Genetic and environmental correlates of morphological variation in a marine fish: The case of Baltic Sea herring (Clupea harengus)

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 65, Issue 3, 2008, Pages 389-400

  Jørgensen, Hanne B H ^a,b   Pertoldi, Cino ^b,d   Hansen, Michael M ^a   Ruzzante, Daniel E ^c   Loeschcke, Volker ^b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c DALHOUSIE UNIVERSITY   (Canada)

^d MAMMAL RESEARCH INSTITUTE   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BEHAVIORAL RESPONSE; BODY SIZE; CLUPEOID; GENETIC VARIATION; MARINE ECOSYSTEM; MORPHOLOGY; PHENOTYPIC PLASTICITY; SALINITY; SKULL; SPATIOTEMPORAL ANALYSIS; SPAWNING; TEMPERATURE GRADIENT;

ATLANTIC OCEAN; BALTIC SEA;

CLUPEA HARENGUS; CLUPEIDAE; VERTEBRATA;

EID: 40849113041     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/F07-177     Document Type: Article

References (74)

1. Adams, D.C., and Funk, D.J. 1997. Morphometric inferences on sibling species and sexual dimorphism in Neoclamisus bebbinae leaf beetles: multivariate applications of the thin-plate spline. Syst. Biol. 46: 180-194.
2. Adams, D.C., and Rohlf, F.J. 2000. Ecological character displacement in Plethodon: biochemical differences found from a geometric morphometric study. Proc. Natl. Acad. Sci. U.S.A. 97: 4106-4111.
3. Adams, D.C., Rohlf, F.J., and Slice, D.E. 2004. Geometric morphometrics: ten years of progress following the 'revolution'. Ital. J. Zool. 71: 5-16.
4. Anonymous. 1962. Recommendations adopted by the Herring Committee. Rapp. P.-V. Cons. Perm. Int. Explor. Mer, 27 (Appendix 1): 72-96.
5. Aro, E. 1989. A review of fish migration patterns in the Baltic. Rapp. P.-V. Cons. Perm. Int. Explor. Mer, 190: 72-96.
6. Beaumont, M.A., and Balding, D.J. 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13: 969-980.
7. Bekkevold, D., André, C., Dahlgreen, T.G., Clausen, L.A.W., Torstensen, E., Mosegaard, H., Calvalho, G.R., Christensen, T.B., Norlinder, E., and Ruzzante, D.E. 2005. Environmental correlates of population differentiation in Atlantic herring. Evolution, 59: 2656-2668.
8. Belkhir, K. 2000. GENETIX, logiciel sous Windows pour la génétique des populations. Laboratoire Génomes et Populations, Université de Montpellier, Montpellier, France.
9. Birdsall, K., Zimmerman, E., Teeter, K., and Gibson, G. 2000. Genetic variation for the positioning of wing veins in Drosophila melanogaster. Evol. Dev. 2: 16-24.
10. Bohonak, A.J. 2002. IBD (isolation by distance): a program for analyses of isolation by distance. J. Hered. 93: 153-154.
11. Bonin, A., Bellemain, E., Bronken Eidesen, P., Pompanon, F., Brochmann, C., and Taberlet, P. 2004. How to track and assess genotyping errors in population genetics studies. Mol. Ecol. 13: 3261-3273.
12. Bookstein, F.L. 1996. Biometrics, biomathematics and the morphometric synthesis. Bull. Math. Biol. 58: 313-365.
13. Caldecutt, W.J., and Adams, D.C. 1998. Morphometrics of trophic osteology on the three-spine stickleback, Gasterosteus aculeatus. Copeia, 1998: 827-838.
14. Chakraborty, R., and Leimar, O. 1987. Genetic variation within a subdivided population. In Population genetics and fisheries management. Edited by N. Ryman and F.M. Utter. University of Washington Press, Seattle, Washington. pp. 89-120.
15. Conover, D.O., Brown, J.J., and Ehtisham, A. 1997. Countergradient variation in growth of young striped bass (Morone saxatilis) from different latitudes. Can. J. Fish. Aquat. Sci. 54: 2401-2409.
16. Conover, D.O., Clarke, L.M., Munch, S.B., and Wagner, G.N. 2006. Spatial and temporal scales of adaptive divergence in marine fishes and the implication for conservation. J. Fish Biol. 69(Suppl. C): 21-47.
17. DeWoody, J.A., and Avise, J.C. 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol. 56: 461-473.
18. Estoup, A., Largiader, C.R., Perrot, E., and Chourrout, D. 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol. Mar. Biol. Biotechnol. 5: 295-298.
19. Excoffier, L., Lval, G., and Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinformatics Online, 1: 47-50.
20. Goudet, J. 1995. FSTAT. Version 1.2. A computer program to calculate F statistics. J. Hered. 86: 485-486.
