Problems in the Analysis of Genetic Differentiation Among Populations – a Case Study in Quercus robur

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The conclusions drawn from studies of genetic differentiation among populations largely determine our understanding of ecological and population genetic processes. These conclusions basically depend on the applied type of genetic marker and the method of measuring and estimating genetic differentation. However, concerns have been raised about the conceptual appropriateness of common methods of measuring genetic differentiation. The present paper contributes to the clarification of the problems involved by recalling the conceptual characteristics of FST (= GST), by specifying basic tests of the major causal factors of genetic differentiation with the help of permutation analysis, by comparing FST and Hedrick’s new normalization F’ST with the basic index δ of differentiation for data on allozymes and microsatellites obtained from 6 oak stands. All three descriptors display small values, among which δ is largest and closely followed by F’ST, while FST is distinctly smaller than both across all loci. Degrees of covariation of δ with FST and F’ST differ distinctly between allozymes and microsatellites as a probable consequence of confounding aspects of differentiation with aspects of fixation in the FST descriptors. Permutation analysis reveals that the boundary conditions provided by the number of populations and their (sample) sizes as well as the overall genetic variation across population samples determine the order of magnitude of differentiation. This mathematical artefact undermines the widely held opinion that small degrees of differentiation at many loci are the result of extensive gene flow or recent joint history. Differentation patterns vary considerably among allozyme loci (indicating the action of homogenizing and diversifying selection). In contrast, microsatellite loci consistently display significant differentiation as can be explained by mechanisms of non-recurrent mutation. These observations apply to all three descriptors for the relatively high within population polymorphism observed in the studied stands. At least for low within population polymorphism close to fixation, however, it is shown theoretically that the predictions may diverge distinctly among the three descriptors.

BARRENECHE, T., M. CASASOLI, K. RUSSELL, A. AKKAK, H. MEDDOUR, C. PLOMION, F. VILLANI and A. KREMER (2004): Comparative mapping between Quercus and Castanea using simple-sequence repeats (SSRs). Theoretical and Applied Genetics 108: 558-566.

CHARLESWORTH, B. (1998): Measures of Divergence Between Populations and the Effect of Forces that Reduce Variability. Mol. Biol. Evol. 15: 538-543.

CROW, J. F. and M. KIMURA (1970): An Introduction to Population Genetics Theory. Harper and Row, New York.

DEGEN, B., R. STREIFF and B. ZIEGENHAGEN (1999): Comparative study of genetic variation and differentiation of two pedunculate oak (Quercus robur) stands using microsatellite and allozyme loci. Heredity 83: 597-603.

DOW, B. D., M. V. ASHLEY and H. F. HOWE (1995): Characterization of Highly Variable (Ga/Ct) (N) Microsatellites in the Bur Oak, Quercus inacrocarpa. Theoretical and Applied Genetics 91: 137-141.

DUMOLIN, S., B. DEMESURE and R. J. PETIT (1995): Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated by an efficient PCR method. Theoretical and Applied Genetics 91: 1253-1256.

GREGORIUS, H.-R. (1987): The relationship between the concepts of genetic diversity and differentiation. Theor. Appl. Genetics 74: 397-401.

GREGORIUS, H.-R. (1998): The system analytical approach to the study of hypotheses. URL

GREGORIUS, H.-R. (2002): An integrative approach to modeling mating systems of tree populations. In: B. DEGEN, M. D. LOVELESS, A. KREMER 2002. Modelling and Experimental Research on Genetic Processes in Tropical and Temperate Forests. Belém, PA: Embrapa Amazônia Oriental, pp. 42-68.

GREGORIUS, H.-R. and F. BERGMANN (1995): Analysis of isoenzyme genetic profiles observed in forest tree populations. Pp. 79-96. In: PH. BARADAT, W. T. ADAMS, G. MÜLLER-STARCK (eds.): Population Genetics and Genetic Conservation of Forest Trees. SPB Academic Publishing, Amsterdam.

