Abstract
According to measures of molecular divergence, the three species of the Drosophila simulans clade are closely related to and essentially equidistant from each other. We introgressed 10% of the D. sechellia X chromosome into a pure D. simulans genetic background and found that males carrying this introgressed region were consistently fertile; in contrast, males carrying the same segment from D. mauritiana are sterile and suffer from incompatibilities at a minimum of four loci. Together with other recent results, these data suggest that D. simulans and D. sechellia are much more closely related to each other than either is to D. mauritiana. How can we reconcile the phylogeny inferred from the density of hybrid sterility genes with that inferred from molecular divergence? If the molecular phylogeny is correct, the discrepancy might be explained by uneven rates of functional evolution, resulting in the uneven accumulation of substitutions with corresponding negative effects in hybrids. If the functional phylogeny is correct, then low levels of gene flow across nascent species boundaries, particularly for loci not tightly linked to a hybrid sterility gene, may have erased the original pattern of lineage splitting. We propose tests that will allow us to discriminate between these hypotheses.
Full Text
The Full Text of this article is available as a PDF (839.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Cabot E. L., Davis A. W., Johnson N. A., Wu C. I. Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics. 1994 May;137(1):175–189. doi: 10.1093/genetics/137.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Caccone A., Amato G. D., Powell J. R. Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics. 1988 Apr;118(4):671–683. doi: 10.1093/genetics/118.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cariou M. L. Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena. Genet Res. 1987 Dec;50(3):181–185. doi: 10.1017/s0016672300023673. [DOI] [PubMed] [Google Scholar]
- Coyne J. A., Charlesworth B. Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila. Heredity (Edinb) 1989 Feb;62(Pt 1):97–106. doi: 10.1038/hdy.1989.13. [DOI] [PubMed] [Google Scholar]
- Coyne J. A., Charlesworth B. Location of an X-linked factor causing sterility in male hybrids of Drosophila simulans and D. mauritiana. Heredity (Edinb) 1986 Oct;57(Pt 2):243–246. doi: 10.1038/hdy.1986.114. [DOI] [PubMed] [Google Scholar]
- Davis A. W., Wu C. I. The broom of the sorcerer's apprentice: the fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics. 1996 Jul;143(3):1287–1298. doi: 10.1093/genetics/143.3.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischman J. Evidence mounts for our African origins--and alternatives. Science. 1996 Mar 8;271(5254):1364–1364. doi: 10.1126/science.271.5254.1364. [DOI] [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]
- Hollocher H., Wu C. I. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics. 1996 Jul;143(3):1243–1255. doi: 10.1093/genetics/143.3.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson N. A., Hollocher H., Noonburg E., Wu C. I. The effects of interspecific Y chromosome replacements on hybrid sterility within the Drosophila simulans clade. Genetics. 1993 Oct;135(2):443–453. doi: 10.1093/genetics/135.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson N. A., Perez D. E., Cabot E. L., Hollocher H., Wu C. I. A test of reciprocal X-Y interactions as a cause of hybrid sterility in Drosophila. Nature. 1992 Aug 27;358(6389):751–753. doi: 10.1038/358751a0. [DOI] [PubMed] [Google Scholar]
- King M. C., Wilson A. C. Evolution at two levels in humans and chimpanzees. Science. 1975 Apr 11;188(4184):107–116. doi: 10.1126/science.1090005. [DOI] [PubMed] [Google Scholar]
- Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Naveira H. F. Location of X-linked polygenic effects causing sterility in male hybrids of Drosophila simulans and D. mauritiana. Heredity (Edinb) 1992 Mar;68(Pt 3):211–217. doi: 10.1038/hdy.1992.34. [DOI] [PubMed] [Google Scholar]
- Orr H. A. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995 Apr;139(4):1805–1813. doi: 10.1093/genetics/139.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palopoli M. F., Wu C. I. Genetics of hybrid male sterility between drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics. 1994 Oct;138(2):329–341. doi: 10.1093/genetics/138.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- R'Kha S., Capy P., David J. R. Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1835–1839. doi: 10.1073/pnas.88.5.1835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satta Y., Takahata N. Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9558–9562. doi: 10.1073/pnas.87.24.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahata N. Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics. 1989 Aug;122(4):957–966. doi: 10.1093/genetics/122.4.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tishkoff S. A., Dietzsch E., Speed W., Pakstis A. J., Kidd J. R., Cheung K., Bonné-Tamir B., Santachiara-Benerecetti A. S., Moral P., Krings M. Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science. 1996 Mar 8;271(5254):1380–1387. doi: 10.1126/science.271.5254.1380. [DOI] [PubMed] [Google Scholar]
- Wilson A. C., Maxson L. R., Sarich V. M. Two types of molecular evolution. Evidence from studies of interspecific hybridization. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2843–2847. doi: 10.1073/pnas.71.7.2843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson A. C., Sarich V. M., Maxson L. R. The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3028–3030. doi: 10.1073/pnas.71.8.3028. [DOI] [PMC free article] [PubMed] [Google Scholar]