21. Goudet, J., Raymond, M., deMeeus, T., and Rousset, F. 1996. Testing differentiation in diploid populations. Genetics, 144: 1933-1940.
22. 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: 167-182.
23. Guo, S.W., and Thompson, E.A. 1992. Performing the exact test for Hardy-Weinberg proportion for multiple alleles. Biometrics, 48: 361-372.
24. Hammer, Ø., Harper, D.A.T., and Ryan, P.D. 2004. PAST - PAlaeontological STatistics. Version1.21. folk.uio.no/ohammer/past.
25. Hendry, A.P., Day, T., and Taylor, E.B. 2001. Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution, 55: 459-466.
26. International Council for the Exploration of the Sea. 2003. Report of the Herring Assessment Working Group for the area south of 62°N. International Council for the Exploration of the Sea (ICES) CM 2003/ACFM:17.
27. Ignatius, H., Axberg, S., Niemistö, L., and Winterhalter, B. 1981. Quarternary geology of the Baltic Sea. In The Baltic Sea. Edited by A. Voipio. Elsevier Oceanography Series 30, Elsevier Scientific Publishing Company, Amsterdam, the Netherlands. pp. 54-69.
28. Insightful Corporation. 2002. S-PLUS. Version 6.1. Insightful Corporation, Seattle, Wash.
29. Jørgensen, H.B.H., Bekkevold, D., Hansen, M.M., Ruzzante, D.E., and Loeschcke, V. 2005. Marine landscapes and population structure of herring (Clupea harengus L.) in the Baltic Sea. Mol. Ecol. 14: 3219-3234.
30. Kawecki, T.J., and Ebert, D. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7: 1225-1241.
31. Klingenberg, C.P., Barluenga, M., and Meyer, A. 2003. Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex. Biol. J. Linn. Soc. 80: 397-408.
32. Klinkhardt, M. 1996. Der Hering Clupea harengus. Westarp Wissenschaften, Magdeburg, Germany.
33. Knutsen, H., Jorde, P.E., André, C., and Stenseth, C. 2003. Fine-scaled geographic population structuring in a highly mobile marine species: the Atlantic cod. Mol. Ecol. 12: 385-394.
34. Langerhans, R.B., and DeWitt, T.J. 2004. Shared and unique features of evolutionary diversification. Am. Nat. 164: 335-349.
35. Legendre, P., and Legendre, L. 1998. Numerical ecology. In Developments in environmental modelling, 20. Elsevier, Amsterdam, the Netherlands.
36. Manly, B.F.J. 1994. Multivariate statistical methods: a primer. 2nd ed. Chapman & Hall, New York.
37. Marcil, J., Swain, D.P., and Hutchings, J.A. 2006. Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biol. J. Linn. Soc. 88: 351-265.
38. McPherson, A.A., Stephenson, R.L., O'Reilly, P.T., Jones, M.W., and Taggart, C.T. 2001a. Genetic diversity of coastal Northwest Atlantic herring populations: implications for management. J. Fish Biol. 59(Suppl. A): 356-370.
39. McPherson, A.A., O'Reilly, P.T., McParland, T.L., Jones, M.W., and Bentzen, P. 2001b. Isolation of nine novel tetranucleotide microsatellites in Atlantic herring (Clupea harengus). Mol. Ecol. Notes, 1: 40.
40. Möllmann, C., Kornilovs, G., and Sidrevics, L. 2000. Long-term dynamics of main mesozooplankton species in the central Baltic Sea. J. Plankton Res. 22: 2015-2038.
41. Möllmann, C., Kornilovs, G., Fetter, M., and Köster, F.W. 2004. Feeding ecology of central Baltic Sea herring and sprat. J. Fish Biol. 65: 1563-1581.
42. Neves, F.M., and Monteiro, L.R. 2003. Body shape and size divergence among populations of Poecilia vivipara in coastal lagoons of south-eastern Brazil. J. Fish Biol. 63: 928-941.
43. Nielsen, E.E., Hansen, M.M., Ruzzante, D.E., Meldrup, D., and Grønkjær, P. 2003. Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Mol. Ecol. 12: 1497-1508.
44. Nielsen, E.E., Nielsen, P.H., Meldrup, D., and Hansen, M.M. 2004. Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol. Ecol. 13: 585-595.
45. Ojaveer, E., and Elken, J. 1997. On regional subunits in the ecosystem of the Baltic Sea. In Proceedings of the 14th BMB Symposium, 5-8 August 1995, Pärnu. Estonian Academy Publishers, Tallinn, Estonia. pp. 156-169.
46. Olsen, J.B., Lewis, C.J., Kretchmer, E.J., Wilson, S.L., and Seeb, J.E. 2002. Characterization of 14 tetranucleotide microsatellite loci derived from Pacific herring. Mol. Ecol. Notes, 2: 101-103.
47. Parmanne, R. 1990. Growth, morphological variation and migrations of herring (Clupea harengus L.) in the northern Baltic Sea. Fish. Res. 10: 1-48.
