Abstract
The divergence of Drosophila pseudoobscura and close relatives D. persimilis and D. pseudoobscura bogotana has been studied using comparative DNA sequence data from multiple nuclear loci. New data from the Hsp82 and Adh regions, in conjunction with existing data from Adh and the Period locus, are examined in the light of various models of speciation. The principal finding is that the three loci present very different histories, with Adh indicating large amounts of recent gene flow among the taxa, while little or no gene flow is apparent in the data from the other loci. The data were compared with predictions from several isolation models of divergence. These models include no gene flow, and they were found to be incompatible with the data. Instead the DNA data, taken together with other evidence, seem consistent with divergence models in which natural selection acts against gene flow at some loci more than at others. This family of models includes some sympatric and parapatric speciation models, as well as models of secondary contact and subsequent reinforcement of sexual isolation.
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- Anderson W. W., Ayala F. J., Michod R. E. Chromosomal and allozymic diagnosis of three species of Drosophila. Drosophila pseudoobscura, D. persimilis, and D. miranda. J Hered. 1977 Mar-Apr;68(2):71–74. doi: 10.1093/oxfordjournals.jhered.a108793. [DOI] [PubMed] [Google Scholar]
- Barrio E., Latorre A., Moya A., Ayala F. J. Phylogenetic reconstruction of the Drosophila obscura group, on the basis of mitochondrial DNA. Mol Biol Evol. 1992 Jul;9(4):621–635. doi: 10.1093/oxfordjournals.molbev.a040749. [DOI] [PubMed] [Google Scholar]
- Blackman R. K., Meselson M. Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol. 1986 Apr 20;188(4):499–515. doi: 10.1016/s0022-2836(86)80001-8. [DOI] [PubMed] [Google Scholar]
- DOBZHANSKY T., HUNTER A. S., PAVLOVSKY O., SPASSKY B., WALLACE B. Genetics of natural populations. XXXI. Genetics of an isolated marginal population of Drosophila pseudoobscura. Genetics. 1963 Jan;48:91–103. doi: 10.1093/genetics/48.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
- Hey J. The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics. 1991 Aug;128(4):831–840. doi: 10.1093/genetics/128.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hey J., Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. doi: 10.1093/genetics/145.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson R. R. Properties of a neutral allele model with intragenic recombination. Theor Popul Biol. 1983 Apr;23(2):183–201. doi: 10.1016/0040-5809(83)90013-8. [DOI] [PubMed] [Google Scholar]
- Kaplan N. L., Darden T., Hudson R. R. The coalescent process in models with selection. Genetics. 1988 Nov;120(3):819–829. doi: 10.1093/genetics/120.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noor M. A. Speciation driven by natural selection in Drosophila. Nature. 1995 Jun 22;375(6533):674–675. doi: 10.1038/375674a0. [DOI] [PubMed] [Google Scholar]
- Orr H. A. Localization of genes causing postzygotic isolation in two hybridizations involving Drosophila pseudoobscura. Heredity (Edinb) 1989 Oct;63(Pt 2):231–237. doi: 10.1038/hdy.1989.96. [DOI] [PubMed] [Google Scholar]
- Powell J. R. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci U S A. 1983 Jan;80(2):492–495. doi: 10.1073/pnas.80.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prakash S. Origin of reproductive isolation in the absence of apparent genic differentiation in a geographic isolate of Drosophila pseudoobscura. Genetics. 1972 Sep;72(1):143–155. doi: 10.1093/genetics/72.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prost E., Moore D. D. CAT vectors for analysis of eukaryotic promoters and enhancers. Gene. 1986;45(1):107–111. doi: 10.1016/0378-1119(86)90138-1. [DOI] [PubMed] [Google Scholar]
- RIZKI M. T. M. Morphological differences between two sibling species; Drosophila pseudoobscura and Drosophila persimilis. Proc Natl Acad Sci U S A. 1951 Mar;37(3):156–159. doi: 10.1073/pnas.37.3.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaeffer S. W., Aquadro C. F. Nucleotide sequence of the Adh gene region of Drosophila pseudoobscura: evolutionary change and evidence for an ancient gene duplication. Genetics. 1987 Sep;117(1):61–73. doi: 10.1093/genetics/117.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaeffer S. W., Miller E. L. Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics. 1993 Oct;135(2):541–552. doi: 10.1093/genetics/135.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaeffer S. W., Miller E. L. Molecular population genetics of an electrophoretically monomorphic protein in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics. 1992 Sep;132(1):163–178. doi: 10.1093/genetics/132.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaeffer S. W., Miller E. L. Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6097–6101. doi: 10.1073/pnas.88.14.6097. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Segarra C., Lozovskaya E. R., Ribó G., Aguadé M., Hartl D. L. P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller's A element in two species of the obscura group of Drosophila. Chromosoma. 1995 Nov;104(2):129–136. doi: 10.1007/BF00347695. [DOI] [PubMed] [Google Scholar]
- Segarra C., Ribó G., Aguadé M. Differentiation of Muller's chromosomal elements D and E in the obscura group of Drosophila. Genetics. 1996 Sep;144(1):139–146. doi: 10.1093/genetics/144.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. On the rate of DNA sequence evolution in Drosophila. J Mol Evol. 1989 May;28(5):398–402. doi: 10.1007/BF02603075. [DOI] [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]
- Takahata N., Nei M. Gene genealogy and variance of interpopulational nucleotide differences. Genetics. 1985 Jun;110(2):325–344. doi: 10.1093/genetics/110.2.325. [DOI] [PMC free article] [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]
- Wakeley J. The variance of pairwise nucleotide differences in two populations with migration. Theor Popul Biol. 1996 Feb;49(1):39–57. doi: 10.1006/tpbi.1996.0002. [DOI] [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]
- 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]