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Contemporary and historical river connectivity influence population structure in western brook lamprey in the Columbia River Basin

  • Erin K. Spice
  • Timothy A. Whitesel
  • Gregory S. Silver
  • Margaret F. DockerEmail author
Research Article
  • 41 Downloads

Abstract

The western brook lamprey Lampetra richardsoni (WBL) is a small non-parasitic lamprey that inhabits rivers and streams from southern Alaska to northern California. WBL remain in fresh water throughout their entire life and show limited dispersal. Although adults may migrate short distances upstream to spawn, most movement likely occurs through passive drifting of larvae downstream. Genetic differentiation among populations is thus expected to be high, even within a single basin, but WBL population structure has received little attention. The present study examined population connectivity of WBL from 23 sites throughout the Columbia River Basin and coastal Washington, using eight microsatellite loci and cytochrome b sequence data. Although population structure generally corresponded to contemporary river connectivity, there were some cases where genetic patterns were better explained by historical connections. Microsatellite genetic differentiation among populations separated by < 570 km was moderate to high; FST values ranged from − 0.0026 to 0.7117 and averaged 0.2929. Tributary distance was the best predictor of FST, suggesting that most gene flow takes place in tributaries rather than through the mainstem of the Columbia River. As predicted, gene flow occurred primarily in a downstream direction, resulting in lower genetic diversity in upstream sites. WBL populations in these areas may be particularly vulnerable to local extinction. Therefore, whereas anadromous lamprey management efforts are focused on improving passage at mainstem dams, conservation of WBL will require protection of individual watersheds with particular emphasis on headwater areas.

Keywords

Population structure River system Genetic diversity Glacial refugia Gene flow Non-migratory species 

Notes

Acknowledgements

We thank Jeff Jolley, Ralph Lampman, and Christina Wang for collecting and providing samples; Erin Butts and David Hines for GIS support; Colin Garroway for assistance with spatial analyses; Karen Bailey and Meagan Robidoux for technical assistance in the laboratory; Don Anglin for providing access to a previously unstudied area; and three reviewers from the United States Fish and Wildlife Service (USFWS) for the helpful comments they provided on an earlier draft of this manuscript. Funding was provided by the USFWS and the Natural Sciences and Engineering Research Council (NSERC) of Canada. Mention of trade names does not imply endorsement by the USFWS. The findings and conclusions in this manuscript are those of the authors and do not necessarily represent the views of the USFWS.

Supplementary material

10592_2018_1137_MOESM1_ESM.pdf (629 kb)
Supplementary material 1 (PDF 628 KB)

