Assessing population differentiation and isolation from single-nucleotide polymorphism data
We introduce a new, hierarchical, model for single-nucleotide polymorphism allele frequencies in a structured population, which is naturally fitted via Markov chain Monte Carlo methods. There is one parameter for each population, closely analogous to a population-specific version of Wright's FS...
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| Published in: | Journal of the Royal Statistical Society. Series B, Statistical methodology Vol. 64; no. 4; pp. 695 - 715 |
|---|---|
| Main Authors: | , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
Oxford, UK
Blackwell Publishers
01.10.2002
Blackwell Royal Statistical Society |
| Series: | Journal of the Royal Statistical Society Series B |
| Subjects: | |
| ISSN: | 1369-7412, 1467-9868 |
| Online Access: | Get full text |
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| Abstract | We introduce a new, hierarchical, model for single-nucleotide polymorphism allele frequencies in a structured population, which is naturally fitted via Markov chain Monte Carlo methods. There is one parameter for each population, closely analogous to a population-specific version of Wright's FST, which can be interpreted as measuring how isolated the relevant population has been. Our model includes the effects of single-nucleotide polymorphism ascertainment and is motivated by population genetics considerations, explicitly in the transient setting after divergence of populations, rather than as the equilibrium of a stochastic model, as is traditionally the case. For the sizes of data set that we consider the method provides good parameter estimates and considerably outperforms estimation methods analogous to those currently used in practice. We apply the method to one new and one existing human data set, each with rather different characteristics-the first consisting of three rather close European populations; the second of four populations taken from across the globe. A novelty of our framework is that the fit of the underlying model can be assessed easily, and these results are encouraging for both data sets analysed. Our analysis suggests that Iceland is more differentiated than the other two European populations (France and Utah), a finding which is consistent with the historical record, but not obvious from comparisons of simple summary statistics. |
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| AbstractList | We introduce a new, hierarchical, model for single‐nucleotide polymorphism allele frequencies in a structured population, which is naturally fitted via Markov chain Monte Carlo methods. There is one parameter for each population, closely analogous to a population‐specific version of Wright's FST, which can be interpreted as measuring how isolated the relevant population has been. Our model includes the effects of single‐nucleotide polymorphism ascertainment and is motivated by population genetics considerations, explicitly in the transient setting after divergence of populations, rather than as the equilibrium of a stochastic model, as is traditionally the case. For the sizes of data set that we consider the method provides good parameter estimates and considerably outperforms estimation methods analogous to those currently used in practice. We apply the method to one new and one existing human data set, each with rather different characteristics—the first consisting of three rather close European populations; the second of four populations taken from across the globe. A novelty of our framework is that the fit of the underlying model can be assessed easily, and these results are encouraging for both data sets analysed. Our analysis suggests that Iceland is more differentiated than the other two European populations (France and Utah), a finding which is consistent with the historical record, but not obvious from comparisons of simple summary statistics. We introduce a new, hierarchical, model for single-nucleotide polymorphism allele frequencies in a structured population, which is naturally fitted via Markov chain Monte Carlo methods. There is one parameter for each population, closely analogous to a population-specific version of Wright's "F""ST", which can be interpreted as measuring how isolated the relevant population has been. Our model includes the effects of single-nucleotide polymorphism ascertainment and is motivated by population genetics considerations, explicitly in the transient setting after divergence of populations, rather than as the equilibrium of a stochastic model, as is