Landscape structure and climatic variation determine Atlantic salmon genetic connectivity in the Northwest Atlantic

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 71, Issue 2, 2014, Pages 246-258

  Bradbury, Ian R ^a   Hamilton, Lorraine C ^b   Robertson, Martha J ^a   Bourgeois, Chuck E ^a   Mansour, Atef ^a   Dempson, J Brian ^a  

^a FISHERIES AND OCEANS CANADA   (Canada)

^b BEDFORD INSTITUTE OF OCEANOGRAPHY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLIMATE CHANGE; CLUSTER ANALYSIS; CONSERVATION MANAGEMENT; DIVERGENCE; ENDANGERED SPECIES; GENETIC DRIFT; GENETIC MARKER; HABITAT AVAILABILITY; LANDSCAPE STRUCTURE; LOCAL ADAPTATION; REGRESSION ANALYSIS; SALMONID; WILDLIFE MANAGEMENT;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHWEST); CANADA; NEWFOUNDLAND AND LABRADOR;

EID: 84893492815     PISSN: 0706652X     EISSN: 12057533     Source Type: Journal    
DOI: 10.1139/cjfas-2013-0240     Document Type: Article

References (79)

1. Adkison, M.D. 1995. Population differentiation in Pacific salmons: local adaptation, genetic drift, or the environment? Can. J. Fish. Aquat. Sci. 52(12): 2762-2777. doi:10.1139/f95-865.
2. Allendorf, F.W., Hohenlohe, P.A., and Luikart, G. 2010. Genomics and the future of conservation genetics. Nat. Rev. Genet. 11(10): 697-709. doi:10.1038/ nrg2844.
3. Anderson, T.C. 1985. The rivers of Labrador. Department of Fisheries and Oceans Canada Special Publications 81.
4. Beacham, T.D., and Dempson, J.B. 1998. Population structure of Atlantic salmon from the Conne River, Newfoundland as determined from microsatellite DNA. J. Fish Biol. 52: 665-676. doi:10.1111/j.1095-8649.1998.tb00811.x.
5. Bourret, V., Kent, M.P., Primmer, C.R., Vasemägi, A., Karlsson, S., Hindar, K., McGinnity, P., Verspoor, E., Bernatchez, L., and Lien, S. 2013. SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar). Mol. Ecol. 22(3): 532-551. doi:10.1111/mec.12003.
6. Bradbury, I.R., and Bentzen, P. 2007. Non-linear genetic isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Mar. Ecol. Progr. Ser. 340: 245-257. doi:10.3354/meps340245.
7. Bradbury, I.R., Campana, S.E., and Bentzen, P. 2008. Integrating molecular and otolith elemental estimates of dispersal in an estuarine fish, rainbow smelt (Osmerus mordax) from coastal Newfoundland. Mol. Ecol. 17 (6): 1438-1450.
8. Bradbury, I.R., Hubert, S., Higgins, B., Bowman, S., Paterson, I., Snelgrove, P.V.R., Morris, C., Gregory, R., Hardie, D., Hutchings, J., and Bentzen, P. 2010. Parallel adaptive evolution of Atlantic cod in the eastern and western Atlantic Ocean in response to ocean temperature. Proc. R. Soc. B Biol. Sci. 277 (1701): 3725-3734. doi:10.1098/rspb.2010.0985.
9. Bradbury, I.R., Hubert, S., Higgins, B., Bowman, S., Borza, T., Paterson, I.G., Snelgrove, P.V.R., Morris, C.J., Gregory, R.S., Hardie, D., Hutchings, J.A., Ruzzante, D.E., Taggart, C.T., and Bentzen, P. 2013. Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evol. Appl. 6(3): 450-461. doi:10.1111/eva.12026.
10. Castric, V., and Bernatchez, L. 2004. Individual assignment test reveals differential restriction to dispersal between two salmonids despite no increase of genetic differences with distance. Mol. Ecol. 13(5): 1299-1312. doi:10.1111/j.1365-294X.2004.02129.x.
