Abstract
Microsatellite DNA loci, when used in population genetic studies, are usually assumed to be neutral (unaffected by natural selection, either directly or as a result of tight linkage), but this assumption is rarely tested. Here, the assumption of neutrality is examined using established methods, principally that based on the expected relationship between F ST and heterozygosity, at 12 putative neutral microsatellite loci utilised in a study of Atlantic herring Clupea harengus in the north east Atlantic (west of Great Britain and around Ireland) and in the Baltic Sea. All but two of these loci demonstrate relationships that suggest that they may be regarded as neutral genetic markers. Of the other two loci, however, one shows a relationship suggestive of the action of directional selection and the other of balancing natural selection, though other locus-specific effects may operate. Thus, the latter two loci may provide inaccurate inference if used in phylogeographic studies and also demonstrate the danger of assuming neutrality at all microsatellite loci without explicit testing. However, such loci, particularly those affected by directional as opposed to balancing selection, may be of great use in stock discrimination studies, and selected loci in general, have considerably potential in studies of adaptation.
Similar content being viewed by others
References
Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 22: 4692–4693.
Baer, C. F., 1999. Among-locus variation in F ST: fish, allozymes and the Lewontin-Krakauer test revisited. Genetics 152: 653–659.
Beacham, T. D., M. Lapointe, J. R. Candy, B. McIntosh, C. MacConnachie, A. Tabata, K. Kaukinen, L. Deng, K. M. Miller & R. E. Withler, 2004. Stock identification of Fraser river sockeye salmon using microsatellites and major histocompatibility complex variation. Transactions of the American Fisheries Society 133: 1117–1137.
Beaumont, M. A. & D. J. Balding, 2004. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 13: 969–980.
Beaumont, M. A. & R. A. Nichols, 1996. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London B 263: 1619–1626.
Bohonak, A. J., 1999. Dispersal, gene flow and population structure. Quarterly Review of Biology 74: 21–45.
Case, R. A. J., W. F. Hutchinson, L. Hauser, C. Van Oosterhout & G. R. Carvalho, 2005. Macro- and micro-geographic variation in pantophysin (PanI) allele frequencies in NE Atlantic cod Gadus morhua. Marine Ecology Progress Series 301: 267–278.
Goudet, J., 1995. FSTAT, Version 1.2: a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.
Guinand, B., C. Lemaire & F. Bonhomme, 2004. How to detect polymorphisms undergoing selection in marine fishes? A review of methods and case studies, including flatfishes. Journal of Sea Research 51: 167–182.
Hedrick, P. W., 1999. Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313–318.
Hilbish, T. J. & R. Koehn, 1985. The physiological basis of natural selection at the LAP locus. Evolution 39: 1302–1317.
Karlsson, S. & J. Mork, 2003. Selection-induced variation at the pantophysin locus (PanI) in a Norwegian fjord population of cod (Gadus morhus L.). Molecular Ecology 12: 3265–3274.
Kinlan, B. P. & S. D. Gaines, 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84: 2007–2020.
Lemaire, C., G. Allegrucci, M. Naciri, L. Bahri-Sfar, H. Kara & F. Bonhomme, 2000. Do discrepancies between microsatellite and allozyme variation reveal differential selection between sea and lagoon in the sea bass (Dicentrarchus labrax)? Molecular Ecology 9: 457–467.
de Leon, F. G., L. Chikhi & F. Bonhomme, 1997. Microsatellite polymorphism and population subdivision in natural populations of sea bass Dicentrarchus labrax L. 1758. Molecular Ecology 6: 51–62.
Lewontin, R. C. & J. Krakauer, 1973. Distribution of gene frequency as a test of the theory of selective neutrality. Genetics 74: 175–195.
Mariani, S., W. F. Hutchinson, E. M. C. Hatfield, D. E. Ruzzante, E. J. Simmonds, T. G. Dahlgren, C. Andre, J. Brigham, E. Torstensen & G. R. Carvalho, 2005. North Sea herring population structure revealed by microsatellite analysis. Marine Ecology Progress Series 303: 245–247.
McPherson, A. A., P. T. O’Reilly, T. L. McParland, M. W. Jones & P. Bentzen, 2001a. Isolation of nine novel tetranucleotide microsatellites in Atlantic herring (Clupea harengus). Molecular Ecology Notes 1: 31–32.
