Invasion genetics of vendace (Coregonus albula (L.)) in the Inari-Pasvik watercourse: Revealing the origin and expansion pattern of a rapid colonization event

Ecology and Evolution

Volumn 3, Issue 5, 2013, Pages 1400-1412

  Præbel, Kim ^a,c   Gjelland, Karl Øystein ^a   Salonen, Erno ^b   Amundsen, Per Arne ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Biological invasions; Effective population size; Exotic species; Genetic bottleneck; Rapid divergence

Indexed keywords

EID: 84886299228     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.552     Document Type: Article

References (94)

1. Allan, J. D., and A. S. Flecker 1993. Biodiversity conservation in running waters. Bioscience 43:32-43.
2. Amundsen, P. A., F. J. Staldvik, Y. S. Reshetnikov, N. Kashulin, A. Lukin, T. Bøhn, et al. 1999. Invasion of vendace Coregonus albula in a subarctic watercourse. Biol. Conserv. 88:405-413.
3. Amundsen, P. A., T. Bøhn, O. A. Popova, F. J. Staldvik, Y. S. Reshetnikov, N. A. Kashulin, et al. 2003. Ontogenetic niche shifts and resource partitioning in a subarctic piscivore fish guild. Hydrobiologia 497:109-119.
4. Amundsen, P. A., E. Salonen, T. Niva, K. O. Gjelland, K. Præbel, O. T. Sandlund, et al. 2012. Invader population speeds up life history during colonization. Biol. Invasions 14:1501-1513.
5. Ayres, R. M., V. J. Pettigrove, and A. A. Hoffmann 2010. Low diversity and high levels of population genetic structuring in introduced eastern mosquitofish (Gambusia holbrooki) in the greater Melbourne area, Australia. Biol. Invasions 12:3727-3744.
6. Bacigalupe, L. D. 2009. Biological invasions and phenotypic evolution: a quantitative genetic perspective. Biol. Invasions 11:2243-2250.
7. Bell, K. C., and M. D. Matocq 2011. Regional genetic subdivision in the Mohave ground squirrel: evidence of historic isolation and ongoing connectivity in a Mojave desert endemic. Anim. Conserv. 14:371-381.
8. Bernatchez, L., S. Renaut, A. R. Whiteley, N. Derome, J. Jeukens, L. Landry, et al. 2010. On the origin of species: insights from the ecological genomics of lake whitefish. Philos. Trans. R. Soc. B Biol. Sci. 365:1783-1800.
9. Blanchet, S. 2012. The use of molecular tools in invasion biology: an emphasis on freshwater ecosystems. Fish. Manage. Ecol. 19:120-132.
10. Bøhn, T., and P. A. Amundsen 1998. Effects of invading vendace (Coregonus albula L.) on species composition and body size in two zooplankton communities of the Pasvik river system, northern Norway. J. Plankton Res. 20:243-256.
11. Bøhn, T., and P. A. Amundsen 2001. The competitive edge of an invading specialist. Ecology 82:2150-2163.
12. Bøhn, T., O. T. Sandlund, P. A. Amundsen, and R. Primicerio 2004. Rapidly changing life history during invasion. Oikos 106:138-150.
13. Bøhn, T., P.-A. Amundsen, and A. Sparrow 2008. Competitive exclusion after invasion? Biol. Invasions 10:359-368.
14. Brown, J. E., and C. A. Stepien 2009. Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Mol. Ecol. 18:64-79.
15. Colautti, R. I., I. A. Grigorovich, and H. J. MacIsaac 2006. Propagule pressure: a null model for biological invasions. Biol. Invasions 8:1023-1037.
16. Cornuet, J. M., and G. Luikart 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001-2014.
17. Davis, M. A. 2009. Invasion biology. Oxford University Press, Oxford.
18. DeWoody, J. A., and J. C. Avise 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol. 56:461-473.
19. Dlugosch, K. M., and I. M. Parker 2008a. Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol. Lett. 11:701-709.
20. Dlugosch, K. M., and I. M. Parker 2008b. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17:431-449.
21. Driscoll, D. A., A. Felton, P. Gibbons, A. M. Felton, N. T. Munro, and D. B. Lindenmayer 2012. Priorities in policy and management when existing biodiversity stressors interact with climate-change. Clim. Change 111:533-557.
22. Earl, D. A., and B. M. vonHoldt 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359-361.
23. Estoup, A., and T. Guillemaud 2010. Reconstructing routes of invasion using genetic data: why, how and so what? Mol. Ecol. 19:4113-4130.
24. Excoffier, L., and H. E. L. Lischer 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564-567.
25. Facon, B., B. J. Genton, J. Shykoff, P. Jarne, A. Estoup, and P. David 2006. A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol. Evol. 21:130-135.
26. Facon, B., J.-P. Pointier, P. Jarne, V. Sarda, and P. David 2008. High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr. Biol. 18:363-367.
27. Geller, J. B., J. A. Darling, and J. T. Carlton 2010. Genetic perspectives on marine biological invasions. Ann. Rev. Mar. Sci. 2:367-393.
28. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394-407.
29. Gjelland, K. Ø., T. Bøhn, and P. A. Amundsen 2007. Is coexistence mediated by microhabitat segregation? An in-depth exploration of a fish invasion. J. Fish Biol. 71:196-209.
