Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod

Molecular Ecology

Volumn 22, Issue 9, 2013, Pages 2424-2440

  Therkildsen, Nina O ^a,e   Hemmer Hansen, Jakob ^a   Als, Thomas D ^a   Swain, Douglas P ^b   Morgan, M Joanne ^c   Trippel, Edward A ^d   Palumbi, Stephen R ^e   Meldrup, Dorte ^a   Nielsen, Einar E ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b GULF FISHERIES CENTRE   (Canada)

^c FISHERIES AND OCEANS CANADA   (Canada)

^d ST ANDREWS BIOLOGICAL STATION   (Canada)

^e STANFORD UNIVERSITY   (United States)

Author keywords

fisheries induced evolution; Gadus morhua; genome scan; historical DNA; selection; temporal

Indexed keywords

ADAPTATION; ANIMAL; ARTICLE; ATLANTIC COD; DNA SEQUENCE; ENVIRONMENT; FISHERY; GENE FLOW; GENE FREQUENCY; GENETIC SELECTION; GENETICS; GENOTYPE; MOLECULAR EVOLUTION; POPULATION DYNAMICS; POPULATION GENETICS; REPRODUCIBILITY; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ENVIRONMENT; EVOLUTION, MOLECULAR; FISHERIES; GADUS MORHUA; GENE FLOW; GENE FREQUENCY; GENETICS, POPULATION; GENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULATION DYNAMICS; REPRODUCIBILITY OF RESULTS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

GADUS MORHUA;

EID: 84876692951     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12260     Document Type: Article

References (79)

