Abstract
To study the genetic differences responsible for the sterility of their male hybrids, we introgressed small segments of an X chromosome from Drosophila simulans into a pure Drosophila mauritiana genetic background, then assessed the fertility of males carrying heterospecific introgressions of varying size. Although this analysis examined less than 20% of the X chromosome (roughly 5% of the euchromatic portion of the D. simulans genome), and the segments were introgressed in only one direction, a minimum of four factors that contribute to hybrid male sterility were revealed. At least two of the factors exhibited strong epistasis: males carrying either factor alone were consistently fertile, whereas males carrying both factors together were always sterile. Distinct spermatogenic phenotypes were observed for sterile introgressions of different lengths, and it appeared that an interaction between introgressed segments also influenced the stage of spermatogenic defect. Males with one category of introgression often produced large quantities of motile sperm and were observed copulating, but never inseminated females. Evidently these two species have diverged at a large number of loci which have varied effects on hybrid male fertility. By extrapolation, we estimate that there are at least 40 such loci on the X chromosome alone. Because these species exhibit little DNA-sequence divergence at arbitrarily chosen loci, it seems unlikely that the extensive functional divergence observed could be due mainly to random genetic drift. Significant epistasis between conspecific genes appears to be a common component of hybrid sterility between recently diverged species of Drosophila. The linkage relationships of interacting factors could shed light on the role played by epistatic selection in the dynamics of the allele substitutions responsible for reproductive barriers between species.
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- Barker J. S. Inter-locus interactions: a review of experimental evidence. Theor Popul Biol. 1979 Dec;16(3):323–346. doi: 10.1016/0040-5809(79)90021-2. [DOI] [PubMed] [Google Scholar]
- Barton N. H., Turelli M. Evolutionary quantitative genetics: how little do we know? Annu Rev Genet. 1989;23:337–370. doi: 10.1146/annurev.ge.23.120189.002005. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Coyne J. A. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. doi: 10.1038/355511a0. [DOI] [PubMed] [Google Scholar]
- Davis A. W., Noonburg E. G., Wu C. I. Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. Genetics. 1994 May;137(1):191–199. doi: 10.1093/genetics/137.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heikkinen E., Lumme J. Sterility of male and female hybrids of Drosophila virilis and Drosophila lummei. Heredity (Edinb) 1991 Aug;67(Pt 1):1–11. doi: 10.1038/hdy.1991.58. [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]
- Hutter P., Ashburner M. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. 1987 May 28-Jun 3Nature. 327(6120):331–333. doi: 10.1038/327331a0. [DOI] [PubMed] [Google Scholar]
- Hutter P., Roote J., Ashburner M. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics. 1990 Apr;124(4):909–920. doi: 10.1093/genetics/124.4.909. [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]
- Kemphues K. J., Kaufman T. C., Raff R. A., Raff E. C. The testis-specific beta-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell. 1982 Dec;31(3 Pt 2):655–670. doi: 10.1016/0092-8674(82)90321-x. [DOI] [PubMed] [Google Scholar]
- Khadem M., Krimbas C. B. Studies of the species barrier between Drosophila subobscura and D. madeirensis. I. The genetics of male hybrid sterility. Heredity (Edinb) 1991 Oct;67(Pt 2):157–165. doi: 10.1038/hdy.1991.75. [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]
- LEFEVRE G., Jr, JONSSON U. B. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics. 1962 Dec;47:1719–1736. doi: 10.1093/genetics/47.12.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lemeunier F., Ashburner M. A. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proc R Soc Lond B Biol Sci. 1976 May 18;193(1112):275–294. doi: 10.1098/rspb.1976.0046. [DOI] [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]
- Nei M., Maruyama T., Wu C. I. Models of evolution of reproductive isolation. Genetics. 1983 Mar;103(3):557–579. doi: 10.1093/genetics/103.3.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perez D. E., Wu C. I., Johnson N. A., Wu M. L. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics. 1993 May;134(1):261–275. doi: 10.1093/genetics/134.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Templeton A. R. The theory of speciation via the founder principle. Genetics. 1980 Apr;94(4):1011–1038. doi: 10.1093/genetics/94.4.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wade M. J., Goodnight C. J. Wright's shifting balance theory: an experimental study. Science. 1991 Aug 30;253(5023):1015–1018. doi: 10.1126/science.1887214. [DOI] [PubMed] [Google Scholar]
- Wade M. J., Johnson N. A. Reproductive isolation between two species of flour beetles, Tribolium castaneum and T. freemani: variation within and among geographical populations of T. castaneum. Heredity (Edinb) 1994 Feb;72(Pt 2):155–162. doi: 10.1038/hdy.1994.22. [DOI] [PubMed] [Google Scholar]
- Wittbrodt J., Adam D., Malitschek B., Mäueler W., Raulf F., Telling A., Robertson S. M., Schartl M. Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature. 1989 Oct 5;341(6241):415–421. doi: 10.1038/341415a0. [DOI] [PubMed] [Google Scholar]
- Zapata C., Alvarez G. On the detection of nonrandom associations between DNA polymorphisms in natural populations of Drosophila. Mol Biol Evol. 1993 Jul;10(4):823–841. doi: 10.1093/oxfordjournals.molbev.a040045. [DOI] [PubMed] [Google Scholar]
- Zouros E. The chromosomal basis of sexual isolation in two sibling species of Drosophila: D. arizonensis and D. mojavensis. Genetics. 1981 Mar-Apr;97(3-4):703–718. doi: 10.1093/genetics/97.3-4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]