Skip to main content
Log in

DNA tests of neutral theory: applications in marine genetics

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The principal methods of using DNA sequence information to test the neutral theory of evolution and polymorphism are described. These include the use of synonymous and nonsynonymous substitutions for detecting purifying and positive selection, the analysis of nucleotide diversity, mismatch analysis and the HKA, McDonald-Kreitman, Tajima and Ewens-Watterson tests. Analysis of the covariation of different kinds of molecular markers and the relationship between genetic variation and fitness is also considered. Examples of the use of these approaches in a wide variety of marine organisms are described. It is emphasised that tests of neutral theory, in addition to providing important fundamental knowledge about the action of evolutionary forces, provide valuable information about the influence of environmental and demographic factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aguade, M. & C. H. Langley, 1994. Polymorphism and divergence in regions of low recombination in Drosophila. In Golding, B. (ed.), Non-Neutral Evolution: Theories and Data. Chapman & Hall, New York: 67–76.

    Google Scholar 

  • Arnason, E. & S. Palsson, 1996. Mitochondrial cytochrome b DNA sequence variation of Atlantic cod Gadus morhua, from Norway. Mol. Ecol. 5: 715–724.

    Google Scholar 

  • Beerli, P., 1998. Estimation of migration rates and populations sizes in geographically structured populations. In Carvalho, G. (ed.), Advances in Molecular Ecology. NATO Science, Series A: Life Sciences. IOS Press, Amsterdam: 39–53.

    Google Scholar 

  • Begun, C. J. & C. F. Aquadro, 1992. Levels of naturally occurring DNA polymorphism correlate with recombination rates of Drosophila melanogaster. Nature 356: 519–520.

    Google Scholar 

  • Bertorelle, G. & M. Slatkin, 1995. The number of segregating sites in expanding human populations, with implications for estimates of demographic parameters. Mol. Biol. Evol. 12: 887–892.

    Google Scholar 

  • Boom, J. D. G., E. G. Boulding & A. T. Beckenback, 1994. Mitochondrial DNA variation in introduced populations of pacific oyster, Crassostrea gigas, in British Columbia. Can. J. Fish. aquat. Sci. 51: 1608–1614.

    Google Scholar 

  • Britten, H. B., 1996. Meta-analysis of the association between multilocus heterozygosity and fitness. Evolution 50: 2158–2164.

    Google Scholar 

  • Brookfield, J. F. Y & P. M. Sharp, 1994. Neutralism and selectionism face up to DNA data. Trends Genet. 10: 109–111.

    Google Scholar 

  • Buroker, N. E., 1983. Population genetics of the American oyster Crassostrea virginica along the Atlantic coast and the Gulf of Mexico. Mar. Biol. 75: 99–112.

    Google Scholar 

  • Burton, R. S. & B.-N. Lee, 1994. Nuclear and mitochondrial gene genealogies and allozyme polymorphisms across a major phylogeographic break in the copepod Tigriopus californicus. Proc. natn. Acad. Sci. U.S.A. 91: 5197–5201.

    Google Scholar 

  • Charlesworth, D., B. Charlesworth & M. T. Morgan, 1995. The pattern of neutral molecular variation under the background selection model. Genetics 141: 1605–1617.

    Google Scholar 

  • Endo, T., K. Ikeo & T. Gojobori, 1996. Large-scale search for genes on which positive selection may operate. Mol. Biol. Evol. 13: 685–690.

    Google Scholar 

  • Fevolden, S. E. & R. Schneppenheim, 1989. Genetic homogeneity of krill (Euphausia superba Dana) in the Southern Ocean. Polar. Biol. 9: 533–539.

    Google Scholar 

  • FitzSimmons, N. N., C. Moritz, C. J. Limpus, L. Pope & R. Prince, 1997. Geographic structure of mitochondrial and nuclear gene polymorphisms in Australian green turtle populations and male-biased gene flow. Genetics 147: 184–1854.

    Google Scholar 

  • Ford, M. J., 1998. Testing models of migration and isolation among populations of chinook salmon (Oncorhynchus tschawytscha). Evolution 52: 539–557.

    Google Scholar 

  • Fu, Y. X., 1994. A phylogenetic estimator of effective population size or mutation rate. Genetics 136: 685–692.

    Google Scholar 

  • Gillespie, J. H., 1989. Could natural selection account for molecular evolution and polymorphism? Genome 31: 311–315.

    Google Scholar 

  • Gillespie, J. H., 1991. The causes of molecular evolution. Oxford University Press, New York.