11. COSEWIC. 2010. COSEWIC assessment and update status report on the North Atlantic cod, Gadus moruha, in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ont.
12. COSEWIC. 2011. COSEWIC assessment and status report on the Atlantic salmon Salmo salar in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ont.
13. Crooks, K.R., and Sanjayan, M. 2006. Connectivity conservation. Cambridge University Press, Cambridge, UK.
14. Cunjak, R.A., and Randall, R.G. 1993. In-stream movements of young Atlantic salmon (Salmo salar) during winter and early spring. In Production of juvenile Atlantic salmon, Salmo salar, in natural waters. Edited by R.J. Gibson and R.E. Cutting. Canadian Special Publication Fishery and Aquatic Sciences. pp. 43-51.
15. Dadswell, M.J., Spares, A.D., Reader, J.M., and Stokesbury, M.J.W. 2010. The North Atlantic subpolar gyre and the marine migration of Atlantic salmon Salmo salar: the 'Merry-Go-Round' hypothesis. J. Fish Biol. 77(3): 435-467.
16. Dalley, E.L., Andrews, C.W., and Green, J.M. 1983. Precocious male Atlantic salmon parr (Salmo salar) in insular Newfoundland. Can. J. Fish. Aquat. Sci. 40(5): 647-652. doi:10.1139/f83-086.
17. Dieringer, D., and Schlötterer, C. 2003. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes, 3(1): 167-169. doi:10.1046/j.1471-8286.2003.00351.x.
18. Dillane, E., Cross, M.C., McGinnity, P., Coughlan, J.P., Galvin, P.T., Wilkins, N.P., and Cross, T.F. 2007. Spatial and temporal patterns in microsatellite DNA variation of wild Atlantic salmon, Salmo salar, in Irish rivers. Fish. Manage. Ecol. 14: 209-219. doi:10.1111/j.1365-2400.2007.00544.x.
19. Dillane, E., McGinnity, P., Coughlan, J.P., Cross, M.C., De Eyto, E., Kenchington, E., Prodöhl, P., and Cross, T.F. 2008. Demographics and landscape features determine intrariver population structure in Atlantic salmon (Salmo salar L.): the case of the River Moy in Ireland. Mol. Ecol. 17(22): 4786-4800. doi:10.1111/j.1365-294X.2008.03939.x.
20. Dionne, M., Miller, K.M., Dodson, J.J., Caron, F., and Bernatchez, L. 2007. Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution, 61(9): 2154-2164. doi:10.1111/j.1558-5646.2007.00178.x.
21. Dionne, M., Caron, F., Dodson, J.J., and Bernatchez, L. 2008. Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flowand local adaptation. Mol. Ecol. 17(10): 2382-2396. doi:10.1111/j.1365-294X. 2008.03771.x.
22. Dionne, M., Caron, F., Dodson, J., and Bernatchez, L. 2009. Comparative survey of within-river genetic structure in Atlantic salmon; relevance for management and conservation. Conserv. Genet. 10(4): 869-879. doi:10.1007/s10592-008-9647-5.
23. Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620. doi:10.1111/j.1365-294X.2005.02553.x.
24. Excoffier, L., and Lischer, H.E.L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10(3): 564-567. doi:10.1111/j.1755-0998.2010.02847.x.
25. Foll, M., and Gaggiotti, O.E. 2006. Identifying the environmental factors that determine the genetic structure of populations. Genetics, 174: 875-891. doi: 10.1534/genetics.106.059451.
26. Funk, W.C., McKay, J.K., Hohenlohe, P.A., and Allendorf, F.W. 2012. Harnessing genomics for delineating conservation units. Trends Ecol. Evol. 27(9): 489-496. doi:10.1016/j.tree.2012.05.012.
27. Gibson, R.J. 1993. The Atlantic salmon in fresh water: spawning, rearing and production. Rev. Fish Biol. Fish. 3: 39-73. doi:10.1007/BF00043297.