30. Golubtsov, B. A. S., I. I. Ilyin, and M. V. Mina 1993. Polymorphisms at two enzyme loci (Sod and Odh) in populations of the Amur sleeper, Perccottus glenii (Pisces, Eleotrididae), from its native range and the colonized area: the effect of introduction on genetic variation. J. Zoolog. Syst. Evol. Res. 31:269-279.
31. Guo, S. W., and E. A. Thompson 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361-372.
32. Gutowsky, L. F. G., and M. G. Fox 2012. Intra-population variability of life-history traits and growth during range expansion of the invasive round goby, Neogobius melanostomus. Fish. Manage. Ecol. 19:78-88.
33. Hedrick, P. W. 2000. Genetics of populations. Jones and Bartlett Publishers, Sudbury, MA.
34. Henry, P., G. Le Lay, J. Goudet, A. Guisan, S. Jahodova, and G. Besnard 2009. Reduced genetic diversity, increased isolation and multiple introductions of invasive giant hogweed in the western Swiss Alps. Mol. Ecol. 18:2819-2831.
35. Hewitt, G. M. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58:247-276.
36. Hubisz, M. J., D. Falush, M. Stephens, and J. K. Pritchard 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9:1322-1332.
37. Ibrahim, K. M., R. A. Nichols, and G. M. Hewitt 1996. Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282-291.
38. Kalinowski, S. T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5:187-189.
39. Knutsen, H., P. E. Jorde, C. Andre, and N. C. Stenseth 2003. Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Mol. Ecol. 12:385-394.
40. Kolbe, J. J., R. E. Glor, L. R. G. Schettino, A. C. Lara, A. Larson, and J. B. Losos 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177-181.
41. Langella, O. 2005. Populations, a free population genetic software (1999-2005). Available at http://bioinformatics.org/project/?group_id=84 (accessed February 13, 2011).
42. Lavergne, S., and J. Molofsky 2007. Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc. Natl. Acad. Sci. USA 104:3883-3888.
43. Lee, C. E. 2002. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17:386-391.
44. Lockwood, J. L., P. Cassey, and T. Blackburn 2005. The role of propagule pressure in explaining species invasions. Trends Ecol. Evol. 20:223-228.
45. Lodge, D. M. 1993. Biological invasions - lessons for ecology. Trends Ecol. Evol. 8:133-137.
46. Luikart, G., and J. M. Cornuet 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12:228-237.
47. Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10:689-710.
48. Mariani, S., W. F. Hutchinson, E. M. C. Hatfield, D. E. Ruzzante, E. J. Simmonds, T. G. Dahlgren, et al. 2005. North Sea herring population structure revealed by microsatellite analysis. Mar. Ecol. Prog. Ser. 303:245-257.
49. Mooney, H. A., and R. J. Hobbs 2000. Invasive species in a changing world. Island Press, Washington, DC.
50. Moyle, P. B. 1986. Fish introductions into North America. Pp. 27-43 in H. A. Mooney and J. A. Drake, eds. Ecology of biological invasions of North America and Hawaii. Springer Verlag, New York.
51. Mutenia, A., and E. Salonen 1992. The vendace (Coregonus albula L.), a new species in the fish community and fisheries of Lake Inari. Pol. Arch. Hydrobiol. 39:797-805.
52. Nei, M., T. Maruyama, and R. Chakraborty 1975. Bottleneck effect and genetic variability in populations. Evolution 29:1-10.
53. Nei, M., F. Tajima, and Y. Tateno 1983. Accuracy of estimated phylogenetic trees from molecular-data. 2. Gene-frequency data. J. Mol. Evol. 19:153-170.
54. Novak, S. J., and R. N. Mack 2005. Genetic bottlenecks in alien plant species: influences of mating systems and introduction dynamics. Pp. 201-228 in D. F. Sax, J. J. Stachowicz, and S. D. Gaines, eds. Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland.
55. Olden, J. D., and N. L. Poff 2004. Ecological processes driving biotic homogenization: testing a mechanistic model using fish faunas. Ecology 85:1867-1875.
56. Olden, J. D., and T. P. Rooney 2006. On defining and quantifying biotic homogenization. Glob. Ecol. Biogeogr. 15:113-120.
57. Østbye, K., P. A. Amundsen, L. Bernatchez, A. Klemetsen, R. Knudsen, R. Kristoffersen, et al. 2006. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol. Ecol. 15:3983-4001.
58. Page, R. D. M. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
59. Parker, I. M., D. Simberloff, W. M. Lonsdale, K. Goodell, M. Wonham, P. M. Kareiva, et al. 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1:3-19.
60. Peakall, R., and P. E. Smouse 2006. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288-295.
61. Peterson, D. P., K. D. Fausch, and G. C. White 2004. Population ecology of an invasion: effects of brook trout on native cutthroat trout. Ecol. Appl. 14:754-772.
62. Pimentel, D., L. Lach, R. Zuniga, and D. Morrison 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53-65.