    Google Scholar 

  • Gillespie, J. H., 1994. Alternatives to the neutral theory. In Golding, B. (ed.), Non-Neutral Evolution: Theories and Data. Chapman & Hall, New York: 1–17.

    Google Scholar 

  • Graur, D. & W. H. Li, 1991. Neutral mutation hypothesis test. Nature 354: 114–115.

    Google Scholar 

  • Hare, M. P. & J. C. Avise, 1998. Population structure in the American oyster as inferred by nuclear gene genealogies. Mol. Biol. Evol. 15: 119–128.

    Google Scholar 

  • Hare, M. P., S. A. Karl & J. C. Avise, 1996. Anonymous nuclear DNA markers in the American oyster and their implications for the heterozygote deficiency phenomenon in marine bivalves. Mol. Biol. Evol. 13: 334–345.

    Google Scholar 

  • Hudson, R. R., 1991. Gene genealogies and the coalescent approach. Oxford Surv. evol. Biol. 7: 1–44.

    Google Scholar 

  • Hudson. R. R., M. Kreitman & M. Aguade, 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153–159.

    Google Scholar 

  • Karl, S. A. & J. C. Avise, 1992. Balancing selection at allozyme loci in oysters: implications from nuclear RFLP's. Science 256: 100–102.

    Google Scholar 

  • Karl, S. A., S. Schultz, D. Desbruyeres, R. Lutz & R. C. Vrijenhoek, 1996. Molecular analysis of gene flow in the hydrothermal vent clam (Calyptogena magnifica). Mol. mar. Biol. Biotech. 5: 193–202.

    Google Scholar 

  • Kimura, M., 1983. The neutral theory of molecular evolution. Cambridge University Press, London.

    Google Scholar 

  • Kimura, M. & J. F. Crow, 1964. The number of alleles that can be maintained in a finite population. Genetics 49: 725–738.

    Google Scholar 

  • Lavery, S., C. Moritz & D. R. Fielder, 1996. Genetic patterns suggest exponential population growth in a declining species. Mol. Biol. Evol. 13: 1106–1113.

    Google Scholar 

  • Lee, Y.-H. & V. D. Vacquier, 1992. The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol. Bull. 182: 97–104.

    Google Scholar 

  • Lee, Y.-H., T. Ota & V. D. Vacquier, 1995. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol. Biol. Evol. 12: 231–238.

    Google Scholar 

  • Lewontin, R. C. & J. Krakauer, 1975. Testing the heterogeneity of F values. Genetics 80: 397–398.

    Google Scholar 

  • McDonald, J. H., 1994. Detecting natural selection by comparing geographic variation in protein and DNA polymorphisms. In Golding, B. (ed.), Non-Neutral Evolution: Theories and Data. Chapman & Hall, New York: 88–100.

    Google Scholar 

  • McDonald, J. H. & M. Kreitman, 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654.

    Google Scholar 

  • McDonald, J. H., B. C. Verrelli & L. B. Geyer, 1996. Lack of geographic variation in anonymous nuclear polymorphisms in the American oyster, Crassostrea virginica. Mol. Biol. Evol. 13: 1114–1118.

    Google Scholar 

  • Metz, C. E., G. Gomez-Gutierrez & V. D. Vacquier, 1998b. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol. Biol. Evol. 15: 185–195.

    Google Scholar 

  • Metz, E. C. & S. R. Palumbi, 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13: 397–406.

    Google Scholar 

  • Metz, C. E., R. Robles-Sikisaka & V. D. Vacquier, 1998a. Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc. natn. Acad. Sci. U.S.A. 95: 10676–10681.

    Google Scholar 

  • Moriyama, E. N. & J. R. Powell, 1996. Intraspecific nuclear DNA variation in Drosophila. Mol. Biol. Evol. 13: 261–277.

    Google Scholar 

  • Nei, M. & T. Maruyama, 1975. Lewontin-Krakauer test for neutral genes. Genetics 80: 395.

    Google Scholar 

  • Ohta, T., 1992. The nearly neutral theory of molecular evolution. Ann. Rev. Ecol. Syst. 23: 263–286.

    Google Scholar 

  • Pogson, G. H. & S. E. Fevolden, 1998. DNA heterozygosity and growth rate in the Atlantic cod Gadus morhua (L). Evolution 52: 915–920.

    Google Scholar 

  • 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.

    Google Scholar 

  • Pogson, G. H. & E. Zouros, 1994. Allozyme and RFLP heterozygosities as correlates of growth rate in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics 137: 221–231.

