Spatiotemporal SNP analysis reveals pronounced biocomplexity at the northern range margin of Atlantic cod Gadus morhua

Evolutionary Applications

Volumn 6, Issue 4, 2013, Pages 690-705

  Therkildsen, Nina Overgaard ^a,b   Hemmer Hansen, Jakob ^a   Hedeholm, Rasmus Berg ^b   Wisz, Mary S ^b,c   Pampoulie, Christophe ^d   Meldrup, Dorte ^a   Bonanomi, Sara ^a,b   Retzel, Anja ^b   Olsen, Steffen Malskær ^b,e   Nielsen, Einar Eg ^a,b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b GREENLAND INSTITUTE OF NATURAL RESOURCES   (Greenland)

^c AARHUS UNIVERSITY   (Denmark)

^d MARINE RESEARCH INSTITUTE   (Iceland)

^e DANISH METEOROLOGICAL INSTITUTE   (Denmark)

Author keywords

Adaptive divergence; Climate change; Contemporary evolution; Genetic monitoring; Greenland; Marine fish; Population structure; Temporal change

Indexed keywords

EID: 84878190937     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12055     Document Type: Article

References (71)

1. Árnason, E., P. H. Petersen, K. Kristinsson, H. Sigurgislason, and S. Palsson 2000. Mitochondrial cytochrome b DNA sequence variation of Atlantic cod from Iceland and Greenland. Journal of Fish Biology 56:409-430.
2. Barrett, R. D. H., and H. E. Hoekstra 2011. Molecular spandrels: tests of adaptation at the genetic level. Nature Reviews Genetics 12:767-780.
3. Beaumont, M. A., and D. J. Balding 2004. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 13:969-980.
4. Beaumont, M. A., and R. A. Nichols 1996. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London Series B-Biological Sciences 263:1619-1626.
5. Bierne, N., J. Welch, E. Loire, F. Bonhomme, and P. David 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology 20:2044-2072.
6. Bigg, G. R., C. W. Cunningham, G. Ottersen, G. H. Pogson, M. R. Wadley, and P. Williamson 2008. Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proceedings of the Royal Society of London Series B-Biological Sciences 275:163-173.
7. Borza, T., B. Higgins, G. Simpson, and S. Bowman 2010. Integrating the markers Pan I and haemoglobin with the genetic linkage map of Atlantic cod (Gadus morhua). BMC Research Notes 3:261.
8. Bowman, S., S. Hubert, B. Higgins, C. Stone, J. Kimball, T. Borza, J. T. Bussey et al. 2011. An integrated approach to gene discovery and marker development in Atlantic cod (Gadus morhua). Marine Biotechnology 13:242-255.
9. Bradbury, I. R., S. Hubert, B. Higgins, T. Borza, S. Bowman, I. G. Paterson, P. V. R. Snelgrove et al. 2010. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proceedings of the Royal Society of London Series B-Biological Sciences 277:3725-3734.
10. Buch, E., S. A. Horsted, and H. Hovgård 1994. Fluctuations in the occurrence of cod in Greenland waters and their possible causes. ICES Marine Science Symposia. 198:158-174.
11. Burrows, M. T., D. S. Schoeman, L. B. Buckley, P. Moore, E. S. Poloczanska, K. M. Brander, C. Brown et al. 2011. The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652-655.
12. Carr, S. M., and H. D. Marshall 2008. Intraspecific phylogeographic genomics from multiple complete mtDNA genomes in Atlantic cod (Gadus morhua): origins of the "Codmother, "transatlantic vicariance and midglacial population expansion. Genetics 180:381-389.
13. Chen, I. C., J. K. Hill, R. Ohlemuller, D. B. Roy, and C. D. Thomas 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333:1024-1026.
14. Coop, G., D. Witonsky, A. Di Rienzo and J. K. Pritchard 2010. Using environmental correlations to identify loci underlying local adaptation. Genetics 185:1411-1423.
15. Corander, J., P. Marttinen, J. Sirén, and J. Tang. 2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539.
16. Drinkwater, K. F. 2005. The response of Atlantic cod (Gadus morhua) to future climate change. ICES Journal of Marine Science 62:1327-1337.
17. Drinkwater, K 2009. Comparison of the response of Atlantic cod (Gadus morhua) in the high-latitude regions of the North Atlantic during the warm periods of the 1920s-1960s and the 1990s-2000s. Deep-Sea Research Part II 56:2087-2096.
18. 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. Molecular Ecology Resources 10:564-567.
19. Excoffier, L., T. Hofer, and M. Foll 2009. Detecting loci under selection in a hierarchically structured population. Heredity 103:285-298.