1. Andersen KH, Brander K, (2009) Expected rate of fisheries-induced evolution is slow. Proceedings of the National Academy of Sciences of the United States of America, 106, 11657-11660.
2. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G, (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics, 9, 323.
3. Árnason E, Hernandez UB, Kristinsson K, (2009) Intense habitat-specific fisheries-induced selection at the molecular Pan I locus predicts imminent collapse of a major cod fishery. PLoS ONE, 4, e5529.
4. Beacham TD, Brattey J, Miller KM, Le KD, Withler RE, (2002) Multiple stock structure of Atlantic cod (Gadus morhua) off Newfoundland and Labrador determined from genetic variation. ICES Journal of Marine Science, 59, 650-665.
5. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
6. Beaumont MA, Nichols RA, (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.
7. Bell G, (2010) Fluctuating selection: the perpetual renewal of adaptation in variable environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 87-97.
8. Bourret V, O'Reilly PT, Carr JW, Berg PR, Bernatchez L, (2011) Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees. Heredity, 106, 500-510.
9. Bowman S, Hubert S, Higgins B, et al,. (2011) An integrated approach to gene discovery and marker development in Atlantic cod (Gadus morhua). Marine Biotechnology, 13, 242-255.
10. Bradbury IR, Hubert S, Higgins B, 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.
11. Campana SE, Chouinard GA, Hanson JM, Frechet A, Brattey J, (2000) Otolith elemental fingerprints as biological tracers of fish stocks. Fisheries Research, 46, 343-357.
12. Cavalli-Sforza L, (1966) Population structure and human evolution. Proceedings of the Royal Society of London Series B-Biological Sciences, 164, 362-379.
13. Chassé J, (2003) Modeling of cod eggs and larvae drift, growth and survival in the Gulf of St. Lawrence, Canada. ICES CM, 2003/O:02, 6 pp.
14. Ernande B, Dieckmann U, Heino M, (2004) Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation. Proceedings of the Royal Society of London Series B-Biological Sciences, 271, 415-423.
15. Excoffier L, Lischer HEL, (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.
16. Faubet P, Waples RS, Gaggiotti OE, (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Molecular Ecology, 16, 1149-1166.
17. Foll M, Gaggiotti O, (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics, 180, 977-993.
18. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J, (2008) Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology, 17, 167-178.
19. Grabowski TB, Young SP, Libungan LA, Steinarsson A, Marteinsdottir G, (2009) Evidence of phenotypic plasticity and local adaption in metabolic rates between components of the Icelandic cod (Gadus morhua L.) stock. Environmental Biology of Fishes, 86, 361-370.
20. Guillot G, Mortier F, Estoup A, (2005) GENELAND: a computer package for landscape genetics. Molecular Ecology Notes, 5, 712-715.
21. Hansen MM, Meier K, Mensberg K-LD, (2010) Identifying footprints of selection in stocked brown trout populations: a spatio-temporal approach. Molecular Ecology, 19, 1787-1800.
22. Hansen MM, Olivieri I, Waller DM, Nielsen EE, GeM Working Group (2012) Monitoring adaptive genetic responses to environmental change. Molecular Ecology, 21, 1311-1329.
23. Hemmer-Hansen J, Nielsen EE, Meldrup D, Mittelholzer C, (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.
24. Hendry AP, Farrugia TJ, Kinnison MT, (2008) Human influences on rates of phenotypic change in wild animal populations. Molecular Ecology, 17, 20-29.
25. Hilborn R, Minte-Vera CV, (2008) Fisheries-induced changes in growth rates in marine fisheries: are they significant? Bulletin of Marine Science, 83, 95-105.
26. Hilborn R, Quinn TP, Schindler DE, Rogers DE, (2003) Biocomplexity and fisheries sustainability. Proceedings of the National Academy of Sciences of the United States of America, 100, 6564-6568.
27. Hoffmann AA, Sgrò CM, (2011) Climate change and evolutionary adaptation. Nature, 470, 479-485.
28. Hubert S, Higgins B, Borza T, Bowman S, (2010) Development of a SNP resource and a genetic linkage map for Atlantic cod (Gadus morhua). BMC genomics, 11, 191.
29. Hutchings JA, (2005) Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences, 62, 824-832.
30. Hutchings JA, Reynolds JD, (2004) Marine fish population collapses: consequences for recovery and extinction risk. BioScience, 54, 297-309.
31. Hutchings JA, Swain DP, Rowe S, et al,. (2007) Genetic variation in life-history reaction norms in a marine fish. Proceedings of the Royal Society of London Series B-Biological Sciences, 274, 1693-1699.
32. Hutchinson WF, (2008) The dangers of ignoring stock complexity in fishery management: the case of the North Sea cod. Biology Letters, 4, 693-695.
33. Jakobsdottir KB, Pardoe H, Magnússon Á, et al,. (2011) Historical changes in genotypic frequencies at the Pantophysin locus in Atlantic cod (Gadus morhua) in Icelandic waters: evidence of fisheries-induced selection? Evolutionary Applications, 4, 562-573.
34. Jombart T, (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
35. Jørgensen C, Enberg K, Dunlop ES, et al,. (2007) Managing evolving fish stocks. Science, 318, 1247-1248.
36. Kingsolver JG, Diamond SE, (2011) Phenotypic selection in natural populations: what limits directional selection? The American naturalist, 177, 346-357.
37. Kinnison MT, Hendry AP, (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica, 112-113, 145-164.
38. Kuparinen A, Merilä J, (2007) Detecting and managing fisheries-induced evolution. Trends in Ecology & Evolution, 22, 652-659.
39. Law R, (2007) Fisheries-induced evolution: present status and future directions. Marine Ecology Progress Series, 335, 271-277.
