Spatial and temporal microsatellite variation in spawning Atlantic cod, Gadus morhua, around Iceland

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 70, Issue 8, 2013, Pages 1151-1158

  Eiríksson, Gudni Magnús ^a   Árnason, Einar ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

Author keywords

[No Author keywords available]

Indexed keywords

GADOID; GENETIC DIFFERENTIATION; GENETIC DRIFT; GENETIC MARKER;

ICELAND;

EID: 84880928339     PISSN: 0706652X     EISSN: 12057533     Source Type: Journal    
DOI: 10.1139/cjfas-2012-0494     Document Type: Article

References (61)

1. André, C., Larsson, L.C., Laikre, L., Bekkevold, D., Brigham, J., Carvalho, G.R., Dahlgren, T.G., Hutchinson, W.F., Mariani, S., Mudde, K., Ruzzante, D.E., and Ryman, N. 2011. Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity, 106: 270-280. doi:10.1038/hdy.2010.71. PMID:20551979.
2. Applied Biosystems. 2004. GeneMapper Software Version 3.7 user guide. Tech. Rep. Applied Biosystems.
3. Árnason, E. 2004. Mitochondrial cytochrome b DNA variation in the highfecundity Atlantic cod: trans-Atlantic clines and shallow gene genealogy. Genetics, 166(4): 1871-1885. doi:10.1534/genetics.166.4.1871. PMID:15126405.
4. Árnason, E., Pálsson, S., and Arason, A. 1992. Gene flow and lack of population differentiation in Atlantic cod, Gadus morhua L., from Iceland, and comparison of cod from Norway and Newfoundland. J. Fish Biol. 40(4): 751-770. doi:10.1111/j.1095-8649.1992.tb02622.x.
5. Árnason, E., Petersen, P.H., Kristinsson, K., Sigurgíslason, H., and Pálsson, S. 2000. Mitochondrial cytochrome b DNA sequence variation of Atlantic cod from Iceland and Greenland. J. Fish Biol. 56(2): 409-430. doi:10.1111/j.1095-8649.2000.tb02115.x.
6. Árnason, E., Hernandez, U.B., and Kristinsson, K. 2009. Intense habitat-specific fisheries-induced selection at the molecular PanI locus predicts imminent collapse of a major cod fishery. PLoS ONE, 4(5): e5529. doi:10.1371/journal. pone.0005529. PMID:19479037.
7. Beaumont, M., and Nichols, R. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. B Biol. Sci. 263(1377): 1619-1626. doi:10.1098/rspb.1996.0237.
8. Bradbury, I.R., Hubert, S., Higgins, B., Borza, T., Bowman, S., Paterson, I.G., Snelgrove, P.V.R., Morris, C.J., Gregory, R.S., Hardie, D.C., Hutchings, J.A., Ruzzante, D.E., Taggart, C.T., and Bentzen, P. 2010. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proc. R. Soc. B Biol. Sci. 277(1701): 3725-3734. doi:10.1098/rspb.2010. 0985.
9. Braithwaite, V.A., and Salvanes, A.G.V. 2005. Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations. Proc. R. Soc. B Biol. Sci. 272(1568): 1107-1113. doi:10.1098/rspb.2005.3062.
10. Brooker, A.L., Cook, D., Bentzen, P., Wright, J.M., and Doyle, R.W. 1994. Organization of microsatellites differs between mammals and cold-water teleost fishes. Can. J. Fish. Aquat. Sci. 51(9): 1959-1966. doi:10.1139/f94-198.
11. Brownstein, M.J., Carpten, J.D., and Smith, J.R. 1996. Modulation of nontemplated nucleotide addition by TaqDNA polymerase: primer modifications that facilitate genotyping. BioTechniques, 20(6): 1004-1010. PMID:8780871.
12. Carr, S.M., Snellen, A.J., Howse, K.A., and Wroblewski, J.S. 1995. Mitochondrial DNA sequence variation and genetic stock structure of Atlantic cod (Gadus morhua) from bay and offshore locations on the Newfoundland continental shelf. Mol. Ecol. 4(1): 79-88. doi:10.1111/j.1365-294X.1995.tb00194.x. PMID: 7711956.