63. Præbel, K., J.-I. Westgaard, S.-E. Fevolden, and J. S. Christiansen 2008. Circumpolar genetic population structure of capelin, Mallotus villosus. Mar. Ecol. Prog. Ser. 360:189-199.
64. Præbel, K., J.-I. Westgaard, P.-A. Amundsen, A. Siwertsson, R. Knudsen, K. K. Kahilainen, et al. in press. A diagnostic tool for efficient analysis of population structure, hybridization and conservation status of European whitefish (Coregonus lavaretus (L.)) and vendace (C. albula (L.)). Adv. Limnol. (in press).
65. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
66. Rahel, F. J. 2000. Homogenization of fish faunas across the United States. Science 288:854-856.
67. Rahel, F. J. 2002. Homogenization of freshwater faunas. Annu. Rev. Ecol. Syst. 33:291-315.
68. Reusch, T. B. H., S. Bolte, M. Sparwel, A. G. Moss, and J. Javidpour 2010. Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world's most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Mol. Ecol. 19:2690-2699.
69. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
70. Rousset, F. 2007. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8:103-106.
71. Saisa, M., J. Ronn, T. Aho, M. Bjorklund, P. Pasanen, and M. L. Koljonen 2008. Genetic differentiation among European whitefish ecotypes based on microsatellite data. Hereditas 145:69-83.
72. Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32:305-332.
73. Salonen, E. 1998. The vendace stock and fisheries in lake Inari. Boreal Environ. Res. 3:307-319.
74. Salonen, E. 2004. Estimation of vendace year-class strength with different methods in the subarctic lake Inari. Ann. Zool. Fenn. 41:249-254.
75. Salonen, E., P.-A. Amundsen, and T. Bøhn 2007. Boom and bust development by invading vendace Coregonus albula in the subarctic lnari-Pasvik watershed (Finland, Norway and Russia). Adv. Limnol. 60:331-342.
76. Sandlund, O. T. 1992. Differences in the ecology of two vendace populations separated in 1895. Nord. J. Freshw. Res. 67:52-60.
77. Sandlund, O. T., P. J. Schei, and Å. Viken 1999. Invasive species and biodiversity management. Kluwer Academic Publishers, Dordrecht, The Netherlands.
78. Sax, D. F., J. J. Stachowicz, J. H. Brown, J. F. Bruno, M. N. Dawson, S. D. Gaines, et al. 2007. Ecological and evolutionary insights from species invasions. Trends Ecol. Evol. 22:465-471.
79. Shea, K., and P. Chesson 2002. Community ecology theory as a framework for biological invasions. Trends Ecol. Evol. 17:170-176.
80. Shine, R. 2012. Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol. Appl. 5:107-116.
81. Simberloff, D. 2009. The role of propagule pressure in biological invasions. Pp. 81-102inAnnual review of ecology, evolution and systematics. Annual Reviews, Palo Alto.
82. Stepien, C. A., J. E. Brown, M. E. Neilson, and M. A. Tumeo 2005. Genetic diversity of invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Anal. 25:1043-1060.
83. Suarez, A. V., and N. D. Tsutsui 2008. The evolutionary consequences of biological invasions. Mol. Ecol. 17:351-360.
84. Szpiech, Z. A., M. Jakobsson, and N. A. Rosenberg 2008. ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498-2504.
85. Tallmon, D. A., A. Koyuk, G. Luikart, and M. A. Beaumont 2008. ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol. Ecol. Resour. 8:299-301.
86. Tonione, M. A., N. Reeder, and C. C. Moritz 2011. High genetic diversity despite the potential for stepping-stone colonizations in an invasive species of gecko on Moorea, French Polynesia. PLoS ONE 6: e26874. doi:10.1371/journal.pone.0026874
87. Tsutsui, N. D., A. V. Suarez, D. A. Holway, and T. J. Case 2000. Reduced genetic variation and the success of an invasive species. Proc. Natl. Acad. Sci. USA 97:5948-5953.
88. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills, and P. Shipley 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4:535-538.
89. Vitousek, P. M., C. M. DAntonio, L. L. Loope, and R. Westbrooks 1996. Biological invasions as global environmental change. Am. Sci. 84:468-478.
90. Ward, J. L., M. J. Blum, D. M. Walters, B. A. Porter, N. Burkhead, and B. Freeman 2012. Discordant introgression in a rapidly expanding hybrid swarm. Evol. Appl. 5:380-392.
91. Wares, J. P., A. R. Hughes, and R. K. Grosberg 2005. Mechanisms that drive evolutionary change: insights from species introductions and invasions. Pp. 229-257 in D. F. Sax, J. J. Stachowicz, and S. D. Gaines, eds. Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland.
92. Weir, B. S., and C. C. Cockerham 1984. Estimating F-statistics for the analysis of population-structure. Evolution 38:1358-1370.
93. Williamson, M. 1996. Biological invasions. Chapman and Hall, London.
94. Wilson, J. R. U., E. E. Dormontt, P. J. Prentis, A. J. Lowe, and D. M. Richardson 2009. Something in the way you move: dispersal pathways affect invasion success. Trends Ecol. Evol. 24:136-144.