20. Falush, D., M. Stephens, and J. K. Pritchard 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567-1587.
21. Fevolden, S. E., and G. H. Pogson 1997. Genetic divergence at the synaptophysin (Syp I) locus among Norwegian coastal and north-east Arctic populations of Atlantic cod. Journal of Fish Biology 51:895-908.
22. Foll, M., and O. Gaggiotti 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977-993.
23. Gienapp, P., C. Teplitsky, J. S. Alho, J. A. Mills, and J. Merilä 2008. Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology 17:167-178.
24. Guillot, G., F. Mortier, and A. Estoup 2005. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5:712-715.
25. Hansen, P 1949. Studies on the biology of the cod in Greenland waters. Rapports et Procès-Verbaux des Réunions du Conseil International pour l'Éxploration de la Mer 123:1-77.
26. Hauser, L., and G. R. Carvalho 2008. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish and Fisheries 9:333-362.
27. Hemmer-Hansen, J., E. E. Nielsen, D. Meldrup, and C. Mittelholzer 2011. Identification of single nucleotide polymorphisms in candidate genes for growth and reproduction in a nonmodel organism; the Atlantic cod, Gadus morhua. Molecular Ecology Resources 11:71-80.
28. Hilborn, R., T. P. Quinn, D. E. Schindler, and D. E. Rogers 2003. Biocomplexity and fisheries sustainability. Proceedings of the National Academy of Sciences of the United States of America 100:6564-6568.
29. Hoffmann, A. A., and C. M. Sgrò 2011. Climate change and evolutionary adaptation. Nature 470:479-485.
30. Horsted, S. A. 2000. A review of the cod fisheries at Greenland, 1910-1995. Journal of Northwest Atlantic Fishery Science 28:1-109.
31. Hubert, S., B. Higgins, T. Borza, and S. Bowman 2010. Development of a SNP resource and a genetic linkage map for Atlantic cod (Gadus morhua). BMC Genomics 11:191.
32. ICES 2011. Report of the North Western Working Group (NWWG), 26 April - 3 May 2011, ICES Headquarters, Copenhagen.
33. Jeffreys, H 1939. Theory of Probability. Clarendon Press, Oxford.
34. Jombart, T 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403-1405.
35. Jombart, T., S. Devillard, and F. Balloux 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11:94.
36. Kelly, M. W., E. Sanford, and R. K. Grosberg 2011. Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proceedings of the Royal Society of London Series B-Biological Sciences 279:349-356.
37. Latch, E. K., G. Dharmarajan, J. C. Glaubitz, and O. E. Rhodes Jr 2006. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics 7:295-302.
38. Luikart, G., P. R. England, D. Tallmon, S. Jordan, and P. Taberlet 2003. The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics 4:981-994.
39. Moen, T., B. Hayes, F. Nilsen, M. Delghandi, K. T. Fjalestad, S.-E. Fevolden, P. R. Berg et al. 2008. Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genetics 9:18.
40. Nielsen, E. E., J. Hemmer-Hansen, N. A. Poulsen, V. Loeschcke, T. Moen, T. Johansen, C. Mittelholzer et al. 2009. Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evolutionary Biology 9:276.
41. Nielsen, E. E., A. Cariani, E. M. Aoidh, G. E. MAES, I. Milano, R. Ogden, M. I. Taylor et al. 2012. Gene-associated markers provide tools for tackling illegal fishing and false eco-certification. Nature Communications 3:851.
42. Nosil, P., D. J. Funk, and D. Ortiz-Barrientos 2009. Divergent selection and heterogeneous genomic divergence. Molecular Ecology 18:375-402.
43. O Leary, D. B., J. Coughlan, E. Dillane, T. V. McCarthy, and T. F. Cross 2007. Microsatellite variation in cod Gadus morhua throughout its geographic range. Journal of Fish Biology 70:310-335.
44. Pampoulie, C., D. E. Ruzzante, V. Chosson, T. D. Jorundsdottir, L. Taylor, V. Thorsteinsson, A. K. Danielsdottir et al. 2006. The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Canadian Journal of Fisheries and Aquatic Sciences 63:2660-2674.
45. Pampoulie, C., A. K. Danielsdottir, M. Storr-Paulsen, H. Hovgård, E. Hjörleifsson, and B. Æ. Steinarsson 2011. Neutral and nonneutral genetic markers revealed the presence of inshore and offshore stock components of Atlantic cod in Greenland waters. Transactions of the American Fisheries Society 140:307-319.
46. Parmesan, C., and G. Yohe 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42.
47. Poulsen, N. A., E. E. Nielsen, M. H. Schierup, V. Loeschcke, and P. Grønkjær 2006. Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua). Molecular Ecology 15:321-331.
48. Poulsen, N., J. Hemmer-Hansen, and V. Loeschcke 2011. Microgeographical population structure and adaptation in Atlantic cod Gadus morhua. Marine Ecology Progress Series 436:231-243.
49. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
50. Rätz, H., and J. Lloret 2005. Long-term variability of growth and recruitment of cod (Gadus morhua) off Greenland. ICES Journal of Marine Science 62:1310-1321.
51. Rätz, H., M. Stein, and J. Lloret 1999. Variation in growth and recruitment of Atlantic cod (Gadus morhua) off Greenland during the second half of the twentieth century. Journal of Northwest Atlantic Fishery Science 25:161-170.
52. Russello, M., S. Kirk, and K. Frazer 2011. Detection of outlier loci and their utility for fisheries management. Evolutionary Applications 5:39-52.
53. Ruzzante, D. E., C. T. Taggart, R. W. Doyle, and D. Cook 2001. Stability in the historical pattern of genetic structure of Newfoundland cod (Gadus morhua) despite the catastrophic decline in population size from 1964 to 1994. Conservation Genetics 2:257-269.
54. Ryman, N 2006. CHIFISH: a computer program testing for genetic heterogeneity at multiple loci using chi-square and Fisher's exact test. Molecular Ecology Notes 6:285-287.
55. Schindler, D. E., R. Hilborn, B. Chasco, C. P. Boatright, T. P. Quinn, L. A. Rogers, and M. S. Webster 2010. Population diversity and the portfolio effect in an exploited species. Nature 465:609-612.
56. Star, B., A. J. Nederbragt, S. Jentoft, U. Grimholt, M. Malmstrøm, T. F. Gregers, T. B. Rounge et al. 2011. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207-210.
57. Stein, M 2007. Warming periods off Greenland during 1800-2005: their potential influence on the abundance of cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) in Greenlandic waters. Journal of Northwest Atlantic Fishery Science 39:1-20.
58. Stinchcombe, J. R., and H. E. Hoekstra 2007. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158-170.
59. Storey, J. D., and R. Tibshirani 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America 100:9440-9445.
60. Storr-Paulsen, M., K. Wieland, H. Hovgård, and H. Rätz 2004. Stock structure of Atlantic cod (Gadus morhua) in West Greenland waters: implications of transport and migration. ICES Journal of Marine Science 61:972-982.
61. Storz, J. F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology 14:671-688.
62. Therkildsen, N. O., J. Hemmer-Hansen, T. D. Als, D. P. Swain, M. J. Morgan, E. Trippel, S. Palumbi et al. (in press). Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod. Molecular Ecology.
63. Therkildsen, N. O., E. E. Nielsen, K. Hüssy, D. Meldrup, and A. J. Geffen 2010a. Does DNA extraction affect the physical and chemical composition of historical cod (Gadus morhua) otoliths? ICES Journal of Marine Science 67:1251-1259.
64. Therkildsen, N. O., E. E. Nielsen, D. P. Swain, and J. S. Pedersen 2010b. Large effective population size and temporal genetic stability in Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 67:1585-1595.
65. Turner, T. L., M. W. Hahn, and S. V. Nuzhdin 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biology 3:e285.
66. Waples, R. S 1998. Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Journal of Heredity 89:438-450.
67. Waples, R. S., and O. Gaggiotti 2006. What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology 15:1419-1439.
68. Warnes, G 2003. The genetics package. R News 3:9-13.
69. Weir, B., and C. Cockerham 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
70. Wennevik, V., K. E. Jorstad, G. Dahle, and S.-E. Fevolden 2008. Mixed stock analysis and the power of different classes of molecular markers in discriminating coastal and oceanic Atlantic cod (Gadus morhua L.) on the Lofoten spawning grounds, Northern Norway. Hydrobiologia 606:7-25.
71. Wieland, K., and H. Hovgård 2002. Distribution and drift of Atlantic cod (Gadus morhua) eggs and larvae in Greenland offshore waters. Journal of Northwest Atlantic Fishery Science 30:61-76.