Hydrobiologia

, Volume 794, Issue 1, pp 223–240 | Cite as

Temporal genetic population structure and interannual variation in migration behavior of Pacific Lamprey Entosphenus tridentatus

  • Benjamin J. Clemens
  • Lance Wyss
  • Rebecca McCoun
  • Ian Courter
  • Lawrence Schwabe
  • Christopher Peery
  • Carl B. Schreck
  • Erin K. Spice
  • Margaret F. Docker
Primary Research Paper

Abstract

Studies using neutral loci suggest that Pacific lamprey, Entosphenus tridentatus, lack strong spatial genetic population structure. However, it is unknown whether temporal genetic population structure exists. We tested whether adult Pacific lamprey: (1) show temporal genetic population structure; and (2) migrate different distances between years. We non-lethally sampled lamprey for DNA in 2009 and 2010 and used eight microsatellite loci to test for genetic population structure. We used telemetry to record the migration behaviors of these fish. Lamprey were assignable to three moderately differentiated genetic clusters (F ST = 0.16–0.24 for all pairwise comparisons): one cluster was composed of individuals from 2009, and the other two contained individuals from 2010. The F ST value between years was 0.13 and between genetic clusters within 2010 was 0.20. A total of 372 (72.5%) fish were detected multiple times during their migrations. Most fish (69.9%) remained in the mainstem Willamette River; the remaining 30.1% migrated into tributaries. Eighty-two lamprey exhibited multiple back-and-forth movements among tributaries and the mainstem, which may indicate searching behaviors. All migration distances were significantly greater in 2010, when the amplitude of river discharge was greater. Our data suggest genetic structuring between and within years that may reflect different cohorts.

Keywords

Petromyzontiformes Temporal variation Anadromous Spawning migration 

Notes

Acknowledgements

Funding was provided by the Columbia River Inter-Tribal Fish Commission through the Columbia Basin Fish Accords partnership with the Bonneville Power Administration under project 2008-524-00 (Brian McIlraith, project manager). Flight surveys were funded by the U. S. Bureau of Reclamation. The project was also funded by the U.S. Fish and Wildlife Service Tribal Wildlife Grant and the Administration for Native Americans to the Confederated Tribes of the Grand Ronde. Shadia Duery provided significant assistance with the field research. Several individuals from the University of Idaho and Oregon State University provided technical assistance. L. Belonga, S. Starcevich, L. Schultz, and M. Falcy reviewed earlier drafts of this manuscript. Staff from Portland General Electric, Normandeau Associates, Inc., and the Confederated Tribes of the Warm Springs assisted with collection and radio-tagging of lamprey. Use of equipment, supplies, or computer software does not constitute endorsement. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Supplementary material

10750_2017_3096_MOESM1_ESM.docx (52 kb)
Supplementary material 1 (DOCX 51 kb)

References

  1. Aspinwall, N., 1974. Genetic analysis of North American populations of the pink salmon, Oncorhynchus gorbuscha, possible evidence for the neutral mutation-random drift hypothesis. Evolution 28: 295–305.CrossRefGoogle Scholar
  2. Beamish, R. J., 1980. Adult biology of the river lamprey (Lampetra ayresi) and the Pacific lamprey (Lampetra tridentata) from the Pacific coast of Canada. Canadian Journal of Fisheries and Aquatic Sciences 37: 1906–1923.CrossRefGoogle Scholar
  3. Beamish, R. J. & C. D. Levings, 1991. Abundance and freshwater migrations of the anadromous parasitic lamprey, Lampetra tridentata, in a tributary of the Fraser River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 48: 1250–1263.CrossRefGoogle Scholar
  4. Chapuis, M. P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621–631.CrossRefPubMedGoogle Scholar
  5. Clemens, B. J. & S. S. Crawford, 2009. Body size and depth distribution of bloater (Coregonus hoyi Gill) in the Laurentian Great Lakes: Patterns and hypotheses. Reviews in Fisheries Science 17: 174–186.CrossRefGoogle Scholar
  6. Clemens, B. J., T. R. Binder, M. F. Docker, M. L. Moser & S. A. Sower, 2010. Similarities, differences, and unknowns in biology and management of three parasitic lampreys of North America. Fisheries 35: 580–594.CrossRefGoogle Scholar
  7. Clemens, B. J., M. G. Mesa, R. J. Magie, D. A. Young & C. B. Schreck, 2012. Pre-spawning migration of adult Pacific lamprey, Entosphenus tridentatus, in the Willamette River, Oregon (USA). Environmental Biology of Fishes 93: 245–254.CrossRefGoogle Scholar
  8. Clemens, B. J., S. van de Wetering, S. A. Sower & C. B. Schreck, 2013. Maturation characteristics and life history strategies of the Pacific Lamprey, Entosphenus tridentatus. Canadian Journal of Zoology 91: 775–788.CrossRefGoogle Scholar
  9. Clemens, B. J., C. B. Schreck, S. A. Sower & S. J. van de Wetering, 2016. The potential roles of river environments in selecting for stream- and ocean-maturing Pacific Lamprey, Entosphenus tridentatus (Gairdner, 1836). In Orlov, A. M. & R. J. Beamish (eds.), Jawless fishes of the world. Chapman Hall, London: 299–322.Google Scholar
  10. Cooke, S. J., S. G. Hinch, M. Wikelski, R. D. Andrews, L. J. Kuchel, T. G. Wolcott & P. J. Butler, 2004. Biotelemetry: a mechanistic approach to ecology. Trends in Ecology & Evolution 19(6): 334–343.CrossRefGoogle Scholar
  11. Dawson, H., B. R. Quintella, P. R. Almeida, A. J. Treble & J. C. Jolley, 2015. The ecology of larval and metamorphosing lampreys. In Docker, M. F. (ed.), Lampreys: Biology, Conservation and Control, Vol. 1. Springer, New York: 75–138.Google Scholar
  12. Dingle, H. & A. Drake, 2007. What is migration? Bioscience 57: 113–121.CrossRefGoogle Scholar
  13. Docker, M. F., J. B. Hume & P. J. Clemens, 2015. Introduction: a surfeit of lampreys. In Docker, M. F. (ed.), Lampreys: Biology, Conservation, and Control. Springer, Dordrecht: 1–34.Google Scholar
  14. Earl, D. A. & B. M. vonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.CrossRefGoogle Scholar
  15. Fillatre, E. K., P. Etherton & D. D. Heath, 2003. Bimodal run distribution in a northern population of sockeye salmon (Oncorhynchus nerka): life history and genetic analysis on a temporal scale. Molecular Ecology 12: 1793–1805.CrossRefPubMedGoogle Scholar
  16. Gilmore, S. A. 2004. Genetic assessment of adult mating success and accuracy of statolith aging in the sea lamprey Petromyzon marinus. Master’s Thesis, Michigan State University.Google Scholar
  17. Goodman, D. H., S. B. Reid, M. F. Docker, G. R. Haas & A. P. Kinziger, 2008. Mitochondrial DNA evidence for high levels of gene flow among populations of a widely distributed anadromous lamprey Entosphenus tridentatus (Petromyzontidae). Journal of Fish Biology 72: 400–417.CrossRefGoogle Scholar
  18. Goudet, J., 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.CrossRefGoogle Scholar
  19. Goudet, J. & T. Jombart. 2015. hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-22. https://CRAN.R-project.org/package=hierfstat.
  20. Groot, C. & L. Margolis, 1991. Pacific Salmon Life Histories. University of British Columbia Press, Vancouver.Google Scholar
  21. Hendry, A. P. & T. Day, 2005. Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology 14: 901–916.CrossRefPubMedGoogle Scholar
  22. Hendry, A. P., J. K. Wenburg, P. Bentzen, E. C. Volk & T. P. Quinn, 2000. Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290: 516–518.CrossRefPubMedGoogle Scholar
  23. Hendry, M. A., J. K. Wenburg, K. W. Myers & A. P. Hendry, 2002. Genetic and phenotypic variation through the migratory season provides evidence for multiple populations of wild steelhead in the Dean River, British Columbia. Transactions of the American Fisheries Society 131: 418–434.CrossRefGoogle Scholar
  24. Hendry, A. P., V. Castric, M. T. Kinnison & T. P. Quinn, 2004. The evolution of philopatry and dispersal: homing versus straying in salmonids. In Hendry, A. P. & S. C. Stearns (eds.), Evolution illuminated: salmon and their relatives. Oxford University Press, Oxford: 52–91.Google Scholar
  25. Hess, J. E., N. R. Campbell, D. A. Close, M. F. Docker & S. R. Narum, 2013. Population genomics of Pacific lamprey: Adaptive variation in a highly dispersive species. Molecular Ecology 22: 2898–2916.CrossRefPubMedGoogle Scholar
  26. Hess, J. E., C. C. Caudill, M. L. Keefer, B. J. McIlraith, M. L. Moser & S. R. Narum, 2014. Genes predict long distance migration and large body size in a migratory fish, Pacific lamprey. Evolutionary Applications 7: 1192–1208.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hess, J. E., N. R. Campbell, M. F. Docker, C. Baker, A. Jackson, R. Lampman, B. McIlraith, M. L. Moser, D. P. Statler, W. P. Young, A. J. Wildbill & S. R. Narum, 2015. Use of genotyping by sequencing data to develop a high-throughput and multifunctional SNP panel for conservation applications in Pacific lamprey. Molecular Ecology Resources 15: 187–202.CrossRefPubMedGoogle Scholar
  28. Hinch, S. G., S. J. Cooke, M. C. Healey & A. P. Farrell, 2006. Behavioural physiology of fish migrations: salmon as a model approach. In Sloman, K., S. Balshine & R. Wilson (eds.), Fish physiology, Behaviour and physiology of fish, Vol. 24. Elsevier Press, New York: 239–295.CrossRefGoogle Scholar
  29. IDFG (Idaho Department of Fish and Game). 2011. The status of Pacific Lamprey (Entosphenus tridentatus) in Idaho. Boise, Idaho. July 2011. https://collaboration.idfg.idaho.gov/FisheriesTechnicalReports/mgt999-040Grunder2011%20The%20Status%20of%20Pacific%20Lamprey.pdf Accessed August 2016.
  30. Jackson, A. & M. Moser, 2012. Low-elevation dams are impediments to adult Pacific lamprey spawning migration in the Umatilla River, Oregon. North American Journal of Fisheries Management 32: 548–556.CrossRefGoogle Scholar
  31. Jakobsson, M. & N. A. Rosenberg, 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.CrossRefPubMedGoogle Scholar
  32. Johnson, E. L., C. C. Caudill, M. L. Keefer, T. S. Clabough, C. A. Peery, M. A. Jepson & M. L. Moser, 2012. Movement of radio-tagged adult Pacific lampreys during a large-scale fishway velocity experiment. Transactions of the American Fisheries Society 141: 571–579.CrossRefGoogle Scholar
  33. Johnson, N. S., T. J. Buchinger & W. Li, 2015. Reproductive ecology of lampreys. In Docker, M. F. (ed.), Lampreys: biology, conservation, and control. Springer, Dordrecht: 265–303.Google Scholar
  34. Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.CrossRefPubMedGoogle Scholar
  35. Jones, O.R. & J. Wang. 2010. COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources. 10:551–555.CrossRefPubMedGoogle Scholar
  36. Keefer, M. L., M. L. Moser, C. T. Boggs, W. R. Daigle & C. A. Peery, 2009a. Variability in migration timing of adult Pacific lamprey (Lampetra tridentata) in the Columbia River, U.S.A. Environmental Biology of Fishes 85: 253–264.CrossRefGoogle Scholar
  37. Keefer, M. L., M. L. Moser, C. T. Boggs, W. R. Daigle & C. A. Peery, 2009b. Effects of body size and river environment on the upstream migration of adult Pacific lampreys. North American Journal of Fisheries Management 29: 1214–1224.CrossRefGoogle Scholar
  38. Keefer, M. L., W. R. Daigle, C. A. Peery, H. T. Pennington, S. R. Lee & M. L. Moser, 2010. Testing adult Pacific lamprey performance at structural challenges in fishways. North American Journal of Fisheries Management 30: 376–385.CrossRefGoogle Scholar
  39. Keefer, M. L., C. A. Peery, S. R. Lee, W. R. Daigle, E. L. Johnson & M. L. Moser, 2011. Behaviour of adult Pacific lamprey in near-field flow and fishway design experiments. Fisheries Management and Ecology 18: 177–189.CrossRefGoogle Scholar
  40. Keefer, M. L., C. T. Boggs, C. A. Peery & C. C. Caudill, 2013. Factors affecting dam passage and upstream distribution of adult Pacific lamprey in the interior Columbia River basin. Ecology of Freshwater Fish 22: 1–10.CrossRefGoogle Scholar
  41. Lin, B., Z. Zhang, Y. Wang, K. P. Currens, A. Spidle, Y. Yamazaki & D. A. Close, 2008. Amplified fragment length polymorphism assessment of genetic diversity in Pacific lampreys. North American Journal of Fisheries Management 28: 1182–1193.CrossRefGoogle Scholar
  42. Lucas, M. C. & E. Baras, 2001. Migration of freshwater fishes. Blackwell Science Limited, Osney Mead.CrossRefGoogle Scholar
  43. Maes, G. E., J. M. Pujolar, B. Hellemans & F. A. M. Volckaert, 2006. Evidence for isolation by time in the European eel (Anguilla Anguilla L.). Molecular Ecology 15: 2095–2107.CrossRefPubMedGoogle Scholar
  44. McIlraith, B. J., C. C. Caudill, B. P. Kennedy, C. A. Peery & M. L. Keefer, 2015. Seasonal migration behaviors and distribution of adult Pacific Lampreys in unimpounded reaches of the Snake River Basin. North American Journal of Fisheries Management 35: 123–134.CrossRefGoogle Scholar
  45. McKeown, B. A., 1984. Fish migration. Croom Helm, London.Google Scholar
  46. Mehner, T., 2012. Diel vertical migration of freshwater fishes—proximate triggers, ultimate causes and research perspectives. Freshwater Biology 57: 1342–1359.CrossRefGoogle Scholar
  47. Mesa, M. G., R. J. Magie & E. S. Copeland, 2010. Passage and behavior of radio-tagged adult Pacific lamprey (Entosphenus tridentatus) at the Willamette Falls Project, Oregon. Northwest Science 84: 233–242.CrossRefGoogle Scholar
  48. Mesa, M. G., R. J. Magie, E. S. Copeland & H. E. Christiansen, 2011. Surgical wound healing in radio-tagged adult Pacific lamprey Entosphenus tridentatus held on different substrata. Journal of Fish Biology 79: 1068–1075.CrossRefPubMedGoogle Scholar
  49. Moser, M. L., A. L. Matter, L. C. Stuehrenberg & T. C. Bjornn, 2002. Use of An extensive radio receiver network to document Pacific lamprey (Lampetra tridentata) entrance efficiency at fishways in the lower Columbia River. Hydrobiologia 483: 45–53.CrossRefGoogle Scholar
  50. Moser, M. L., D. A. Ogden & B. P. Sandford, 2007. Effects of surgically implanted transmitters on anguilliform fishes: lessons from lamprey. Journal of Fish Biology 71: 1847–1852.CrossRefGoogle Scholar
  51. Moser, M. L., P. R. Almeida, P. S. Kemp & P. W. Sorensen, 2015. Lamprey spawning migration. In Docker, M. F. (ed.), Lampreys: Biology, Conservation, and Control. Springer, Dordrecht: 215–263.Google Scholar
  52. Murauskas, J. G., A. M. Orlov & K. A. Siwicke, 2013. Relationships between the abundance of Pacific Lamprey in the Columbia River and their common hosts in the marine environment. Transactions of the American Fisheries Society 142: 143–155.CrossRefGoogle Scholar
  53. Northrup, J. M., A. B. A. Shafer, C. R. Anderson Jr., D. W. Coltman & G. Wittemyer, 2014. Fine-scale genetic correlates to condition and migration in a wild cervid. Evolutionary Applications 7: 937–948.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  55. Quinn, T. P., 2005. The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle.Google Scholar
  56. Quinn, T. P. & K. W. Myers, 2004. Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. Reviews in Fish Biology and Fisheries 14: 421–442.CrossRefGoogle Scholar
  57. R Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
  58. Raymond, M. & F. Rousset, 1995. An exact test for population differentiation. Evolution 49: 1280–1283.CrossRefGoogle Scholar
  59. Robinson, T. C. & J. M. Bayer, 2005. Upstream migration of Pacific lampreys in the John Day River, Oregon: behavior, timing, and habitat use. Northwest Science 79: 106–119.Google Scholar
  60. Rougemont, Q., A. Gaigher, E. Lasne, J. Côte, M. Coke, A.-L. Besnard, S. Launey & G. Evanno, 2015. Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation by European river and brook lampreys. Journal of Evolutionary Biology 28: 2248–2263.CrossRefPubMedGoogle Scholar
  61. Rosenberg, N. A., 2004. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138.CrossRefGoogle Scholar
  62. Rousset, F., 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106.CrossRefPubMedGoogle Scholar
  63. Scott, W. B. & E. J. Crossman. 1973. Freshwater fishes of Canada. Fisheries Research Board of Canada: Ottawa, Bulletin 184.Google Scholar
  64. Sorensen, P. W., et al., 2005. Mixture of new sulfated steroids function as a migratory pheromone in the sea lamprey. Nature Chemical Biology 1: 324–328.CrossRefPubMedGoogle Scholar
  65. Sorensen, P. W. & T. R. Hoye, 2007. A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus L. Journal of Fish Biology 71: 100–114.CrossRefGoogle Scholar
  66. Spice, E. K., T. A. Whitesel, C. T. McFarlane & M. F. Docker, 2011. Characterization of twelve microsatellite loci for the Pacific lamprey, Entosphenus tridentatus (Petromyzontidae), and cross-amplification in five other lamprey species. Genetics and Molecular Research 10: 3246–3250.CrossRefPubMedGoogle Scholar
  67. Spice, E. K., D. H. Goodman, S. B. Reid & M. F. Docker, 2012. Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggest lack of natal homing but limits to dispersal in Pacific lamprey. Molecular Ecology 21: 2916–2930.CrossRefPubMedGoogle Scholar
  68. Starcevich, S. J., S. L. Gunckel & S. E. Jacobs, 2013. Movements, habitat use, and population characteristics of adult Pacific lamprey in a coastal river. Environmental Biology of Fishes. doi: 10.1007/s10641-013-0196-5.Google Scholar
  69. van Oosterhout, C., W. F. Hutchinson, D. P. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  70. Wagner, C. M., M. B. Twohey & J. M. Fine, 2009. Conspecific cueing in the sea lamprey: do reproductive migrations consistently follow the most intense larval odour? Animal Behaviour 78: 593–599.CrossRefGoogle Scholar
  71. Waldman, J., C. Grunwald & I. Wirgin, 2008. Sea lamprey Petromyzon marinus: an exception to the rule of homing in anadromous fishes. Biology Letters 4: 659–662.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Benjamin J. Clemens
    • 1
    • 2
    • 3
  • Lance Wyss
    • 1
    • 4
  • Rebecca McCoun
    • 5
    • 6
  • Ian Courter
    • 7
    • 8
  • Lawrence Schwabe
    • 5
  • Christopher Peery
    • 7
    • 9
  • Carl B. Schreck
    • 10
  • Erin K. Spice
    • 11
  • Margaret F. Docker
    • 11
  1. 1.Department of Fisheries and Wildlife104 Nash Hall Oregon State UniversityCorvallisUSA
  2. 2.Department of MicrobiologyOregon State UniversityCorvallisUSA
  3. 3.Oregon Department of Fish and WildlifeCorvallisUSA
  4. 4.The Freshwater TrustAshlandUSA
  5. 5.Natural Resources DepartmentThe Confederated Tribes of Grand RondeGrand RondeUSA
  6. 6.North Santiam Watershed CouncilStaytonUSA
  7. 7.Cramer Fish SciencesGreshamUSA
  8. 8.Mount Hood EnvironmentalBoringUSA
  9. 9.U.S. Fish and Wildlife Service, Idaho Fisheries Research OfficeOrofinoUSA
  10. 10.U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife104 Nash Hall Oregon State UniversityCorvallisUSA
  11. 11.Department of Biological SciencesUniversity of ManitobaWinnipegCanada

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