References

  1. Adamson EAS, Hurwood DA, Mather PB (2012) Insights into historical drainage evolution based on the phylogeography of the chevron snakehead fish (Channa striata) in the Mekong Basin. Freshw Biol 57:2211–2229CrossRefGoogle Scholar
  2. Almada VC, Pereira AM, Robalo JI, Fonseca JP, Levy A, Maia C, Valente A (2008) Mitochondrial DNA fails to reveal genetic structure in sea-lampreys along European shores. Mol Phylogenet Evol 46:391–396PubMedCrossRefPubMedCentralGoogle Scholar
  3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefPubMedCentralGoogle Scholar
  5. Barson NJ, Cable J, Van Oosterhout C (2009) Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source-sink metapopulation structure, founder events and population bottlenecks. J Evol Biol 22:485–497PubMedCrossRefPubMedCentralGoogle Scholar
  6. Beacham TD, McIntosh B, MacConnachie C, Miller KM, Withler RE, Varnavskaya N (2006) Pacific Rim population structure of sockeye salmon as determined from microsatellite analysis. Trans Am Fish Soc 135:174–187CrossRefGoogle Scholar
  7. Beamish RJ, Neville CM (1992) The importance of size as an isolating mechanism in lampreys. Copeia 1992:191–196CrossRefGoogle Scholar
  8. Bickham JW, Wood CC, Patton JC (1995) Biogeographic implications of cytochrome b sequences and allozymes in sockeye (Oncorhynchus nerka). J Hered 86:140–144PubMedCrossRefPubMedCentralGoogle Scholar
  9. Blanchet FG, Legendre P, Borcard D (2008a) Modelling directional spatial processes in ecological data. Ecol Model 215:325–336CrossRefGoogle Scholar
  10. Blanchet FG, Legendre P, Borcard D (2008b) Forward selection of spatial explanatory variables. Ecology 89:2623–2632PubMedCrossRefGoogle Scholar
  11. Blanchet FG, Legendre P, Maranger R, Monti D, Pepin P (2011) Modelling the effect of directional spatial ecological processes at different scales. Oecologia 166:357–368PubMedCrossRefGoogle Scholar
  12. Blanchet FG, Legendre P, Gauthier O (2015) AEM: tools to construct asymmetric eigenvector maps (AEM) spatial variables. R package version 0.6/r127. https://R-Forge.R-project.org/projects/sedar/
  13. Boguski DA, Reid SB, Goodman DH, Docker MF (2012) Genetic diversity, endemism and phylogeny of lampreys within the genus Lampetra sensu stricto (Petromyzontiformes: Petromyzontidae) in western North America. J Fish Biol 81:1891–1914PubMedCrossRefGoogle Scholar
  14. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68CrossRefGoogle Scholar
  15. Bracken FSA, Hoelzel AR, Hume JB, Lucas MC (2015) Contrasting population genetic structure among freshwater-resident and anadromous lampreys: the role of demographic history, differential dispersal, and anthropogenic barriers to movement. Mol Ecol 24:1188–1204PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brown AV, Armstrong ML (1985) Propensity to drift downstream among various species of fish. J Freshw Ecol 3:3–17CrossRefGoogle Scholar
  17. Bryan MB, Zalinski D, Filcek KB, Libants S, Li W, Scribner KT (2005) Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes. Mol Ecol 14:3757–3773PubMedCrossRefGoogle Scholar
  18. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  19. Burridge CP, Craw D, Waters JM (2006) River capture, range expansion, and cladogenesis: the genetic signature of freshwater vicariance. Evolution 60:1038–1049PubMedCrossRefGoogle Scholar
  20. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedPubMedCentralGoogle Scholar
  21. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedPubMedCentralCrossRefGoogle Scholar
  22. Clemens BJ, Beamish RJ, Coates KC et al (2017) Conservation challenges and research needs for Pacific Lamprey in the Columbia River Basin. Fisheries 42:269–280CrossRefGoogle Scholar
  23. Dawson HA, Quintella BR, Almeida PR, Treble AJ, Jolley JC (2015) The ecology of larval and metamorphosing lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 1. Springer, Dordrecht, pp 75–138Google Scholar
  24. Dehais CR, Eudeline R, Berrebi P, Argillier C (2010) Microgeographic genetic isolation in chub (Cyprinidae: Squalius cephalus) population of the Durance River: estimating fragmentation by dams. Ecol Freshw Fish 19:267–278CrossRefGoogle Scholar
  25. Docker MF (2009) A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. In: Brown LR, Chase SD, Moyle PB, Beamish RJ, Mesa MG (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society, Symposium 72, Bethesda, Maryland, pp 71–114Google Scholar
  26. Docker MF, Hume JB, Clemens BJ (2015) Introduction: a surfeit of lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 1. Springer, Dordrecht, pp 1–34Google Scholar
  27. Docker MF, Silver GS, Jolley JC, Spice EK (2016) Simple genetic assay distinguishes lamprey genera Entosphenus and Lampetra: comparison with existing genetic and morphological identification methods. N Am J Fish Manag 36:780–787CrossRefGoogle Scholar