    Google Scholar 

  • Powers, D. A. & P. M. Schulte, 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 small fish. J. exp. Zool. 282: 71–94.

    Google Scholar 

  • Quesada, H., M. Warren & D. O. F. Skibinski, 1998. Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149: 1511–1526.

    Google Scholar 

  • Quesada, H., R. Wenne & D. O. F. Skibinski, 1999. Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol. Biol. Evol. 16: 655–665.

    Google Scholar 

  • Rand, D. M., 1996. Neutrality tests of molecular markers and the connection between DNA polymorphism, demography and conservation biology. Conserv. Biol. 10: 665–671.

    Google Scholar 

  • Rand, D. M. & L. M. Kann, 1998. Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica 102/103: 393–407.

    Google Scholar 

  • Raybould, A. F., R. J. Mogg & R. T. Clarke, 1996. The genetic structure of Beta vulgaris ssp. maritima (sea beet) populations: RFLPs and isozymes show different patterns of gene flow. Heredity 77: 245–250.

    Google Scholar 

  • Raybould, A. F, R. J. Mogg, C. Aldam, C. J. Gliddon, R. S. Thorpe & R. T. Clarke, 1998. The genetic structure of sea beet (Beta vulgaris ssp. maritima) populations. III. Detection of isolation by distance at microsatellite loci. Heredity 80: 127–132.

    Google Scholar 

  • Reeb, C. A. & J. C. Avise, 1990. A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124: 397–406.

    Google Scholar 

  • Robertson, A., 1975. Remarks on the Lewontin-Krakauer test. Genetics 80: 396.

    Google Scholar 

  • Rogers, A. R., 1995. Genetic evidence for a Pleistocene population explosion. Evolution 49: 608–615.

    Google Scholar 

  • Rogers, A. R. & H. Harpending, 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9: 552–569.

    Google Scholar 

  • Slatkin, M., 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457–462.

    Google Scholar 

  • Slatkin, M. & R. R. Hudson, 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555–562.

    Google Scholar 

  • Stewart, D. T., E. R. Kenchington, R. K. Singh & E. Zouros, 1996. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143: 1349–1357.

    Google Scholar 

  • Stewart, D. T., C. Saavedra, R. R. Stanwood, A. O. Ball & E. Zouros, 1995. Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol. Biol. Evol. 12: 735–747.

    Google Scholar 

  • Swanson, W. J. & V. D. Vacquier, 1998. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281: 710–712.

    Google Scholar 

  • Tajima, F., 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437–460.

    Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    Google Scholar 

  • Taylor, M. F. J., Y. Shen & M. E. Kreitman, 1995. A population genetic test of selection at the molecular level. Science 270: 1497–1499.

    Google Scholar 

  • Vacquier, V. D., W. J. Swanson & Y.-H. Lee, 1997. Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J. mol. Evol. 44: S15–S22.

    Google Scholar 

  • Watterson, G. A., 1975. On the number of segregation sites. Theor. Pop. Biol. 7: 256–276.

    Google Scholar 

  • Watterson, G. A., 1978. The homozygosity test of neutrality. Genetics 88: 405–417.

    Google Scholar 

  • Whitlock, M. C. & D. E. McCauley, 1999. Indirect measures of gene flow and migration. F ST ≠ 1/(4N m + 1). Heredity 82: 117–125.

    Google Scholar 

  • Whittam, T. S. & M. Nei, 1991. Neutral mutation hypothesis test. Nature 354: 115–116.

    Google Scholar 

  • Williams, S. T. & J. A. H. Benzie, 1997. Indo-West Pacific patterns of genetic differentiation in the high-dispersal starfish Linckia laevigata. Mol. Ecol. 6: 559–573.

    Google Scholar 

  • Zane, I., L. Ostellari, L. Maccatrozzo, L. Bargelloni, B. Battaglia & T. Patarnello, 1998. Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations. Proc. r. Soc., Lond. B 265: 2387–2391.

    Google Scholar 

  • Zouros, E. & G. H. Pogson, 1994. The present status of the relationship between heterozygosity and heterosis. In Beaumont, A. R. (ed.), Genetics and the Evolution of Aquatic Animals. Chapman and Hall, London: 135–146.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Skibinski, D.O.F. DNA tests of neutral theory: applications in marine genetics. Hydrobiologia 420, 137–152 (2000). https://doi.org/10.1023/A:1003954229804

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003954229804

Navigation