13. Chapuis, M.-P., and Estoup, A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24(3): 621-631. doi:10.1093/molbev/ msl191. PMID:17150975.
14. Grabowski, T.B., Thorsteinsson, V., McAdam, B.J., and Marteinsdóttir, G. 2011. Evidence of segregated spawning in a single marine fish stock: sympatric divergence of ecotypes in Icelandic cod? PLoS ONE, 6(3): e17,528. doi:10.1371/ journal.pone.0017528.
15. Guinand, B., Lemaire, C., and Bonhomme, F. 2004. How to detect polymorphisms undergoing selection in marine fishes? A review of methods and case studies, including flatfishes. J. Sea Res. 51(3-4): 167-182. doi:10.1016/j.seares. 2003.10.002.
16. Gupta, A.P., and Lewontin, R.C. 1982. A study of reaction norms in natural populations of Drosophila pseudoobscura. Evolution,36(5):934-948. doi:10.2307/ 2408073.
17. Hartl, D.L., and Clark, A.G. 2006. Principles of population genetics. 4th ed. Sinauer Associates, Inc. Publishers, Sunderland, Mass.
18. Jamieson, A., and Jónsson, J. 1971. The Greenland component of spawning cod at Iceland. Rapp. P.-V. Réun. Cons. Int. Explor. Mer, 161: 65-72.
19. Jombart, T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11): 1403-1405. doi:10.1093/bioinformatics/btn129. PMID:18397895.
20. Jónsdóttir, I.G., Campana, S.E., and Marteinsdóttir, G. 2006. Otolith shape and temporal stability of spawning groups of Icelandic cod (Gadus morhua L.). ICES J. Mar. Sci. 63(8): 1501-1512. doi:10.1016/j.icesjms.2006.05.006.
21. Jónsdóttir, Ó.D.B., Imsland, A.K., Daníelsdóttir, A.K., Thorsteinsson, V., and Nævdal, G. 1999. Genetic differentiation among Atlantic cod in south and south-east Icelandic waters: synaptophysin (Syp I) and haemoglobin (HbI) variation. J. Fish Biol. 54(6): 1259-1274. doi:10.1111/j.1095-8649.1999.tb02053.x.
22. Jónsdóttir, Ó.D.B., Daníelsdóttir, A.K., and Nævdal, G. 2001. Genetic differentiation among Atlantic cod (Gadus morhua L.) in Icelandic waters: temporal stability. ICES J. Mar. Sci. 58(1): 114-122. doi:10.1006/jmsc.2000.0995.
23. Jónsson, J. 1996. Tagging of cod (Gadus morhua) in Icelandic waters 1948-1986 and tagging of haddock (Gadus aeglefinus) in Icelandic waters 1953-1965. Rit Fiskideildar, 14: 1-82.
24. Jónsson, S., and Valdimarsson, H. 2005. The flow of Atlantic water to the North Icelandic shelf and its relation to the drift of cod larvae. ICES J. Mar. Sci. 62(7): 1350-1359. doi:10.1016/j.icesjms.2005.05.003.
25. Kalinowski, S.T. 2002. How many alleles per locus should be used to estimate genetic distances? Heredity, 88(1): 62-65. doi:10.1038/sj.hdy.6800009. PMID: 11813108.
26. Karlsson, S., and Mork, J. 2003. Selection-induced variation at the pantophysin locus (PanI) in a Norwegian fjord population of cod (Gadus morhua L.). Mol. Ecol. 12(12): 3265-3274. doi:10.1046/j.1365-294X.2003.01993.x. PMID:14629344.
27. Knutsen, H., Olsen, E.M., Jorde, P.E., Espeland, S.H., André, C., and Stenseth, N.C. 2011. Are low but statistically significant levels of genetic differentiation in marine fishes 'biologically meaningful'? A case study of coastal Atlantic cod. Mol. Ecol. 20(4): 768-783. doi:10.1111/j.1365-294X. 2010.04979.x.
28. Kovach, A.I., Breton, T.S., Berlinsky, D.L., Maceda, L., and Wirgin, I. 2010. Finescale spatial and temporal genetic structure of Atlantic cod off the Atlantic coast of the USA. Mar. Ecol. Prog. Ser. 410: 177-195. doi:10.3354/meps08612.
