Abstract
Natural selection has been invoked to explain the observed geographic distribution of allozyme allele frequencies for a number of teleost species. The effects of selection on allozyme loci in three species of Pacific salmon were tested. A simulation-based approach to estimate the null distribution of population differentiation (F ST) and test for F ST outliers was used. This approach showed that a majority of allozyme loci conform to neutral expectations predicted by the simulation model, with relatively few F ST outliers found. No consistent F ST outlier loci were found across species. Analysis of population sub-groups based on geography and genetic identity reduced the number of outlier loci for some species, indicating that large geographic groups may include genetically divergent populations and/or that there is geographic heterogeneity in selection pressure upon allozyme loci. Two outlier allozyme loci found in this analysis, lactate dehydrogenase-B and malic enzyme, have been shown to be influenced by selection in other teleost species. This approach is also useful in identifying allozyme loci (or other genetic markers) that meet assumptions for population genetic study.
Similar content being viewed by others
References
Allendorf FW, Knudsen KL, Leary RF (1983) Adaptive significance of differences in the tissue-specific expression of a phosphoglucomutase gene in rainbow trout. Proc Natl Acad Sci (USA) 80:1397–1400
Avise JC (2004) Molecular markers, natural history and evolution. Sinauer, Sunderland, MA
Bartley D, Gall GAE, Bentley B, Brodziak J, Gomulkiewicz R, Mangel M (1992) Geographic-variation in population genetic-structure of Chinook salmon from California and Oregon. Fish Bull 90:77–100
Beaumont MA (2005) Adaptation and speciation: what can FST tell us? Trends Ecol Evol 20:435–440
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Roy Soc Lond Ser B Biol Sci 263:1619–1626
Burridge CP, Hurt AC, Farrington LW, Coutin PC, Austin CM (2004) Stepping stone gene flow in an estuarine-dwelling sparid from south-east Australia. J Fish Biol 64:805–819
Carfagna M, Fucci L, Gaudio L, Pontecorvo G, Rubino R (1980) Adaptive value of PGM polymorphisms in laboratory populations of Drosophila melanogaster. Genet Res 36:265–276
Geertjes GJ, Postema J, Kamping A, van Delden W, Videler JJ, van de Zande L (2004) Allozymes and RAPDs detect little genetic population substructuring in the Caribbean stoplight parrotfish Sparisoma viride. Mar Ecol Progr Ser 279:225–235
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Genet Rev 4:981–994
McDonald JH (1994) Detecting natural selection by comparing geographic variation in protein and DNA polymorphisms. In: Golding B (ed) Non-neutral evolution. Chapman and Hall, New York, New York, USA, pp 88–100
Oakshott JG, Wilson SR, Parnell P (1985) Selective effects of temperature on some enzyme polymorphisms in laboratory populations of Drosophila melanogaster. Heredity 55:69–82
Phelps SR, Leclair LL, Young S, Blankenship HL (1994) Genetic diversity patterns of chum salmon in the Pacific Northwest. Can J Fish Aquat Sci 51:65–83
Powers DA, Schulte PM (1998) Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment: a multidisciplinary approach to address the million-year saga of a small fish. J Exp Zool 282:71–94
Raeymaekers JAM, Maes GE, Audenaert E, Volckaert FAM (2005) Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system. Mol Ecol 14:1001–1014
Ropson IJ, Brown DC, Powers DA (1990) Biochemical genetics of Fundulus heteroclitus (L.) VI. Geographical variation in the gene frequencies at 15 loci. Evolution 44:16–26
Sassaman C, Yoshiyama RM, Darling JDS (1983) Temporal stability of lactate dehydrogenase-A clines of the high cockscomb, Anoplarchus purpurescens. Evolution 37:472–483
Shaklee JB, Allendorf FW, Morizot DC, Whitt GS (1990) Gene nomencalture for the protein-coding loci in fish. Trans Am Fish Soc 119:2–15
Shaklee JB, Bentzen P (1998) Genetic identification of stocks of marine fish and shellfish. Bull Mar Sci 62:589–621
Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688
Storz JF, Nachman MW (2003) Natural selection on protein polymorphism in the rodent genus Peromyscus: evidence from interlocus contrasts. Evolution 57:2628–2635
Varnavskaya NV, Wood CC, Everett RJ (1994) Genetic variation in sockeye salmon (Oncorhynchus nerka) populations of Asia and North America. Can J Fish Aquat Sci 51:142–146
Vespoor E, Jordan WC (1989) Genetic variation at the Me-2 locus in the Atlantic salmon within and between rivers: evidence for its selective maintenance. J Fish Biol 35:205–213
Verrelli BC, Eanes WF (2000) Extensive amino acid polymorphism at the Pgm locus is consistent with adaptive protein evolution in Drosophila melanogaster. Genetics 156:1737–1752
Vitalis R, Dawson K, Boursot P (2001) Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811–1823
Waples RS, Teel DJ, Myers JM, Marshall AR (2004) Life-history divergence in Chinook salmon: historic contingency and parallel evolution. Evolution 58:386–403
Williams GC, Koehn RC, Mitton JB (1973) Genetic differentiation without isolation in the American eel, Anguilla rostrata. Evolution 27:192–204
Wilmot RL, Burger CV (1985) Genetic differences among populations of Alaskan sockeye salmon. Trans Am Fish Soc 114:236–243
Wilmot RL, Everett RJ, Spearman WJ, Baccus R, Varnavskaya NV, Putivkin SV (1994) Genetic stock structure of Western Alaska chum salmon and a comparison with Russian far-East stocks. Can J Fish Aquat Sci 51:84–94
Winans GA, Paquin MM, Van Doornik DM, Baker BM, Thornton P, Rawding D, Marshall A, Moran P, Kalinowski S (2004) Genetic stock identification of steelhead in the Columbia River Basin: an evaluation of different molecular markers. N Am J Fish Manage 24:672–685
Wood CC, Riddell BE, Rutherford DT, Withler RE (1994) Biochemical genetic survey of sockeye salmon (Oncorhynchus nerka) in Canada. Can J Fish Aquat Sci 51:114–131
Acknowledgements
A.A. is funded by a UCOP postdoctoral fellowship. This manuscript has benefited from comments and discussion from J. C. Garza, K. P. Kamer, C. Lemaire, and two anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aguilar, A. Analysis of F ST outliers at allozyme loci in Pacific salmon: implications for natural selection. Environ Biol Fish 76, 329–339 (2006). https://doi.org/10.1007/s10641-006-9037-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-006-9037-0