  28. Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493CrossRefGoogle Scholar
  29. Dray S, Legendre P, Blanchet G (2016) packfor: forward Selection with permutation (Canoco p. 46). R package version 0.0-8/r136. https://R-Forge.R-project.org/projects/sedar/
  30. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  31. ESRI (2015) ArcGIS desktop: release 10.3. Environmental Systems Research Institute, RedlandsGoogle Scholar
  32. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefPubMedCentralGoogle Scholar
  33. Farlinger SP, Beamish RJ (1984) Recent colonization of a major salmon-producing lake in British Columbia by Pacific lamprey (Lampetra tridentata). Can J Fish Aquat Sci 41:278–285CrossRefGoogle Scholar
  34. Flanders J, Jones G, Benda P, Dietz C, Zhang S, Li G, Sharifi M, Rossiter SJ (2009) Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum: contrasting results from mitochondrial and microsatellite data. Mol Ecol 18:306–318PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gelfenbaum G, Kaminsky GM (2010) Large-scale coastal change in the Columbia River littoral cell: an overview. Mar Geol 273:1–10CrossRefGoogle Scholar
  36. Goodman DH, Reid SB, Docker MF, Haas GR, Kinziger AP (2008) Mitochondrial DNA evidence for high levels of gene flow among populations of a widely distributed anadromous lamprey Entosphenus tridentatus (Petromyzontidae). J Fish Biol 72:400–417CrossRefGoogle Scholar
  37. Goodman DH, Kinziger AP, Reid SB, Docker MF (2009) Morphological diagnosis of Entosphenus and Lampetra ammocoetes (Petromyzontidae) in Washington, Oregon, and California. In: Brown LR, Chase SD, Moyle PB, Beamish RJ, Mesa MG (eds) Biology, management, and conservation of lampreys in North America. American Fisheries Society, Symposium 72, Bethesda, Maryland, pp 223–232Google Scholar
  38. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  39. Hänfling B, Weetman D (2006) Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the river sculpin, Cottus gobio. Genetics 173:1487–1501PubMedPubMedCentralCrossRefGoogle Scholar
  40. Harris JE, Jolley JC (2017) Estimation of occupancy, density, and abundance of larval lampreys in tributary river mouths upstream of dams on the Columbia River, Washington and Oregon. Can J Fish Aquat Sci 74:843–852CrossRefGoogle Scholar
  41. Harris JE, Jolley JC, Silver GS, Yuen H, Whitesel TA (2016) An experimental evaluation of electrofishing catchability and catch depletion abundance estimates of larval lampreys in a wadeable stream: use of a hierarchical approach. Trans Am Fish Soc 145:1006–1017CrossRefGoogle Scholar
  42. Heckel G, Burri R, Fink S, Desmet JFF, Excoffier L (2005) Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis. Evolution 59:2231–2242PubMedCrossRefGoogle Scholar
  43. Hess JE, Campbell NR, Close DA, Docker MF, Narum SR (2013) Population genomics of Pacific lamprey: adaptive variation in a highly dispersive species. Mol Ecol 22:2898–2916PubMedCrossRefGoogle Scholar
  44. Hogg R, Coghlan SM, Zydlewski J (2013) Anadromous Sea Lampreys recolonize a Maine coastal river tributary after dam removal. Trans Am Fish Soc 142:1381–1394CrossRefGoogle Scholar
  45. Homola JJ, Ruetz CR, Kohler SL, Thum RA (2016) Complex postglacial recolonization inferred from population genetic structure of mottled sculpin Cottus bairdii in tributaries of eastern Lake Michigan, U.S.A. J Fish Biol 89:2234–2250CrossRefGoogle Scholar
  46. Howes BJ, Lindsay B, Lougheed SC (2006) Range-wide phylogeography of a temperate lizard, the five-lined skink (Eumeces fasciatus). Mol Phylogenet Evol 40:183–194PubMedCrossRefPubMedCentralGoogle Scholar
  47. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914PubMedCrossRefPubMedCentralGoogle Scholar
  48. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedPubMedCentralCrossRefGoogle Scholar
  49. Johnson NS, Buchinger TJ, Li W (2015) Reproductive ecology of lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, Dordrecht, pp 265–303Google Scholar
  50. Jolley JC, Silver GS, Whitesel TA (2012) Occupancy and detection of larval Pacific lampreys and Lampetra spp. in a large river: the lower Willamette River. Trans Am Fish Soc 141:305–312CrossRefGoogle Scholar
  51. Jolley JC, Kovalchuk G, Docker MF (2016) River lamprey Lampetra ayresii outmigrant upstream of the John Day Dam in the mid-Columbia river. Northwest Nat 97:48–52CrossRefGoogle Scholar
  52. Jolley JC, Silver GS, Harris JE, Whitesel TA (2018) Pacific lamprey recolonization of a Pacific Northwest river following dam removal. River Res Appl 34:44–51CrossRefGoogle Scholar
  53. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555PubMedCrossRefGoogle Scholar