traditionally the case. For the sizes of data set that we consider the method provides good parameter estimates and considerably outperforms estimation methods analogous to those currently used in practice. We apply the method to one new and one existing human data set, each with rather different characteristics-the first consisting of three rather close European populations; the second of four populations taken from across the globe. A novelty of our framework is that the fit of the underlying model can be assessed easily, and these results are encouraging for both data sets analysed. Our analysis suggests that Iceland is more differentiated than the other two European populations (France and Utah), a finding which is consistent with the historical record, but not obvious from comparisons of simple summary statistics. Copyright 2002 Royal Statistical Society. |
| Author | Gústafsson, Ómar Stefánsson, Kári Nicholson, George Donnelly, Peter Smith, Albert V. Jónsson, Frosti |
| Author_xml | – sequence: 1 givenname: George surname: Nicholson fullname: Nicholson, George – sequence: 2 givenname: Albert V. surname: Smith fullname: Smith, Albert V. – sequence: 3 givenname: Frosti surname: Jónsson fullname: Jónsson, Frosti – sequence: 4 givenname: Ómar surname: Gústafsson fullname: Gústafsson, Ómar – sequence: 5 givenname: Kári surname: Stefánsson fullname: Stefánsson, Kári – sequence: 6 givenname: Peter surname: Donnelly fullname: Donnelly, Peter |
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| Keywords | Human Bottleneck Stochastic model Monte Carlo method Parameter estimation Demography Index History Population genetics Markov chain Statistical method Fixation Wright Fisher diffusion Genetics Hierarchical model Population dynamics Diffusion Differentiation Fixation index Population history |
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| References | Lewontin, R. and Krakauer, J. (1973) Distribution of gene frequencey as a test of the theory of selective neutrality of polymorphisms. Genetics, 74, 175-195. Foreman, L. A., Smith, A. F. M. and Evett, I. W. (1997) Bayesian analysis of DNA profiling data in forensic identification applications (with discussion). J. R. Statist. Soc. A, 160, 429-469. Nielsen, R. and Wakeley, J. (2001) Distinguishing migration from isolation: a markov chain monte carlo approach. Genetics, 158, 885-896. Whitlock, M. and McCauley, D. (1999) Indirect measures of gene flow and migration: fST≠1/(4nm+1). Heredity, 82, 117-125. (1997) Significant genetic correlations among Caucasians at forensic DNA loci. Heredity, 78, 583-589. (1982) The shifting balances theory and macroevolution. A. Rev. Genet., 16, 1-19. Wakeley, J., Nielsen, R., Liu-Cordero, S. and Ardlie, K. (2001) The discovery of single-nucleotide polymorphisms-and inferences about human demographic history. Am. J. Hum. Genet., 69, 1332-1347. Weir, B. (1996) Genetic Data Analysis II. Sunderland: Sinauer. (1951) The genetic structure of populations. Ann. Eugen., 15, 323-354. Bowcock, A., Hebert, J., Mountain, J., Kidd, J., Rogers, J., Kidd, K. and Cavalli-Sforza, L. (1991a) Study of an additional 58 dna markers in five populations from four continents. Gene Geogr., 5, 151-173. Balding, D. and Nichols, R. (1995) A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity. Genetica, 96, 3-12. Hudson, R. (1998) Island models and the coalescent process. Molec. Ecol., 7, 413-418. Ewens, W. (1979) Mathematical Population Genetics. New York: Springer. Wang, D., Fan, J., Siao, C., Berno, A., Young, P., Sapolsky, R., Ghandour, G., Perkins, N., Winchester, E., Spencer, J., Kruglyak, L., Stein, L., Hsie, L., Topaloglou, T., Hubbell, E., Robinson, E., Mittman, M., Morris, M., Shen, N., Kilburn, D., Rioux, J., Nusbaum, C., Rozen, S., Hudson, T. and Lander, E. (1998) Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science, 280, 1077-1082. Bowcock, A., Kidd, J., Mountain, J., Hebert, J., Carotenuto, L., Kidd, K. and Cavalli-Sforza, L. (1991b) Drift, admixture, and selection in human evolution: a study with dna polymorphisms. Proc. Natn. Acad. Sci. USA, 88, 839-843. Roeder, K., Escobar, M., Kadane, J. and Balazs, I. (1998) Measuring heterogeneity in forensic databases using hierarchical Bayes models. Biometrika, 85, 269-287. Gelman, A. and Rubin, D. (1992) Inference from iterative simulation using multiple sequences. Statist. Sci., 7, 457-511. Cockerham, C. C. and Weir, B. S. (1987) Correlations, descent measures: drift with migration and mutation. Proc. Natn. Acad. Sci. USA, 84, 8512-8514. Ethier, S. and Kurtz, T. (1986) Markov Processes-Characterisation and Convergence. New York: Wiley. Wakeley, J. (2001) The coalescent in an island model of population subdivision with variation among demes. Theor. Popln Biol., 59, 133-144. 