40. Leonard JA, (2008) Ancient DNA applications for wildlife conservation. Molecular Ecology, 17, 4186-4196.
41. Lewontin RC, Krakauer J, (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics, 74, 175-195.
42. Marcil J, Swain DP, Hutchings JA, (2006) Countergradient variation in body shape between two populations of Atlantic cod (Gadus morhua). Proceedings of the Royal Society of London Series B-Biological Sciences, 273, 217-223.
43. Marsden CD, Woodroffe R, Mills MGL, et al,. (2012) Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus). Molecular Ecology, 21, 1379-1393.
44. Morissette L, Castonguay M, Savenkoff C, et al,. (2009) Contrasting changes between the northern and southern Gulf of St. Lawrence ecosystems associated with the collapse of groundfish stocks. Deep Sea Research Part II: Topical Studies in Oceanography, 56, 2117-2131.
45. Morrissey MB, Hadfield JD, (2012) Directional selection in temporally replicated studies is remarkably consistent. Evolution, 66, 435-442.
46. Narum SR, Hess JE, (2011) Comparison of FST outlier tests for SNP loci under selection. Molecular Ecology Resources, 11, 184-194.
47. Nielsen R, (2005) Molecular signatures of natural selection. Annual Review of Genetics, 39, 197-218.
48. Nielsen EE, Bekkevold D, (2012) The memory remains: application of historical DNA for scaling biodiversity loss. Molecular Ecology, 21, 1539-1541.
49. Nielsen EE, Hansen MM, (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish and Fisheries, 9, 450-461.
50. Nielsen EE, Hemmer-Hansen J, Poulsen NA, 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.
51. Olsen EM, Heino M, Lilly GR, et al,. (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature, 428, 932-935.
52. Olsen EM, Lilly GR, Heino M, Morgan MJ, Brattey J, Dieckmann U, (2005) Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences, 62, 811-823.
53. Orsini L, Spanier KI, De Meester L, (2012) Genomic signature of natural and anthropogenic stress in wild populations of the waterflea Daphnia magna: validation in space, time and experimental evolution. Molecular Ecology, 21, 2160-2175.
54. Palumbi SR, (2001) Humans as the world's greatest evolutionary force. Science, 293, 1786-1790.
55. Poulsen N, Hemmer-Hansen J, Loeschcke V, (2011) Microgeographical population structure and adaptation in Atlantic cod Gadus morhua. Marine Ecology Progress Series, 436, 231-243.
56. Robichaud D, Rose GA, (2004) Migratory behaviour and range in Atlantic cod: inference from a century of tagging. Fish and Fisheries, 5, 185-214.
57. Ruzzante DE, Taggart CT, Cook D, (1996) Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation: cohort contribution and genetic stability. Canadian Journal of Fisheries and Aquatic Sciences, 53, 2695-2705.
58. Ruzzante DE, Taggart CT, Lang S, Cook D, (2000) Mixed-stock analysis of Atlantic cod near the Gulf of St. Lawrence based on microsatellite DNA. Ecological Applications, 10, 1090-1109.
59. Ruzzante DE, Taggart CT, Doyle RW, Cook D, (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.
60. 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.
61. Ryman N, Palm S, (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes, 6, 600-602.
62. Schindler DE, Hilborn R, Chasco B, et al,. (2010) Population diversity and the portfolio effect in an exploited species. Nature, 465, 609-612.
63. Siepielski AM, DiBattista JD, Carlson SM, (2009) It's about time: the temporal dynamics of phenotypic selection in the wild. Ecology Letters, 12, 1261-1276.
64. Stinchcombe JR, Hoekstra HE, (2007) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158-170.
65. Stockwell CA, Hendry AP, Kinnison MT, (2003) Contemporary evolution meets conservation biology. Trends in Ecology & Evolution, 18, 94-101.
66. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America, 100, 9440-9445.
67. Storz JF, (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology, 14, 671-688.
68. Swain DP, (2011) Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua). Evolutionary Applications, 4, 18-29.
69. Swain DP, Frank KT, Maillet G, (2001) Delineating stocks of Atlantic cod (Gadus morhua) in the Gulf of St Lawrence and Cabot Strait areas using vertebral number. ICES Journal of Marine Science, 58, 253-269.
70. Swain DP, Sinclair AF, Mark Hanson J, (2007) Evolutionary response to size-selective mortality in an exploited fish population. Proceedings of the Royal Society of London Series B-Biological Sciences, 274, 1015-1022.
71. Therkildsen NO, Nielsen EE, Swain DP, Pedersen JS, (2010a) 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.
72. Therkildsen NO, Nielsen EE, Hüssy K, Meldrup D, Geffen AJ, (2010b) Does DNA extraction affect the physical and chemical composition of historical cod (Gadus morhua) otoliths? ICES Journal of Marine Science, 67, 1251-1259.
73. Trippel EA, (1995) Age at maturity as a stress indicator in fisheries. BioScience, 45, 759-771.
74. Umina PA, Weeks AR, Kearney MR, McKechnie SW, Hoffmann AA, (2005) A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science, 308, 691-693.
75. Vilas A, Pérez-Figueroa A, Caballero A, (2012) A simulation study on the performance of differentiation-based methods to detect selected loci using linked neutral markers. Journal of Evolutionary Biology, 25, 1364-1376.
76. Wandeler P, Hoeck PEA, Keller LF, (2007) Back to the future: museum specimens in population genetics. Trends in Ecology & Evolution, 22, 634-642.
77. Waples RS, Gaggiotti O, (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.
78. Warnes G, (2003) The genetics package. R News, 3, 9-13.
79. Wilson GA, Rannala B, (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177-1191.