  54. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  55. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kostow K (2002) Oregon lampreys: natural history, status, and management issues. Oregon Department of Fish and Wildlife, PortlandGoogle Scholar
  57. Luzier CW, Docker MF, Whitesel TA (2010) Characterization of ten microsatellite loci for western brook lamprey Lampetra richardsoni. Conserv Genet Resour 2:71–74CrossRefGoogle Scholar
  58. Maitland PS, Renaud CB, Quintella BR, Close DA, Docker MF (2015) Conservation of native lampreys. In: Docker MF (ed) Lampreys: biology, conservation, and control, vol 1. Springer, Dordrecht, pp 375–427Google Scholar
  59. Martin KE, Steele CA, Brunelli JP, Thorgaard GH (2010) Mitochondrial variation and biogeographic history of Chinook salmon. Trans Am Fish Soc 139:792–802CrossRefGoogle Scholar
  60. Mateus CS, Almeida PR, Quintella BR, Alves MJ (2011) MtDNA markers reveal the existence of allopatric evolutionary lineages in the threatened lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) in the Iberian glacial refugium. Conserv Genet 12:1061–1074CrossRefGoogle Scholar
  61. Mateus CS, Almeida PR, Mesquita N, Quintella BR, Alves MJ (2016) European lampreys: new insights on postglacial colonization, gene flow and speciation. PLoS ONE 11:e0148107PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mazerolle MJ (2017) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.1-1. https://cran.r-project.org/package=AICcmodavg
  63. McCusker MR, Parkinson E, Taylor EB (2000) Mitochondrial DNA variation in rainbow trout (Oncorhynchus mykiss) across its native range: testing biogeographical hypotheses and their relevance to conservation. Mol Ecol 9:2089–2108PubMedCrossRefGoogle Scholar
  64. McPhail JD, Lindsey CC (1986) Zoogeography of the freshwater fishes of Cascadia (the Columbia system and rivers north to the Stikine). In: Hocutt CH, Wiley EO (eds) The zoogeography of North American freshwater fishes. Wiley, New York, pp 615–637Google Scholar
  65. Mock KE, Brim Box JC, Chong JP, Howard JK, Nez DA, Wolf D, Gardner RS (2010) Genetic structuring in the freshwater mussel Anodonta corresponds with major hydrologic basins in the western United States. Mol Ecol 19:569–591PubMedCrossRefGoogle Scholar
  66. Mock KE, Brim Box JC, Chong JP, Furnish J, Howard JK (2013) Comparison of population genetic patterns in two widespread freshwater mussels with contrasting life histories in western North America. Mol Ecol 22:6060–6073PubMedCrossRefGoogle Scholar
  67. Morrissey MB, de Kerckhove DT (2009) The maintenance of genetic variation due to asymmetric gene flow in dendritic metapopulations. Am Nat 174:875–889PubMedCrossRefGoogle Scholar
  68. Moser ML, Almeida PR, Kemp PS, Sorensen PW (2015) Lamprey spawning migration. In: Docker MF (ed) Lampreys: biology, conservation, and control, vol 1. Springer, Dordrecht, pp 215–263Google Scholar
  69. Oksanen J, Blanchet FJ, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: community ecology package. R package version 2.3-5/r2997. https://R-Forge.R-project.org/projects/vegan/
  70. Orsini L, Mergeay J, Vanoverbeke J, De Meester L (2013) The role of selection in driving landscape genomic structure of the waterflea Daphnia magna. Mol Ecol 22:583–601PubMedCrossRefPubMedCentralGoogle Scholar
  71. Page R (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedPubMedCentralGoogle Scholar
  72. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedPubMedCentralCrossRefGoogle Scholar
  73. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  74. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  75. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  76. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenism. J Hered 86:248–249CrossRefGoogle Scholar
  77. Reid SB, Goodman DH (2015) Detectability of Pacific lamprey occupancy in western drainages: implications for distribution surveys. Trans Am Fish Soc 144:315–322CrossRefGoogle Scholar
  78. Reid SB, Boguski DA, Goodman DH, Docker MF (2011) Validity of Lampetra pacifica (Petromyzontiformes: Petromyzontidae), a brook lamprey described from the lower Columbia River Basin. Zootaxa 3091:42–50Google Scholar
  79. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  80. Rougemont Q, Gaigher A, Lasne E, Côte J, Coke M, Besnard AL, Launey S, Evanno G (2015) Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys. J Evol Biol 28:2248–2263PubMedCrossRefGoogle Scholar
  81. Rougemont Q, Roux C, Neuenschwander S, Goudet J, Launey S, Evanno G (2016) Reconstructing the demographic history of divergence between European river and brook lampreys using approximate Bayesian computations. PeerJ 4:e1910PubMedPubMedCentralCrossRefGoogle Scholar