1995; 96 1992; 7 1998; 280 1982; 16 1987; 84 1973; 74 2001 1997; 160 1997; 78 1991a; 5 1986 1996 2001; 59 1951; 15 1998; 7 1998; 85 1999; 82 1991b; 88 2001; 69 1979 2001; 158 1932; 1 Cockerham (2023040109511895500_) 1987; 84 Rousset (2023040109511895500_) 2001 Wang (2023040109511895500_) 1998; 280 Nielsen (2023040109511895500_) 2001; 158 Excoffier (2023040109511895500_) 2001 Lewontin (2023040109511895500_) 1973; 74 Ewens (2023040109511895500_) 1979 Wakeley (2023040109511895500_) 2001; 69 Bowcock (2023040109511895500_) 1991; 88 Hudson (2023040109511895500_) 1998; 7 (2023040109511895500_) 1951; 15 Balding (2023040109511895500_) 1995; 96 Gelman (2023040109511895500_) 1992; 7 Foreman (2023040109511895500_) 1997; 160 Beaumont (2023040109511895500_) 2001 Bowcock (2023040109511895500_) 1991; 5 Roeder (2023040109511895500_) 1998; 85 Wright (2023040109511895500_) 1932 (2023040109511895500_) 1982; 16 Ethier (2023040109511895500_) 1986 Weir (2023040109511895500_) 1996 Wakeley (2023040109511895500_) 2001; 59 Nordborg (2023040109511895500_) 2001 Whitlock (2023040109511895500_) 1999; 82 (2023040109511895500_) 1997; 78 |
| References_xml | – reference: Bowcock, A., Hebert, J., Mountain, J., Kidd, J., Rogers, J., Kidd, K. and Cavalli-Sforza, L. (1991a) Study of an additional 58 dna markers in five populations from four continents. Gene Geogr., 5, 151-173. – reference: Roeder, K., Escobar, M., Kadane, J. and Balazs, I. (1998) Measuring heterogeneity in forensic databases using hierarchical Bayes models. Biometrika, 85, 269-287. – reference: - (1982) The shifting balances theory and macroevolution. A. Rev. Genet., 16, 1-19. – reference: Wakeley, J. (2001) The coalescent in an island model of population subdivision with variation among demes. Theor. Popln Biol., 59, 133-144. – reference: Wakeley, J., Nielsen, R., Liu-Cordero, S. and Ardlie, K. (2001) The discovery of single-nucleotide polymorphisms-and inferences about human demographic history. Am. J. Hum. Genet., 69, 1332-1347. – reference: Bowcock, A., Kidd, J., Mountain, J., Hebert, J., Carotenuto, L., Kidd, K. and Cavalli-Sforza, L. (1991b) Drift, admixture, and selection in human evolution: a study with dna polymorphisms. Proc. Natn. Acad. Sci. USA, 88, 839-843. – reference: Foreman, L. A., Smith, A. F. M. and Evett, I. W. (1997) Bayesian analysis of DNA profiling data in forensic identification applications (with discussion). J. R. Statist. Soc. A, 160, 429-469. – reference: Nielsen, R. and Wakeley, J. (2001) Distinguishing migration from isolation: a markov chain monte carlo approach. Genetics, 158, 885-896. – reference: Cockerham, C. C. and Weir, B. S. (1987) Correlations, descent measures: drift with migration and mutation. Proc. Natn. Acad. Sci. USA, 84, 8512-8514. – reference: Wang, D., Fan, J., Siao, C., Berno, A., Young, P., Sapolsky, R., Ghandour, G., Perkins, N., Winchester, E., Spencer, J., Kruglyak, L., Stein, L., Hsie, L., Topaloglou, T., Hubbell, E., Robinson, E., Mittman, M., Morris, M., Shen, N., Kilburn, D., Rioux, J., Nusbaum, C., Rozen, S., Hudson, T. and Lander, E. (1998) Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science, 280, 1077-1082. – reference: - (1951) The genetic structure of populations. Ann. Eugen., 15, 323-354. – reference: Balding, D. and Nichols, R. (1995) A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity. Genetica, 96, 3-12. – reference: Whitlock, M. and McCauley, D. (1999) Indirect measures of gene flow and migration: fST≠1/(4nm+1). Heredity, 82, 117-125. – reference: Hudson, R. (1998) Island models and the coalescent process. Molec. Ecol., 7, 413-418. – reference: Lewontin, R. and Krakauer, J. (1973) Distribution of gene frequencey as a test of the theory of selective neutrality of polymorphisms. Genetics, 74, 175-195. – reference: - (1997) Significant genetic correlations among Caucasians at forensic DNA loci. Heredity, 78, 583-589. – reference: Ethier, S. and Kurtz, T. (1986) Markov Processes-Characterisation and Convergence. New York: Wiley. – reference: Weir, B. (1996) Genetic Data Analysis II. Sunderland: Sinauer. – reference: Ewens, W. (1979) Mathematical Population Genetics. New York: Springer. – reference: Gelman, A. and Rubin, D. (1992) Inference from iterative simulation using multiple sequences. Statist. Sci., 7, 457-511. – volume: 84 start-page: 8512 year: 1987 end-page: 8514 article-title: Correlations, descent measures: drift with migration and mutation publication-title: Proc. Natn. Acad. Sci. USA – volume: 74 start-page: 175 year: 1973 end-page: 195 article-title: Distribution of gene frequencey as a test of the theory of selective neutrality of polymorphisms publication-title: Genetics – volume: 88 start-page: 839 year: 1991b end-page: 843 article-title: Drift, admixture, and selection in human evolution: a study with dna polymorphisms publication-title: Proc. Natn. Acad. Sci. USA – volume: 16 start-page: 1 year: 1982 end-page: 19 article-title: The shifting balances theory and macroevolution publication-title: A. Rev. Genet. – year: 1996 – volume: 96 start-page: 3 year: 1995 end-page: 12 article-title: A method for quantifying differentiation between populations at multi‐allelic loci and its implications for investigating identity and paternity publication-title: Genetica – volume: 160 start-page: 429 year: 1997 end-page: 469 article-title: Bayesian analysis of DNA profiling data in forensic identification applications (with discussion) publication-title: J. R. Statist. Soc. – volume: 5 start-page: 151 year: 1991a end-page: 173 article-title: Study of an additional 58 dna markers in five populations from four continents publication-title: Gene Geogr – year: 1979 – volume: 7 start-page: 413 year: 1998 end-page: 418 article-title: Island models and the coalescent process publication-title: Molec. 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Sci. – volume-title: Mathematical Population Genetics year: 1979 ident: 2023040109511895500_ – volume: 85 start-page: 269 year: 1998 ident: 2023040109511895500_ article-title: Measuring heterogeneity in forensic databases using hierarchical Bayes models publication-title: Biometrika doi: 10.1093/biomet/85.2.269 – volume-title: Markov Processes—Characterisation and Convergence year: 1986 ident: 2023040109511895500_ doi: 10.1002/9780470316658 – volume: 82 start-page: 117 year: 1999 ident: 2023040109511895500_ article-title: Indirect measures of gene flow and migration: fST≠1/(4nm+1) publication-title: Heredity doi: 10.1038/sj.hdy.6884960 – volume: 74 start-page: 175 year: 1973 ident: 2023040109511895500_ article-title: Distribution of gene frequencey as a test of the theory of selective neutrality of polymorphisms publication-title: Genetics doi: 10.1093/genetics/74.1.175 – volume: 280 start-page: 1077 year: 1998 ident: 2023040109511895500_ article-title: Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome publication-title: Science doi: 10.1126/science.280.5366.1077 – volume: 84 start-page: 8512 year: 1987 ident: 2023040109511895500_ article-title: Correlations, descent measures: drift with migration and mutation publication-title: Proc. 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Eugen. – volume: 78 start-page: 583 year: 1997 ident: 2023040109511895500_ article-title: Significant genetic correlations among Caucasians at forensic DNA loci publication-title: Heredity doi: 10.1038/hdy.1997.97 – volume: 158 start-page: 885 year: 2001 ident: 2023040109511895500_ article-title: Distinguishing migration from isolation: a markov chain monte carlo approach publication-title: Genetics doi: 10.1093/genetics/158.2.885 – volume: 96 start-page: 3 year: 1995 ident: 2023040109511895500_ article-title: A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity publication-title: Genetica doi: 10.1007/BF01441146 – volume: 69 start-page: 1332 year: 2001 ident: 2023040109511895500_ article-title: The discovery of single-nucleotide polymorphisms—and inferences about human demographic history publication-title: Am. J. Hum. 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| SubjectTerms | Bayes estimators Biological and medical sciences Bottleneck Chromosomes Coalescent Datasets Demography Estimation Estimators Exact sciences and technology Fixation indices Forensic genetics France Fundamental and applied biological sciences. Psychology Gene frequency General aspects Genetic loci Human genetics Iceland Inference from stochastic processes; time series analysis Markov chain Monte Carlo methods Markov processes Markovian processes Mathematics Mathematics in biology. Statistical analysis. Models. Metrology. Data processing in biology (general aspects) Monte Carlo simulation Population Population genetics Population histories Population parameters Probability and statistics Probability theory and stochastic processes Sciences and techniques of general use Statistical methods Statistical models Statistics Sufficiency and information U.S.A Utah |
| Title | Assessing population differentiation and isolation from single-nucleotide polymorphism data |
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