fisheries32035CrossRefGoogle Scholar
  71. Steinberg, E.K., Lindner, K.R., Gallea, J., Maxwell, A., Meng, J., Allendorf, F.W. 2002Rates and patterns of microsatellite mutations in pink salmonMol. Biol. Evol.1911981202PubMedGoogle Scholar
  72. Taberlet, P., Luikart, G. 1999Non-invasive genetic sampling and individual identificationBiol. J. Linn. Soc.684155CrossRefGoogle Scholar
  73. Taylor, E.B., Stamford, M.D., Baxter, J.S. 2003Population subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implicationsMol. Ecol.1226092622PubMedCrossRefGoogle Scholar
  74. Turner, M.G. 1989Landscape ecology: the effect of pattern on processAnnu. Rev. Ecol. Syst.20171197CrossRefGoogle Scholar
  75. Turner, M.G., Collins, S.L., Lugo, A.E., Magnuson, J.J., Rupp, T.S., Swanson, F.J. 2003Disturbance dynamics and the ecological response: the contribution of long-term ecological researchBioscience534656CrossRefGoogle Scholar
  76. Walker, S.R., Novaro, A.J., Branch, L.C. 2003Effects of patch attributes, barriers, and distance between patches on the distribution of a rock-dwelling rodent (Lagidium viscacia)Landcape Ecology18185192CrossRefGoogle Scholar
  77. Waples, R.S. 1990Temporal changes of allele frequency in Pacific salmon: implications for mixed-stock fishery analysisCan. J. Fish. Aquat. Sci.47968976CrossRefGoogle Scholar
  78. Weber, J.L., Wong, C. 1993Mutation of human short tandem repeatsHum. Mol. Genet.211231128PubMedGoogle Scholar
  79. Weir, B.S., Cockerham, C.C. 1984Estimating F-statistics for the analysis of population structureEvolution3813581370CrossRefGoogle Scholar
  80. Whitlock, M.C., McCauley, D.E. 1999Indirect measures of gene flow and migration: Fst/ = 1/(4Nm + 1)Heredity82117125PubMedCrossRefGoogle Scholar
  81. Wiens, J.A. 2002Riverine landscapes: taking landscape ecology into the waterFreshw. Biol.47501515CrossRefGoogle Scholar
  82. Wofford, J.E.B., Gresswell, R.E., Banks, M.A. 2005Influence of barriers to movement on within-watershed genetic variation of coastal cutthroat troutEcol. Appl.15638637Google Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Helen M. Neville
    • 1
    • 2
    Email author
  • Jason B. Dunham
    • 2
    • 3
  • Mary M. Peacock
    • 1
  1. 1.Department of Biology/314University of NevadaRenoUSA
  2. 2.Rocky Mountain Research StationBoiseUSA
  3. 3.USGS FRESC Corvallis Research Group 3200 SW Jefferson Way Corvallis

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