28. Gibson, R.J., and Myers, R.A. 1988. Influence of seasonal river discharge on survival of juvenile Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci. 45(2): 344-348. doi:10.1139/f88-040.
29. Gomez-Uchida, D., Knight, T.W., and Ruzzante, D.E. 2009. Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids. Mol. Ecol. 18(23): 4854-4869. doi:10.1111/j.1365-294X.2009.04409.x.
30. Hendry, A.P. 2004. Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol. Ecol. Res. 6: 1219-1236.
31. Hendry, A.P., Castric, V., Kinnison, M.T., and Quinn, T.P. 2004. The evolution of philpatry and dispersal. In Evolution illuminated: salmon and their relatives. Edited by A.P. Hendry and S.C. Stearns. Oxford University Press, Oxford. Hill, W.G. 1981. Estimation of effective population size from data on linkage disequilibrium. Genet. Res. 38: 209-216. doi:10.1017/S0016672300020553.
32. Hurst, T.P. 2007. Causes and consequences of winter mortality in fishes. J. Fish Biol. 71(2): 315-345. doi:10.1111/j.1095-8649.2007.01596.x.
33. Hutchison, D.W., and Templeton, A.R. 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: 1898-1914. doi:10.2307/2640449.
34. Jakobsson, M., and Rosenberg, N.A. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14): 1801-1806. doi:10. 1093/bioinformatics/btm233.
35. Jamieson, A. 1974. Results of water analysis on selected streams and lakes of Newfoundland and Labrador (1972-1973). Resource Development Branch, Newfoundland Region, Fisheries and Marine Service, Department of the Environment.
36. Johnstone, D.L., O'Connell, M.F., Palstra, F.P., and Ruzzante, D.E. 2013. Mature male parr contribution to the effective size of an anadromous Atlantic salmon (Salmo salar) population over 30 years. Mol. Ecol. 22(9): 2394-2407. doi:10.1111/mec.12186.
37. Jombart, T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11): 1403-1405. doi:10.1093/bioinformatics/btn129.
38. Jonsson, B., and Jonsson, N. 2011. Ecology of Atlantic salmon and brown trout: habitat as a template for life histories. Springer, New York.
39. Jorde, P.E., and Ryman, N. 1995. Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics, 139(2): 1077-1090.
40. Kalinowski, S.T. 2005. hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes, 5(1): 187-189.
41. Kalinowski, S.T., Wagner, A.P., and Taper, M.L. 2006. ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol. Ecol. Notes, 6: 576-579.
42. King, T.L., Spidle, A.P., Eackles, M.S., Lubinski, B.A., and Schill, W.B. 2000. Mitochondrial DNA diversity in North American and European Atlantic salmon with emphasis on the Downeast rivers of Maine. J. Fish Biol. 57(3): 614-630. doi:10.1111/j.1095-8649.2000.tb00264.x.
43. King, T.L., Kalinowski, S.T., Schill, W.B., Spidle, A.P., and Lubinski, B.A. 2001. Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspec-tive from microsatellite DNA variation. Mol. Ecol. 10(4): 807-821. doi:10.1046/ j.1365-294X.2001.01231.x.
44. King, T.L., Eackles, M.S., and Letcher, B.H. 2005. Microsatellite DNA markers for the study of Atlantic salmon (Salmo salar) kinship, population structure, and mixed-fishery analyses. Mol. Ecol. Notes, 5(1): 130-132.
45. King, T.L., Verspoor, E., Spidle, A.P., Gross, R., Phillips, R.B., Koljonen, M.L., Sanchez, J.A., and Morrison, C.L. 2007. Biodiversity and population structure. In The Atlantic salmon. Blackwell Publishing, Ltd. pp. 117-166. Langella, O. 1999. Populations. CNRS 1.2.30.