GREGORIUS, H.-R. and J. H. ROBERDS (1986): Measurement of genetical differentiation among subpopulations. Theoretical and Applied Genetics 71: 826-834.

HASEL, K. and E. SCHWARTZ (2002): Forstgeschichte. Ein Grundriss für Studium und Praxis. Kessel, Remagen.

HEDRICK, P. W. (1999): Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313-318.

HEDRICK, P. W. (2005): A standardized genetic differentiation measure. Evolution 59: 1633-1638.

HERTEL, H. and I. ZASPEL (1996): Investigations on vitality and genetic structure in oak stands. Annales Des Sciences Forestieres 53: 761-773.

HEUERTZ, M., J. F. HAUSMAN, O. J. HARDY, G. G. VENDRAMIN, N. FRASCARIA-LACOSTE and X. VEKEMANS (2004): Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58: 976-988.

KASHI, Y. and D. G. KING (2006): Simple sequence repeats as advantageous mutators in evolution. TRENDS in Genetics 22: 253-259.

KREMER, A., J. L. DUPOUEY, J. D. DEANS, J. COTTRELL, U. CSAIKL, R. FINKELDEY, S. ESPINEL, J. JENSEN, J. KLEINSCHMIT, B. VAN DAM, A. DUCOUSSO, I. FORREST, U. L. DE HEREDIA, A. J. LOWE, M. TUTKOVA, R. C. MUNRO, C. STEINHOFF and V. BADEAU (2002): Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59: 777-787.

LATTA, R. G. and J. B. MITTON (1997): A comparison of population differentiation across four classes of gene marker in Limber Pine (Pinus flexilis James). Genetics 146: 1153-1163.

MANLY, B. F. J. (1997): Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall, London, 399 pp.

NEI, M. (1973): Analysis of gene diversity in subdivided populations. Pro. Nat. Acad. Sci. USA 70(12): 3321-3323.

NAGYLAKI, T. (1998): Fixation Indices in Subdivided Populations. Genetics 148: 1325-1332.

NEIGEL, J. E. (1997): A comparison of alternative strategies for estimating gene flow from genetic markers. Annu. Rev. Ecol. Syst. 28: 105-128.

NEIGEL, J. E. (2002): Is FST obsolete? Conservation Genetics 3: 167-173.

NIELSEN, R. (2001): Statistical tests of selective neutrality in the age of genomics. Heredity 86: 641-647.

SLATKIN, M. (1995): A Measure of Population Subdivision Based on Microsatellite Allele Frequencies. Genetics 139: 457-462.

STEINKELLNER, H., S. FLUSH, C. E. TURETSHEK, C. LEXER, R. STREIFF, A. KREMER, K. BURG and J. GLÖSSL (1997): Identification and characterization of (GA/TC)nmicrosatellite loci from Quercus petraea. Pl. Mol. Bio. 33: 1093-1096.

STREIFF, R., T. LABBE, R. BACILIERI, H. STEINKELLNER, J. GLÖSSL and A. KREMER (1998): Withinpopulation genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites. Molecular Ecology 7: 317-328.

WEIR, B. S. and C. C. COCKERHAM (1984): Estimating FStatistics for the analysis of population structure. Evolution 38: 1358-1370.

WHITLOCK, M. C. and D. E. MCCAULEY (1999): Indirect measures of gene flow and migration: FST not equal 1/(4Nm + 1). Heredity 82: 117-125.

WRIGHT, S. (1978): Evolution and the Genetics of Populations, Vol. 4: Variability within and among Natural Populations. The University of Chicago Press, Chicago.

ZANETTO, A., A. KREMER, G. MÜLLER-STARCK and H. H. HATTEMER (1996): Inheritance of isozymes in pedunculate oak (Quercus robur L.). Journal of Heredity 87: 364-370.

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