Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Nov;150(3):1091–1103. doi: 10.1093/genetics/150.3.1091

Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans.

J A Coyne 1, S Simeonidis 1, P Rooney 1
PMCID: PMC1460387  PMID: 9799261

Abstract

Using deficiencies from Drosophila melanogaster, we looked for genomic regions in the sister species D. simulans that could cause lethality when hemizygous on a hybrid genetic background. Such genotypes allow hemizygous genes from one species to interact with heterozygous genes from other species and may correspond to the kinds of genotypes causing Haldane's rule, the observation that if only one gender is sterile or inviable in species hybrids, it is nearly always the heterogametic sex. A survey of roughly 50% of the D. simulans genome (114 chromosome regions) revealed only four regions causing hybrid lethality and five causing severe reductions in hybrid viability. However, the viability of all of these genotypes was at least partially restored by rearing hybrids at lower temperature or using different genetic backgrounds from D. simulans. We therefore detected no D. simulans chromosome regions causing unconditional hybrid lethality, although several regions were shown to be deleterious under most tested temperatures and genetic backgrounds. The relative paucity of "inviability genes" supports the idea, suggested by work on other species, that hybrid inviability between closely related species might be caused by interactions among relatively few genes, while hybrid sterility may involve many more loci.

Full Text

The Full Text of this article is available as a PDF (140.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Carvajal A. R., Gandarela M. R., Naveira H. F. A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae. Genetica. 1996 Jul;98(1):1–19. doi: 10.1007/BF00120214. [DOI] [PubMed] [Google Scholar]
  2. Coyne J. A., Beecham E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):727–737. doi: 10.1093/genetics/117.4.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Coyne J. A., Charlesworth B. Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia. Genetics. 1997 Apr;145(4):1015–1030. doi: 10.1093/genetics/145.4.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Coyne J. A. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. doi: 10.1038/355511a0. [DOI] [PubMed] [Google Scholar]
  5. Coyne J. A. Genetics of differences in pheromonal hydrocarbons between Drosophila melanogaster and D. simulans. Genetics. 1996 May;143(1):353–364. doi: 10.1093/genetics/143.1.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coyne J. A., Orr H. A. The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):287–305. doi: 10.1098/rstb.1998.0210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis A. W., Roote J., Morley T., Sawamura K., Herrmann S., Ashburner M. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature. 1996 Mar 14;380(6570):157–159. doi: 10.1038/380157a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. Hutter P. Genetics of hybrid inviability in Drosophila. Adv Genet. 1997;36:157–185. doi: 10.1016/s0065-2660(08)60309-0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Laurie C. C. The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics. 1997 Nov;147(3):937–951. doi: 10.1093/genetics/147.3.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ohnishi S., Leigh Brown A. J., Voelker R. A., Langley C. H. Estimation of genetic variability in natural populations of Drosophila simulans by two-dimensional and starch gel electrophoresis. Genetics. 1982 Jan;100(1):127–136. doi: 10.1093/genetics/100.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Orr H. A., Madden L. D., Coyne J. A., Goodwin R., Hawley R. S. The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics. 1997 Apr;145(4):1031–1040. doi: 10.1093/genetics/145.4.1031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Orr H. A. Mapping and characterization of a 'speciation gene' in Drosophila. Genet Res. 1992 Apr;59(2):73–80. doi: 10.1017/s0016672300030275. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Orr H. A. The unexpected recovery of hybrids in a Drosophila species cross: a genetic analysis. Genet Res. 1996 Feb;67(1):11–18. doi: 10.1017/s0016672300033437. [DOI] [PubMed] [Google Scholar]
  20. Orr H. A., Turelli M. Dominance and Haldane's rule. Genetics. 1996 May;143(1):613–616. doi: 10.1093/genetics/143.1.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Perez D. E., Wu C. I. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics. 1995 May;140(1):201–206. doi: 10.1093/genetics/140.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Quackenbush L. S. UNISEXUAL BROODS OF DROSOPHILA. Science. 1910 Aug 5;32(814):183–185. doi: 10.1126/science.32.814.183. [DOI] [PubMed] [Google Scholar]
  23. Sawamura K., Taira T., Watanabe T. K. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics. 1993 Feb;133(2):299–305. doi: 10.1093/genetics/133.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sawamura K., Yamamoto M. T., Watanabe T. K. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of D. melanogaster. Genetics. 1993 Feb;133(2):307–313. doi: 10.1093/genetics/133.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sturtevant A H. Genetic Studies on DROSOPHILA SIMULANS. I. Introduction. Hybrids with DROSOPHILA MELANOGASTER. Genetics. 1920 Sep;5(5):488–500. doi: 10.1093/genetics/5.5.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. True J. R., Weir B. S., Laurie C. C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics. 1996 Mar;142(3):819–837. doi: 10.1093/genetics/142.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Turelli M., Begun D. J. Haldane's rule and X-chromosome size in Drosophila. Genetics. 1997 Dec;147(4):1799–1815. doi: 10.1093/genetics/147.4.1799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Turelli M., Orr H. A. The dominance theory of Haldane's rule. Genetics. 1995 May;140(1):389–402. doi: 10.1093/genetics/140.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yamamoto M. T. Inviability of hybrids between D. melanogaster and D. simulans results from the absence of simulans X not the presence of simulans Y chromosome. Genetica. 1992;87(3):151–158. doi: 10.1007/BF00240554. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES