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Hydrobiologia

, Volume 783, Issue 1, pp 269–281 | Cite as

Contrasting levels of strays and contemporary gene flow among anadromous populations of Arctic charr, Salvelinus alpinus (L.), in northern Norway

  • Aintzane Santaquiteria
  • Martin-A. Svenning
  • Kim PræbelEmail author
CHARR II

Abstract

Arctic charr, Salvelinus alpinus (L.), occur as anadromous, resident, and landlocked populations within their circumpolar distribution. While resident Arctic charr reside in freshwater their entire life, anadromous Arctic charr migrate to sea in the summer due to the increased resource availability, but return to freshwater to overwinter and/or spawn. The migratory behaviour in Arctic charr is generally restricted to the northern range of their distribution area. The objective of this study was to estimate the amount of straying and contemporary gene flow among anadromous Arctic charr from eight river systems in northern Norway to illuminate the role of straying for the contemporary genetic stability of the populations. The results revealed that Arctic charr frequently stray among watercourses, especially among those in close geographical proximity, although strays were found nearly 500 km from their river of origin. While straying was revealed among six river systems, the results also revealed limited or no contemporary gene flow among the nine populations identified in the eight sampled river systems. The study also shows that Arctic charr may be a potential host for spreading diseases and parasites among watercourses.

Keywords

Arctic charr Salmonids Anadromy Straying Gene flow Local adaptation 

Notes

Acknowledgments

We would like to thank Helene Hodal Lødemel and Shripathi Bhat for assistance in the laboratory and with bioinformatic assistance, respectively. Jenny Stien is acknowledged for improving the English, and Øyvind Kanstad-Hanssen, Narve Johansen, and Trond Johansen for their field assistance. We also thank three anonymous reviewers and guest Editor Colin Adams for useful comments on previous versions of the manuscript.

Supplementary material

10750_2016_2905_MOESM1_ESM.docx (114 kb)
Supplementary material 1 (DOCX 114 kb)

References

  1. Antao, T., A. Lopes, R. J. Lopes, A. Beja-Pereira & G. Luikart, 2008. LOSITAN: a workbench to detect molecular adaptation based on a FST-outlier method. BioMed Central Ltd 9: 323.Google Scholar
  2. Berg, O. K. & M. Berg, 1989. Sea growth and time of migration anadromous Arctic charr (Salvelinus alpinus) from the Vardnes River, in northern Norway. Canadian Journal of Fisheries and Aquatic Sciences 46: 955–960.CrossRefGoogle Scholar
  3. Berg, O. K. & B. Jonsson, 1989. Migratory patterns of anadromous Atlantic salmon, brown trout, and Arctic charr from the Vardnes River in northern Norway. In Brannon, E. & B. Jonsson (eds), Proceedings of the salmonid migration and distribution symposium. School of Fisheries, University of Washington, Seattle: 106–115.Google Scholar
  4. Berg, O. K. & B. Jonsson, 1990. Growth and survival rates of the anadromous trout, Salmo trutta from the Vardnes River northern Norway. Environmental Biology of Fishes 29: 145–154.CrossRefGoogle Scholar
  5. Black, G. A., 1981. Metazoan parasites as indicators of movements of anadromous brook char (Salvelinus fontinalis) to sea. Canadian Journal of Zoology 59: 1892–1896.CrossRefGoogle Scholar
  6. Bouillon, R. & B. Dempson, 1989. Metazoan parasite infection in landlocked and anadromous Arctic charr (Salvelinus alpinus Linnaeus), and their use as indicators of movement to sea in young anadromous charr. Canadian Journal of Zoology 67: 2478–2485.CrossRefGoogle Scholar
  7. Crane, P. A., C. J. Lewis, E. J. Kretschmer, S. J. Miller, W. J. Spearman, A. L. DeCicco, M. J. Lisac & J. K. Wenburg, 2004. Characterization and inheritance of seven microsatellite loci from Dolly Varden, Salvelinus malma, and cross-species amplification in Arctic char, S. alpinus. Conservation Genetics 5: 737–741.CrossRefGoogle Scholar
  8. Dehaan, P. W. & W. R. Ardren, 2005. Characterization of 20 highly variable tetranucleotide microsatellite loci for bull trout (Salvelinus confluentus) cross-amplification in other Salvelinus species. Molecular Ecology Notes 5: 582–585.CrossRefGoogle Scholar
  9. Dempson, J. B. & A. H. Kristoffersen, 1987. Spatial and temporal aspects of the ocean migration of anadromous Arctic charr. American Fisheries Society Symposium 1: 340–357.Google Scholar
  10. Dick, T. A., 1984. Parasites and Arctic charr management—An academic curiosity or practical reality? In Johnson, L. & B. L. Burns (eds), Biology of the Arctic charr, Proceedings of the International Symposium on Arctic Charr. University of Manitoba Press, Winnipeg: 371–394.Google Scholar
  11. Dick, T. A. & M. Belosevic, 1981. Parasites of Arctic charr Salvelinus alpinus (Linnaeus) and their use in separating sea-run and non-migrating charr. Journal of Fish Biology 18: 339–347.CrossRefGoogle Scholar
  12. Dionne, M., F. Caron, J. Dodson & L. Bernatchez, 2008. Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Molecular Ecology 17: 2382–2396.CrossRefPubMedGoogle Scholar
  13. Dionne, M., F. Caron, J. J. Dodson & L. Bernatchez, 2009. Comparative survey of within-river genetic structure in Atlantic salmon; relevance for management and conservation. Conservation Genetics 10: 869–879.CrossRefGoogle Scholar
  14. Dodson, J. J., N. Aubin-Horth, V. Thériault & D. J. Páez, 2013. The evolutionary ecology of alternative migratory tactics in salmonid fishes. Biology Review 88: 602–625.CrossRefGoogle Scholar
  15. Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite v 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.CrossRefPubMedGoogle Scholar
  16. Finstad, B., 1993. Økologiske og fysiologiske konsekvenser av lus på laksefisk i fjordsystem. NINA. Oppdragsmelding 213: 1–18 (In Norwegian).Google Scholar
  17. Gross, M. R., R. M. Coleman & R. M. McDowall, 1988. Aquatic productivity and the evolution of diadromous fish migration. Science 239: 1291–1293.CrossRefPubMedGoogle Scholar
  18. Gyselman, E. C., 1984. The seasonal movements of anadromous Arctic charr at Nauyuk Lake, Northwest Territories, Canada. In Johnson, L. & B. L. Burns (eds), Biology of the Arctic charr. University of Manitoba Press, Winnipeg: 575–578.Google Scholar
  19. Hendry, A. P., V. Castric, M. T. Kinnison & T. P. Quinn, 2004. The evolution of phylopatry and dispersal: Homing versus straying in Salmonids. In Hendry, A. P. & S. Stearns (eds), Evolution Illuminated: Salmon and their relatives. Oxford University Press, Oxford: 52–91.Google Scholar
  20. Hubisz, M. J., D. Falush, M. Stephens & J. K. Pritchard, 2009. Inferring wear population structure with the assistance of sample group information. Molecular Ecology Resources 9: 1322–1332.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hutchings, J. A. & R. A. Myers, 1988. Mating success of alternative maturation phenotypes in Atlantic salmon, Salmo salar. Oecologia 75: 169–174.CrossRefGoogle Scholar
  22. Jensen, K. W. & M. Berg, 1977. Growth, mortality and migrations of the anadromous char, Salvelinus alpinus L., in the Vardnes River, Troms, northern Norway. Report of the Institute of Freshwater Research, Drottningholm 56: 70–80.Google Scholar
  23. Jensen, J. L. A. & A. H. Rikardsen, 2012. Archival tags reveal that Arctic charr Salvelinus alpinus and brown trout Salmo trutta can use estuarine and marine waters during winter. Journal of Fish Biology 81: 735–749.CrossRefPubMedGoogle Scholar
  24. Jensen, A. J., O. H. Diserud, B. Finstad, P. Fiske & A. H. Rikardsen, 2015. Between-watershed movements of two anadromous salmonids in the Arctic. Canadian Journal of Fisheries and Aquatic Sciences 46: 955–960.Google Scholar
  25. Johnson, L., 1989. The anadromous Arctic charr, Salvelinus alpinus of Nauyuk Lake, Northwest Territories, Canada. Physiology and Ecology Japan 1: 201–228.Google Scholar
  26. Jonsson, B. & N. Jonsson, 1993. Partial migration: niche shift versus sexual maturation in fishes. Reviews in Fish Biology and Fisheries 3: 348–365.CrossRefGoogle Scholar
  27. Jonsson, B. & N. Jonsson, 2011. Ecology of Atlantic salmon and brown trout: Habitat as a template for life histories. Springer, Dordrecht: 247–345.CrossRefGoogle Scholar
  28. Kalinowski, S. T., 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5: 187–189.CrossRefGoogle Scholar
  29. Keefer, M. L. & C. C. Caudill, 2014. Homing and straying by anadromous salmonids: a review of mechanisms and rates. Reviews in Fish Biology and Fisheries 24: 333–368.CrossRefGoogle Scholar
  30. Kennedy, C., 1977. Distribution and zoogeographical characteristics of parasite fauna of char Salvelinus alpinus in Arctic Norway, including Spitsbergen and Jan Mayen islands. Astarte 10: 49–55.Google Scholar
  31. Klemetsen, A., P. A. Amundsen, J. B. Dempson, B. Jonsson, N. Jonsson, M. F. O’Connell & E. Mortensen, 2003. Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12: 1–59.CrossRefGoogle Scholar
  32. Kristoffersen, R., 1988. A new species of parasite on Arctic charr, Salvelinus alpinus (L.), in seawater cages in Scandinavia. Aquaculture 71: 187–191.CrossRefGoogle Scholar
  33. Kristoffersen, K., 1994. The influence of physical watercourse parameters of the degree of anadromy in different lake populations of Arctic charr (Salvelinus alpinus (L.)) in northern Norway. Ecology Freshwater Fish 3: 80–91.CrossRefGoogle Scholar
  34. Kristoffersen, K., M. Halvorse & L. Jørgensen, 1994. Influence of parr growth, lake morphology, and freshwater parasites on the degree of anadromy in different populations of Arctic char (Salvelinus alpinus) in northern Norway. Canadian Journal of Fisheries and Aquatic Sciences 46: 955–960.Google Scholar
  35. Mathisen, O. A. & M. Berg, 1968. Growth rates of the char, Salvelinus alpinus (L.) in the Vardnes River, Troms, northern Norway. Report of the Institute of Freshwater Research, Drottningholm 48: 177–186.Google Scholar
  36. McGowan, C. R., E. A. Davidson, R. A. Woram, R. G. Danzmann, M. M. Ferguson & W. S. Davidson, 2004. Ten polymorphic microsatellite markers from Arctic charr (Salvelinus alpinus): linkage analysis and amplification in other salmonids. Animal Genetics 35: 479–481.CrossRefPubMedGoogle Scholar
  37. McLean, P. H., G. W. Smith & M. J. Wilson, 1990. Residence time of the sea louse, Lepophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water. Journal of Fish Biology 37: 311–314.CrossRefGoogle Scholar
  38. Moore, J. S., L. N. Harris, R. F. Tallman & E. B. Taylor, 2013. The interplay between dispersal and gene flow in anadromous Arctic char (Salvelinus alpinus): implications for potential for local adaptation. Canadian Journal of Fisheries and Aquatic Sciences 70: 1327–1338.CrossRefGoogle Scholar
  39. Newman, D. & D. A. Tallmon, 2001. Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conservation Biology 15: 1054–1063.CrossRefGoogle Scholar
  40. Nordeng, H., 1983. Solution to the ‘charr problem’ based on Arctic charr (Salvelinus alpinus) in Norway. Canadian Journal of Fisheries and Aquatic Sciences 40: 372–1387.CrossRefGoogle Scholar
  41. Nordeng, H. & L. Knivestøen, 1985. Coexisting forms of Arctic char Salvelinus alpinus (L.) in Norwegian river systems. ISAFC Information Series 3: 118–124.Google Scholar
  42. Paetkau, D., W. Calvert, I. Stirling & C. Strobeck, 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4: 347–354.CrossRefPubMedGoogle Scholar
  43. Paetkau, D., R. Slade, M. Burden & A. Estoup, 2004. Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Molecular Ecology 13: 55–65.CrossRefPubMedGoogle Scholar
  44. Peakall, R. & P. E. Smouse, 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28: 2537–2539.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Perry, G. M. L., T. L. King, J. Cyr, M. Valcourt & L. Bernatchez, 2005. Isolation and cross-familial amplification of 41 microsatellites for the brook charr (Salvelinus fontinalis). Molecular Ecology Notes 5: 346–351.CrossRefGoogle Scholar
  46. Piry, S., A. Alapetite, J. M. Cornuet, D. Paetkau, L. Baudouin & A. Estoup, 2004. GeneClass2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95: 536–539.CrossRefPubMedGoogle Scholar
  47. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  48. Quinn, T. P., 1993. A review of homing and straying of wild and hatchery-produced salmon. Fisheries Research 18: 29–44.CrossRefGoogle Scholar
  49. Radtke, R., M. A. Svenning, D. Malone, A. Klemetsen, J. Ruzicka & D. Fey, 1996. Migrations in an extreme northern population of Arctic charr, Salvelinus alpinus: insights from otolith microchemistry. Marine Ecology Progress Series 136: 13–23.CrossRefGoogle Scholar
  50. Rannala, B. & J. L. Mountain, 1997. Detecting immigration by using multilocus genotypes. Proceedings National Academy Sciences USA 94: 9197–9221.CrossRefGoogle Scholar
  51. Rexroad, C. E., R. L. Coleman, W. K. Hershberger & J. Killefer, 2002. Thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. Journal of Animal Science 80: 541–542.CrossRefPubMedGoogle Scholar
  52. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.CrossRefGoogle Scholar
  53. Rikardsen, A. H., M. A. Svenning & A. Klemetsen, 1997. Variations in juvenile growth, energy allocation and life-history strategies of two populations of Arctic charr in north Norway. Journal of Fish Biology 51: 447–461.CrossRefGoogle Scholar
  54. Rousset, F., 2008. Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106.CrossRefPubMedGoogle Scholar
  55. Sindermann, C. J. & A. E. Farrin, 1962. Ecological studies of Cryptocotyle lingua (Trematoda: Heterophyidae) whose larvae cause “pigment spots” of marine fish. Ecology 43: 69–75.CrossRefGoogle Scholar
  56. Skaala, Ø., B. Høyheim, K. A. Glover & G. Dahle, 2004. Microsatellite analysis in domesticated and wild Atlantic salmon (Salmo salar L.): allelic diversity and identification of individuals. Aquaculture 240: 131–143.CrossRefGoogle Scholar
  57. Svenning, M. A. & N. Gullestad, 2002. Adaptations to stochastic environmental variations: the effects of seasonal temperatures on the migratory window of Svalbard Arctic charr. Environmental Biology of Fishes 64: 165–174.CrossRefGoogle Scholar
  58. Svenning, M. A., A. Smith-Nilsen & M. Jobling, 1992. Sea water migration of Arctic charr (Salvelinus alpinus L.); correlation between freshwater growth and seaward migration, based on back-calculation from otoliths. Nordic Journal of Freshwater Resources 67: 18–26.Google Scholar
  59. Svenning, M. A., A. Klemetsen & T. Olsen, 2007. Habitat and food choice of Arctic charr in Linne´vatn on Spitsbergen, Svalbard: the first year-round investigation in a High Arctic lake. Ecology of Freshwater Fish 16: 70–77.CrossRefGoogle Scholar
  60. Svenning, M. A., K. Præbel, Ø. Kanstad-Hanssen & M. Falkegård, 2013. Anadromous Arctic charr; ecological or genetic segregation? NINA Report 957: 19 pp (in Norwegian).Google Scholar
  61. Tallman, R. F. & M. C. Healey, 1994. Homing, straying, and gene flow among seasonally separated populations of chum salmon (Oncorhynchus keta). Canadian Journal of Fish Aquatic Science 51: 577–588.CrossRefGoogle Scholar
  62. Vähä, J. P., J. Erkinaro, E. Niemelä & C. R. Primmer, 2007. Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Molecular Ecology 16: 2638–2654.CrossRefPubMedGoogle Scholar
  63. Wilson, G. A. & B. Rannala, 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177–1191.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Aintzane Santaquiteria
    • 1
  • Martin-A. Svenning
    • 2
  • Kim Præbel
    • 1
    Email author
  1. 1.Norwegian College of Fishery ScienceUiT The Arctic University of NorwayTromsøNorway
  2. 2.Arctic Ecology Department, Fram CenterNorwegian Institute for Nature Research (NINA)TromsøNorway

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