46. Manel, S., Joost, S., Epperson, B.K., Holderegger, R., Storfer, A., Rosenberg, M.S., Scribner, K.T., Bonin, A., and Fortin, M.-J. 2010. Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Mol. Ecol. 19(17): 3760-3772. doi:10.1111/j.1365-294X.2010.04717.x.
47. Manel, S., Gugerli, F., Thuiller, W., Alvarez, N., Legendre, P., Holderegger, R., Gielly, L., Taberlet, P., and IntraBioDiv Consortium. 2012. Broad-scale adaptive genetic variation in alpine plants is driven by temperature and precipitation. Mol. Ecol. 21(15): 3729-3738. doi:10.1111/j.1365-294X.2012.05656.x.
48. McConnell, S.K., O'Reilly, P., Hamilton, L., Wright, J.M., and Bentzen, P. 1995. Polymorphic microsatellite loci from Atlantic salmon (Salmo salar): genetic differentiation of North American and European populations. Can. J. Fish. Aquat. Sci. 52(9): 1863-1872. doi:10.1139/f95-779.
49. McNamara, J.M., and Houston, A.I. 2008. Optimal annual routines: behaviour in the context of physiology and ecology. Philos. Trans. R. Soc. B Biol. Sci. 363(1490): 301-319. doi:10.1098/rstb.2007.2141.
50. McRae, B.H., Hall, S.A., Beier, P., and Theobald, D.M. 2012. Where to Restore Ecological Connectivity? Detecting Barriers and Quantifying Restoration Benefits. PLoS ONE, 7(12): e52604. doi:10.1371/journal.pone.0052604.
51. Nilsson, J., Gross, R., Asplund, T., Dove, O., Jansson, H., Kelloniemi, J., Kohlmann, K., Löytynoja, A., Nielsen, E.E., Paaver, T., Primmer, C.R., Titov, S., Vasemägi, A., Veselov, A., Öst, T., and Lumme, J. 2001. Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol. Ecol. 10(1): 89-102. doi:10.1046/j.1365-294X. 2001.01168.x.
52. O'Reilly, P.T., Hamilton, L.C., McConnell, S.K., and Wright, J.M. 1996. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci. 53(10): 2292-2298. doi:10.1139/f96-192.
53. Ortego, J., Riordan, E.C., Gugger, P.F., and Sork, V.L. 2012. Influence of environmental heterogeneity on genetic diversity and structure in an endemic southern Californian oak. Mol. Ecol. 21(13): 3210-3223. doi:10.1111/j.1365-294X. 2012.05591.x.
54. Ozerov, M.Y., Veselov, A.E., Lumme, J., and Primmer, C.R. 2012. "Riverscape" genetics: river characteristics influence the genetic structure and diversity of anadromous and freshwater Atlantic salmon (Salmo salar) populations in northwest Russia. Can. J. Fish. Aquat. Sci. 69(12): 1947-1958. doi:10.1139/f2012-114.
55. Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: (357-358).
56. Palstra, F.P., O'Connell, M.F., and Ruzzante, D.E. 2007. Population structure and gene flow reversals in Atlantic salmon (Salmo salar) over contemporary and long-term temporal scales: effects of population size and life history. Mol. Ecol. 16(21): 4504-4522. doi:10.1111/j.1365-294X.2007.03541.x.
57. Paterson, S., Piertney, S.B., Knox, D., Gilbey, J., and Verspoor, E. 2004. Characterization and PCR multiplexing of novel highly variable tetranucleotide Atlantic salmon (Salmo salar L.) microsatellites. Mol. Ecol. Notes, 4(2): 160-162.
58. Perrier, C., Guyomard, R., Bagliniere, J.-L., and Evanno, G. 2011. Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences. Mol. Ecol. 20(20): 4231-4245. doi:10. 1111/j.1365-294X.2011.05266.x.
59. Peterson, E.W., and Sickbert, T.B. 2006. Stream water bypass through a meander neck, laterally extending the hyporheic zone. Hydrogeol. J. 14(8): 1443-1451. doi:10.1007/s10040-006-0050-3.
