Abstract
The genetic study of diverging, closely related populations is required for basic questions on demography and speciation, as well as for biodiversity and conservation research. However, it is often unclear whether divergence is due simply to separation or whether populations have also experienced gene flow. These questions can be addressed with a full model of population separation with gene flow, by applying a Markov chain Monte Carlo method for estimating the posterior probability distribution of model parameters. We have generalized this method and made it applicable to data from multiple unlinked loci. These loci can vary in their modes of inheritance, and inheritance scalars can be implemented either as constants or as parameters to be estimated. By treating inheritance scalars as parameters it is also possible to address variation among loci in the impact via linkage of recurrent selective sweeps or background selection. These methods are applied to a large multilocus data set from Drosophila pseudoobscura and D. persimilis. The species are estimated to have diverged approximately 500,000 years ago. Several loci have nonzero estimates of gene flow since the initial separation of the species, with considerable variation in gene flow estimates among loci, in both directions between the species.
Full Text
The Full Text of this article is available as a PDF (275.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aquadro C. F., Weaver A. L., Schaeffer S. W., Anderson W. W. Molecular evolution of inversions in Drosophila pseudoobscura: the amylase gene region. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):305–309. doi: 10.1073/pnas.88.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bahlo M., Griffiths R. C. Inference from gene trees in a subdivided population. Theor Popul Biol. 2000 Mar;57(2):79–95. doi: 10.1006/tpbi.1999.1447. [DOI] [PubMed] [Google Scholar]
- Beerli P., Felsenstein J. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics. 1999 Jun;152(2):763–773. doi: 10.1093/genetics/152.2.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
- Brunet Michel, Guy Franck, Pilbeam David, Mackaye Hassane Taisso, Likius Andossa, Ahounta Djimdoumalbaye, Beauvilain Alain, Blondel Cécile, Bocherens Hervé, Boisserie Jean-Renaud. A new hominid from the Upper Miocene of Chad, Central Africa. Nature. 2002 Jul 11;418(6894):145–151. doi: 10.1038/nature00879. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen F. C., Li W. H. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet. 2001 Jan 15;68(2):444–456. doi: 10.1086/318206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillespie J. H. Genetic drift in an infinite population. The pseudohitchhiking model. Genetics. 2000 Jun;155(2):909–919. doi: 10.1093/genetics/155.2.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–174. doi: 10.1007/BF02101694. [DOI] [PubMed] [Google Scholar]
- Hey Jody, Machado Carlos A. The study of structured populations--new hope for a difficult and divided science. Nat Rev Genet. 2003 Jul;4(7):535–543. doi: 10.1038/nrg1112. [DOI] [PubMed] [Google Scholar]
- Hey Jody, Won Yong-Jin, Sivasundar Arjun, Nielsen Rasmus, Markert Jeffrey A. Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol. 2004 Apr;13(4):909–919. doi: 10.1046/j.1365-294x.2003.02031.x. [DOI] [PubMed] [Google Scholar]
- Hudson R. R. The sampling distribution of linkage disequilibrium under an infinite allele model without selection. Genetics. 1985 Mar;109(3):611–631. doi: 10.1093/genetics/109.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M. The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics. 1969 Apr;61(4):893–903. doi: 10.1093/genetics/61.4.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M, Weiss G H. The Stepping Stone Model of Population Structure and the Decrease of Genetic Correlation with Distance. Genetics. 1964 Apr;49(4):561–576. doi: 10.1093/genetics/49.4.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kliman R. M., Andolfatto P., Coyne J. A., Depaulis F., Kreitman M., Berry A. J., McCarter J., Wakeley J., Hey J. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics. 2000 Dec;156(4):1913–1931. doi: 10.1093/genetics/156.4.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuhner M. K., Yamato J., Felsenstein J. Maximum likelihood estimation of recombination rates from population data. Genetics. 2000 Nov;156(3):1393–1401. doi: 10.1093/genetics/156.3.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Machado Carlos A., Hey Jody. The causes of phylogenetic conflict in a classic Drosophila species group. Proc Biol Sci. 2003 Jun 7;270(1520):1193–1202. doi: 10.1098/rspb.2003.2333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Machado Carlos A., Kliman Richard M., Markert Jeffrey A., Hey Jody. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol Biol Evol. 2002 Apr;19(4):472–488. doi: 10.1093/oxfordjournals.molbev.a004103. [DOI] [PubMed] [Google Scholar]
- Nielsen R. A likelihood approach to populations samples of microsatellite alleles. Genetics. 1997 Jun;146(2):711–716. doi: 10.1093/genetics/146.2.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nielsen R. Estimation of population parameters and recombination rates from single nucleotide polymorphisms. Genetics. 2000 Feb;154(2):931–942. doi: 10.1093/genetics/154.2.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nielsen R. Maximum likelihood estimation of population divergence times and population phylogenies under the infinite sites model. Theor Popul Biol. 1998 Apr;53(2):143–151. doi: 10.1006/tpbi.1997.1348. [DOI] [PubMed] [Google Scholar]
- Nielsen R., Slatkin M. Likelihood analysis of ongoing gene flow and historical association. Evolution. 2000 Feb;54(1):44–50. doi: 10.1111/j.0014-3820.2000.tb00006.x. [DOI] [PubMed] [Google Scholar]
- Nielsen R., Wakeley J. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics. 2001 Jun;158(2):885–896. doi: 10.1093/genetics/158.2.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noor M. A., Grams K. L., Bertucci L. A., Almendarez Y., Reiland J., Smith K. R. The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution. 2001 Mar;55(3):512–521. doi: 10.1554/0014-3820(2001)055[0512:tgoria]2.0.co;2. [DOI] [PubMed] [Google Scholar]
- Noor M. A., Grams K. L., Bertucci L. A., Reiland J. Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci U S A. 2001 Oct 2;98(21):12084–12088. doi: 10.1073/pnas.221274498. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palsbøll Per J., Bérubé Martine, Aguilar Alex, Notarbartolo-Di-Sciara Giuseppe, Nielsen Rasmus. Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. Evolution. 2004 Mar;58(3):670–675. [PubMed] [Google Scholar]
- Rannala Bruce, Yang Ziheng. Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics. 2003 Aug;164(4):1645–1656. doi: 10.1093/genetics/164.4.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slatkin M., Maddison W. P. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics. 1989 Nov;123(3):603–613. doi: 10.1093/genetics/123.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- Takahata N., Slatkin M. Genealogy of neutral genes in two partially isolated populations. Theor Popul Biol. 1990 Dec;38(3):331–350. doi: 10.1016/0040-5809(90)90018-q. [DOI] [PubMed] [Google Scholar]
- Wakeley J. Distinguishing migration from isolation using the variance of pairwise differences. Theor Popul Biol. 1996 Jun;49(3):369–386. doi: 10.1006/tpbi.1996.0018. [DOI] [PubMed] [Google Scholar]
- Wakeley J., Hey J. Estimating ancestral population parameters. Genetics. 1997 Mar;145(3):847–855. doi: 10.1093/genetics/145.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang R. L., Hey J. The speciation history of Drosophila pseudoobscura and close relatives: inferences from DNA sequence variation at the period locus. Genetics. 1996 Nov;144(3):1113–1126. doi: 10.1093/genetics/144.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang R. L., Wakeley J., Hey J. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics. 1997 Nov;147(3):1091–1106. doi: 10.1093/genetics/147.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson I. J., Balding D. J. Genealogical inference from microsatellite data. Genetics. 1998 Sep;150(1):499–510. doi: 10.1093/genetics/150.1.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wright S. Evolution in Mendelian Populations. Genetics. 1931 Mar;16(2):97–159. doi: 10.1093/genetics/16.2.97. [DOI] [PMC free article] [PubMed] [Google Scholar]