McPherson, A. A., R. L. Stephenson, P. T. O’Reilly, M. W. Jones & C. T. Taggart, 2001b. Genetic diversity of coastal Northwest Atlantic herring populations: implications for management. Journal of Fish Biology 59: 356–370.
McPherson, A. A., R. L. Stephenson & C. T. Taggart, 2003. Genetically different Atlantic herring Clupea harengus spawning waves. Marine Ecology Progress Series 247: 303–309.
Miller, K. M., K. Laberee, A. D. Schulze & K. H. Kaukinen, 2001. Development of microsatellite loci in Pacific herring (Clupea pallasi). Molecular Ecology Notes 1: 131–132.
Nei, M. & T. Maruyama, 1975. Lewontin-Krakauer test for neutral genes. Genetics 80: 395.
Olsen, J. B., C. J. Lewis, E. J. Kretschmer, S. L. Wilson & J. E. Seeb, 2002. Characterization of 14 tetranucleotide microsatellite loci derived from Pacific herring. Molecular Ecology Notes 2: 101–103.
Pogson, G. H., K. A. Mesa & R. G. Boutilier, 1995. Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics 139: 375–385.
Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.
Robertson, A., 1975. Remarks on the Lewontin-Krakauer test. Genetics 80: 396.
Ruzzante, D. E., S. Mariani, D. Bekkevold, C. Andre, H. Mosegaard, L. Clausen, T. Dahlgren, W. Hutchinson, E. Hatfield, E. Tortensen, J. Brigham, E. Simmonds, L. Laikre, L. Larsson, R. Stet, N. Ryman & G. Carvahlo, 2005. Biocomplexity in a highly migratory marine fish, Atlantic herring. Proceedings of the Royal Society of London B 273: 1459–1464.
Schlotterer, C., 2002. A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160: 753–763.
Shaw, P. W., C. Turan, J. M. Wright, M. O’Connell & G. R. Carvalho, 1999. Microsatellite DNA analysis of population structure in Atlantic herring (Clupea harengus), with direct comparison to allozyme and mtDNA RFLP analyses. Heredity 83: 490–499.
Vitalis, R., K. Dawson & P. Boursot, 2001. Interpretation of variation across marker loci as evidence for selection. Genetics 158: 1811–1823.
Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513.
Ward, R. D., 2000. Genetics in fisheries management. Hydrobiologia 420: 191–201.
Watts, P. C. & J. P. Thorpe, 2006. Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans. Marine Biology 149: 1093–1101.
Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
Whitlock, M. C. & D. E. McCauley, 1999. Indirect measures of gene flow and migration: F ST ≠ 1/(4Nm + 1). Heredity 82: 117–125.
Wright, S., 1951. The genetical structure of populations. Annals of Eugenics 15: 323–354.
Acknowledgements
The westher project would not have been possible without a huge sampling and coordination effort that involved many people: we are grateful to the crews of FRS Scotia, RV Roagan, RV Lough Foyle, RV Celtic Voyager and the various commercial fishing vessels that provided access to samples. Also, we thank J. Boyd, N. Campbell, J. Chubb, C. Collins, M. A. Cross, C. O. Cunningham, A. J. Geffen, F. Gell, S. Jansen, C. Kelly, K. MacKenzie, J. Schlickeisen, P.-J. Schön, D. Wolfenden, C. Zimmermann and A. Zuur for collecting samples and informative discussions. M. Burt kindly provided the samples from Hudson Canyon. Funding was provided by the EU 5th Framework RTD contract QLRT-2001-01056.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: J. Davenport, G. Burnell, T. Cross, M. Emmerson, R. McAllen, R. Ramsay & E. Rogan
Challenges to Marine Ecosystems
Rights and permissions
About this article
Cite this article
Watts, P.C., O’Leary, D., Cross, M.C. et al. Contrasting levels of genetic differentiation among putative neutral microsatellite loci in Atlantic herring Clupea harengus populations and the implications for assessing stock structure. Hydrobiologia 606, 27–33 (2008). https://doi.org/10.1007/s10750-008-9350-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-008-9350-z