  82. Rougemont Q, Gagnaire PA, Perrier C, Genthon C, Besnard AL, Launey S, Evanno G (2017) Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and non-parasitic lamprey ecotypes. Mol Ecol 26:142–162PubMedCrossRefGoogle Scholar
  83. Rousset F (2008) GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefGoogle Scholar
  84. Ruppert JLW, James PMA, Taylor EB, Rudolfsen T, Veillard M, Davis CS, Watkinson D, Poesch MS (2017) Riverscape genetic structure of a threatened and dispersal limited freshwater species, the Rocky Mountain Sculpin (Cottus sp.). Conserv Genet 18:925–937CrossRefGoogle Scholar
  85. Sala-Bozano M, Ketmaier V, Mariani S (2009) Contrasting signals from multiple markers illuminate population connectivity in a marine fish. Mol Ecol 18:4811–4826PubMedCrossRefGoogle Scholar
  86. Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Fisheries Research Board of Canada, OttawaGoogle Scholar
  87. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629CrossRefGoogle Scholar
  88. Silver GS (2015) Investigations of larval Pacific lamprey Entosphenus tridentatus osmotic stress tolerance and occurrence in a tidally-influenced estuarine stream. M.S. thesis, Portland State University, Portland, OregonGoogle Scholar
  89. Spice EK, Whitesel TA, McFarlane CT, Docker MF (2011) Characterization of 12 microsatellite loci for the Pacific lamprey, Entosphenus tridentatus (Petromyzontidae), and cross-amplification in five other lamprey species. Genet Mol Res 10:3246–3250PubMedCrossRefGoogle Scholar
  90. Spice EK, Goodman DH, Reid SB, Docker MF (2012) Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey. Mol Ecol 21:2916–2930PubMedCrossRefGoogle Scholar
  91. United States Fish and Wildlife Service (2004) Endangered and threatened wildlife and plants; 90-day finding on a petition to list three species of lampreys as threatened or endangered. Fed Reg 69:77158–77167Google Scholar
  92. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  93. Vangestel C, Mergeay J, Dawson DA, Callens T, Vandomme V, Lens L (2012) Genetic diversity and population structure in contemporary house sparrow populations along an urbanization gradient. Heredity 109:163–172PubMedPubMedCentralCrossRefGoogle Scholar
  94. Waitt RB (1985) Case for periodic, colossal jökulhlaups from Pleistocene glacial Lake Missoula. Geol Soc Am Bull 96:1271–1286CrossRefGoogle Scholar
  95. Waldman J, Grunwald C, Wirgin I (2008) Sea lamprey Petromyzon marinus: an exception to the rule of homing in anadromous fishes. Biol Lett 4:659–662PubMedPubMedCentralCrossRefGoogle Scholar
  96. Wang C, Schaller H (2015) Conserving Pacific lamprey through collaborative efforts. Fisheries 40:72–79CrossRefGoogle Scholar
  97. Ward DL, Clemens BJ, Clugston D et al (2012) Translocating adult Pacific lamprey within the Columbia River basin: state of the science. Fisheries 37:351–361CrossRefGoogle Scholar
  98. Waters JM, Craw D, Youngson JH, Wallis GP (2001) Genes meet geology: fish phylogeographic pattern reflects ancient, rather than modern, drainage connections. Evolution 55:1844–1851PubMedCrossRefGoogle Scholar
  99. Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370PubMedGoogle Scholar
  100. White JL, Harvey BC (2003) Basin-scale patterns in the drift of embryonic and larval fishes and lamprey ammocoetes in two coastal rivers. Environ Biol Fish 67:369–378CrossRefGoogle Scholar
  101. Wu TH, Tsang LM, Chen IS, Chu KH (2016) Multilocus approach reveals cryptic lineages in the goby Rhinogobius duospilus in Hong Kong streams: role of paleodrainage systems in shaping marked population differentiation in a city. Mol Phylogenet Evol 104:112–122PubMedCrossRefGoogle Scholar
  102. Yamazaki Y, Yamano A, Oura K (2011a) Recent microscale disturbance of gene flow in threatened fluvial lamprey, Lethenteron sp. N, living in a paddy water system. Conserv Genet 12:1373–1377CrossRefGoogle Scholar
  103. Yamazaki Y, Yokoyama R, Nagai T, Goto A (2011b) Formation of a fluvial non-parasitic population of Lethenteron camtschaticum as the first step in petromyzontid speciation. J Fish Biol 79:2043–2059PubMedCrossRefGoogle Scholar
  104. Yamazaki Y, Yokoyama R, Nagai T, Goto A (2014) Population structure and gene flow among anadromous Arctic lamprey (Lethenteron camtschaticum) populations deduced from polymorphic microsatellite loci. Environ Biol Fish 97:43–52CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of ManitobaWinnipegCanada
  2. 2.Fisheries and Oceans CanadaWinnipegCanada
  3. 3.U.S. Fish & Wildlife Service, Columbia River Fish & Wildlife Conservation OfficeVancouverUSA
  4. 4.Oregon Department of Environmental Quality, Laboratory and Environmental Assessment DivisionHillsboroUSA

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