60. Porter, T.R., Riche, L.G., and Traverse, G.R. 1974. Catalogue of Rivers in Insular Newfoundland. Resource Development Branch, Fisheries and Marine Service, Newfoundland Region.
61. Presa, P., and Guyomard, R. 1996. Conservation of microsatellites in three species of salmonids. J. Fish Biol. 49(6): 1326-1329.
62. Primmer, C.R., Veselov, A.J., Zubchenko, A., Poututkin, A., Bakhmet, I., and Koskinen, M.T. 2006. Isolation by distance within a river system: genetic population structuring of Atlantic salmon, Salmo salar, in tributaries of the Varzuga River in northwest Russia. Mol. Ecol. 15(3): 653-666. doi:10.1111/j.1365-294X.2005.02844.x.
63. Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2): 945-959.
64. R Devlopment Core Team 2012. R: A language and environment for statistical computing [online]. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/.
65. Rosenberg, M.S. 2001. PASSAGE. Pattern Analysis, Spatial Statistics, and Geographic Exegesis. Department of Biology, Arizona State University, Tempe, Ariz.
66. Rosenberg, N.A. 2004. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes, 4: 137-138. doi:10.1046/j.1471-8286.2003. 00566.x.
67. Shrimpton, J.M., and Heath, D.D. 2003. Census vs. effective population size in chinook salmon: large-and small-scale environmental perturbation effects. Mol. Ecol. 12(10): 2571-2583. doi:10.1046/j.1365-294X.2003.01932.x.
68. Slettan, A., Olsaker, I., and Lie, Ø. 1995. Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim. Genet. 26(4): 281-282.
69. Spidle, A.P., Kalinowski, S.T., Lubinski, B.A., Perkins, D.L., Beland, K.F., Kocik, J.F., and King, T.L. 2003. Population structure of Atlantic salmon in Maine with reference to populations from Atlantic Canada. Trans. Am. Fish. Soc. 132(2): 196-209. doi:10.1577/1548-8659(2003)132<0196:PSOASI>2.0.CO;2.
70. Stabell, O.B. 1984. Homing and olfaction in salmonids: a critical review with special reference to the Atlantic salmon. Biol. Rev. 59(3): 333-388. doi:10.1111/ j.1469-185X.1984.tb00709.x.
71. Storfer, A., Murphy, M.A., Spear, S.F., Holderegger, R., and Waits, L.P. 2010. Landscape genetics: where are we now? Mol. Ecol. 19(17): 3496-3514. doi:10. 1111/j.1365-294X.2010.04691.x.
72. Takezaki, N., and Nei, M. 1996. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics, 144: 389-399.
73. Taylor, E.B. 1991. A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture, 98: 185-207. doi:10. 1016/0044-8486(91)90383-I.
74. Thibert-Plante, X., and Hendry, A. 2009. Five questions on ecological speciation addressed with individual-based simulations. J. Evol. Biol. 22(1): 109-123. doi: 10.1111/j.1420-9101.2008.01627.x.
75. van Oosterhout, C., Hutchison, W.F., and Wills, D.M.P. 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes, 4: 535.
76. Verspoor, E. 2005. Regional differentiation of North American Atlantic salmon at allozyme loci. J. Fish Biol. 67: 80-103. doi:10.1111/j.0022-1112.2005.00841.x.
77. Verspoor, E., and Jordan, W.C. 1989. Genetic variation at the Me-2 locus in the Atlantic salmon within and between rivers: evidence for its selective maintenance. J. Fish Biol. 35: 205-213. doi:10.1111/j.1095-8649.1989.tb03063.x.
78. Waples, R.S. 2006. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv. Genet. 7(2): 167-184. doi:10.1007/s10592-005-9100-y.
79. Waples, R.S., and Do, C. 2010. Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol. Appl. 3(3): 244-262. doi:10.1111/j. 1752-4571.2009.00104.x.