29. Kristjánsson, T. 2013. Comparison of growth in Atlantic cod (Gadus morhua) originating from the northern and southern coast of Iceland reared under common conditions. Fish. Res. 139: 105-109. doi:10.1016/j.fishres.2012.10.005.
30. Li, Y.-C., Korol, A.B., Fahima, T., Beiles, A., and Nevo, E. 2002. Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol. Ecol. 11(12): 2453-2465. doi:10.1046/j.1365-294X.2002.01643.x. PMID:12453231.
31. Li, Y.-C., Korol, A.B., Fahima, T., and Nevo, E. 2004. Microsatellites within genes: Structure, function, and evolution. Mol. Biol. Evol. 21(6): 991-1007. doi:10. 1093/molbev/msh073. PMID:14963101.
32. McAdam, B.J., Grabowski, T.B., and Marteinsdóttir, G. 2012. Identification of stock components using morphological markers. J. Fish Biol. [ISSN: 1095-8649.] doi:10.1111/j.1095-8649.2012.03384.x.
33. Miller, K.M., Le, K.D., and Beacham, T.D. 2000. Development of tri-and tetranucleotide repeat microsatellite loci in Atlantic cod (Gadus morhua). Mol. Ecol. 9(2): 238-239. doi:10.1046/j.1365-294x.2000.00804-2.x. PMID:10672170.
34. Moen, T., Hayes, B., Nilsen, F., Delghandi, M., Fjalestad, K.T., Fevolden, S.-E., Berg, P.R., and Lien, S. 2008. Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genet. 9(18): 1-9. doi:10.1186/1471-2156-9-18.
35. Mork, J., Ryman, N., Ståhl, G., Utter, F., and Sundnes, G. 1985. Genetic variation in Atlantic cod (Gadus morhua) throughout its range. Can. J. Fish. Aquat. Sci. 42(10): 1580-1587. doi:10.1139/f85-198.
36. Nielsen, E.E., Hansen, M.M., and Meldrup, D. 2006. Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Mol. Ecol. 15(11): 3219-3229. doi:10.1111/j.1365-294X.2006.03025.x. PMID:16968266.
37. Nielsen, E.E., MacKenzie, B.R., Magnussen, E., and Meldrup, D. 2007. Historical analysis of Pan I in Atlantic cod (Gadus morhua): temporal stability of allele frequencies in the southeastern part of the species distribution. Can. J. Fish. Aquat. Sci. 64(10): 1448-1455. doi:10.1139/f07-104.
38. Nielsen, E.E., Hemmer-Hansen, J., Poulsen, N.A., Loeschcke, V., Moen, T., Johansen, T., Mittelholzer, C., Taranger, G.-L., Ogden, R., and Carvalho, G.R. 2009. Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol. Biol. 9(276): 1-11. doi:10.1186/1471-2148-9-276.
39. Oosterhout, C.V., Hutchinson, W.F., Wills, D.P.M., and Shipley, P. 2004. MICROCHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. 4(3): 535-538. doi:10.1111/j.1471-8286.2004. 00684.x.
40. O'Reilly, P.T., Canino, M.F., Bailey, K.M., and Bentzen, P. 2000. Isolation of twenty low stutter di-and tetranucleotide microsatellites for population analyses of walleye pollock and other gadoids. J. Fish Biol. 56(5): 1074-1086. doi:10.1111/ j.1095-8649.2000.tb02124.x.
41. Pálsson, Ó.K., and Thorsteinsson, V. 2003. Migration patterns, ambient temperature, and growth of Icelandic cod (Gadus morhua): evidence from storage tag data. Can. J. Fish. Aquat. Sci. 60(11): 1409-1423. doi:10.1139/f03-117.
42. Pampoulie, C., Ruzzante, D.E., Chosson, V., Jörundsdóttir, T.D., Taylor, L., Thorsteinsson, V., Daníelsdóttir, A.K., and Marteinsdóttir, G. 2006. The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Can. J. Fish. Aquat. Sci. 63(12): 2660-2674. doi:10.1139/f06-150.
43. Pampoulie, C., Jakobsdóttir, K.B., Marteinsdóttir, G., and Thorsteinsson, V. 2008. Are vertical behaviour patterns related to the pantophysin locus in the Atlantic cod (Gadus morhua L.)? Behav. Genet. 38(1): 76-81. doi:10.1007/s10519-007-9175-y. PMID:17978867.
44. Pampoulie, C., Daníelsdóttir, A.K., Storr-Paulsen, M., Hovgård, H., Hjörleifsson, E., and Steinarsson, B. Æ. 2011. Neutral and nonneutral genetic markers revealed the presence of inshore and offshore stock components of Atlantic cod in Greenland waters. Trans. Am. Fish. Soc. 140(2): 307-319. doi: 10.1080/00028487.2011.567850.
45. Pétursdóttir, G., Begg, G.A., and Mareinsdóttir, G. 2006. Discrimination between Icelandic cod (Gadus morhua L.) populations from adjacent spawning areas based on otolith growth and shape. Fish. Res. 80: 182-189. doi:10.1016/j.fishres. 2006.05.002.
46. Pogson, G.H., and Fevolden, S.-E. 2003. Natural selection and the genetic differentiation of coastal and Arctic populations of the Atlantic cod in northern Norway: A test involving nucleotide sequence variation at the pantophysin (PanI) locus. Mol. Ecol. 12(1): 63-74. doi:10.1046/j.1365-294X.2003.01713.x. PMID:12492878.
47. Pogson, G.H., and Mesa, K.A. 2004. Positive Darwinian selection at the pantophysin (PanI) locus in marine gadid fishes. Mol. Biol. Evol. 21(1): 65-75. doi:10. 1093/molbev/msg237. PMID:12949133.
48. Raymond, M., and Rousset, F. 1995. An exact test for population differentiation. Evolution, 49(6): 1280-1283. doi:10.2307/2410454.
49. Reiss, H., Hoarau, G., Dickey-Collas, M., and Wolff, W.J. 2009. Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish. 10(4): 361-395. doi:10.1111/j.1467-2979.2008.00324.x.
50. Russello, M.A., Kirk, S.L., Frazer, K.K., and Askey, P.J. 2012. Detection of outlier loci and their utility for fisheries management. Evol. Appl. 5(1): 39-52. doi: 10.1111/j.1752-4571.2011.00206.x.
51. Ryman, N., and Palm, S. 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. 6(3): 600-602. doi:10.1111/j.1471-8286.2006.01378.x.
52. Salvanes, A.G., Moberg, O., and Braithwaite, V.A. 2007. Effects of early experience on group behaviour in fish. Anim. Behav. 74(4): 805-811. doi:10.1016/j. anbehav.2007.02.007.
53. Tåning, Å.V. 1944. Experiments on meristic and other characters in fishes. I. On the influence of temperature on some meristic characters in sea-trout and the fixation-period of these characters. Medd. Komm. Dan. Fisk. Havunders., Fisk. 11: 1-66.
54. Thorsteinsson, V., Pálsson, Ó.K., Tómasson, G.G., Jónsdóttir, I.G., and Pampoulie, C. 2012. Consistency in the behaviour types of the Atlantic cod: repeatability, timing of migration and geo-location. Mar. Ecol. Progr. Ser. 462: 251-260. doi:10.3354/meps09852.
55. Walsh, P.S., Metzger, D.A., and Higuchi, R. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Bio-Techniques, 10(4): 506-513. PMID:1867860.
56. Waples, R.S. 1989. A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics, 121(2): 379-391. PMID:2731727.
57. Waples, R.S. 1998. Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J. Hered. 89(5): 438-450. doi:10.1093/ jhered/89.5.438.
58. Waples, R.S., and 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. Mol. Ecol. 15(6): 1419-1439. doi:10.1111/j.1365-294X.2006.02890.x.
59. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38(6): 1358-1370. doi:10.2307/2408641.
60. Westgaard, J.-I., and Fevolden, S.-E. 2007. Atlantic cod (Gadus morhua L.) in inner and outer coastal zones of northern Norway display divergent genetic signature at non-neutral loci. Fish. Res. 85(3): 306-315. doi:10.1016/j.fishres.2007. 04.001.
61. Williams, G.C., Koehn, R.K., and Mitton, J.B. 1973. Genetic differentiation without isolation in the American eel, Anguilla rostrata. Evolution, 27(2): 192-204. doi:10.2307/2406960.