48. Parsons, L.S. 1972. Use of meristic characters and a discriminant function for classifying spring- and autumn-spawning Atlantic herring. Res. Bull. Int. Comm. Northw. Atl. Fish. 9: 5-9.
49. Pertoldi, C., García-Perea, R., Godoy, A., Delibes, M., and Loeschcke, V. 2005. Morphological consequences of range fragmentation and population decline on the endangered Iberian lynx (Lynx pardinus). J. Zool. 268: 73-86.
50. Popiel, J. 1984. On the biology of the Baltic herring. Rep. Sea Fish. Inst. 19: 7-16.
51. Raymond, M., and Rousset, F. 1995. GENEPOP. Version 1.2. A population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
52. Robinson, B.W., and Parsons, K.J. 2002. Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can. J. Fish. Aquat. Sci. 59: 1819-1833.
53. Robinson, B.W., and Wilson, D.S. 1994. Character release and displacement in fishes: a neglected literature. Am. Nat. 144: 596-626.
54. Rohlf, F.J. 1999. Shape statistics: Procrustes superimpositions and tangent spaces. J. Classif. 16: 197-223.
55. Rohlf, F.J. 2003. tpsRegr - thin-plate spline regression software. Version1.28. Department of Ecology and Evolution, State University of New York at Stony Brook, New York.
56. Rüber, L., and Adams, D.C. 2001. Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. J. Evol. Biol. 14: 325-332.
57. Ruzzante, D.E., Taggart, C.T., and Cook, D. 1998. A nuclear DNA basis for shelf- and bank-scale population structure in northwest Atlantic cod (Gadus morhua): Labrador to Georges Bank. Mol. Ecol. 7: 1663-1680.
58. Ruzzante, D.E., Mariani, S., Bekkevold, D., André, C., Mosegaard, H., Clausen, L.A.W., Dahlgren, T., Hutchinson, W.F., Hatfield, E.M.C., Torstensen, E., Brigham, J., Simmonds, E.J., Laikre, L., Larsson, L.C., Stet, R.J.M., Ryman, N., and Carvalho, G.R. 2006. Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring. Proc. R. Soc. Lond. B Biol. Sci. 273: 1459-1464.
59. Ryman, N., Lagercrantz, U., Chakraborty, R., and Rosenberg, R. 1984. Lack of correspondence between genetic and morphological variability patterns in Atlantic herring (Clupea harengus). Heredity, 53: 687-704.
60. Saint-Laurent, R., Legault, M., and Bernatchez, L. 2003. Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Michill). Mol. Ecol. 12: 315-330.
61. SAS Istitute Inc. 1997. JMP. Version 3.2.2. SAS Institute Inc., Cary, N.C.
62. Schulte, P.M. 2001. Environmental adaptations as windows on molecular evolution. Comp. Biochem. Physiol. B, 128: 597-611.
63. Schultz, E.T., and Conover, D.O. 1997. Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia, 109: 516-529.
64. Sokal, R.R., and Rohlf, F.J. 1995. Biometry. W.H. Freeman and Company, New York.
65. Storz, J.F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol. Ecol. 14: 671-688.
66. Swain, D.P., and Foote, C.J. 1999. Stocks and chameleons: the use of phenotypic variation in stock identification. Fish. Res. 43: 113-128.
67. Swain, D.P., Riddell, B.E., and Murray, C.B. 1991. Morphological differences between hatchery and wild populations of coho salmon (Oncorhynchus kisutch): environmental versus genetic origin. Can. J. Fish. Aquat. Sci. 48: 1783-1791.
68. Truett, G.E., Heeger, P., Mynatt, R.L., Truett, A.A., Walker, J.A., and Warman, M.L. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT). Biotechniques, 29: 52-54.
69. Valentin, A., Sévigny, J.-M., and Chanut, J.-P. 2002. Geometric morphometrics reveals body shape differences between sympatric redfish Sebastes mentella, Sebastes fasciatus and their hybrids in the Gulf of St Lawrence. J. Fish Biol. 60: 857-875.
70. van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., and Shipley, P.F. 2003. Micro-Checker. Version 2.2.0. University of Hull, England.
71. Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S.M., Schlichting, C.D., and Van Tienderen, P.H. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10: 212-217.
72. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370.
73. Workman, M.S., Leamy, L.J., Routman, E.J., and Cheverud, J.M. 2002. Analysis of QTL effects on the size and shape of mandibular molars in mice. Genetics, 160: 1573-1586.
74. Zar, J.H. 1996. Biostatistical analysis. Prentice-Hall International, Inc., Upper Saddle River, N.J.