Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1994 May;137(1):175–189. doi: 10.1093/genetics/137.1.175

Genetics of Reproductive Isolation in the Drosophila Simulans Clade: Complex Epistasis Underlying Hybrid Male Sterility

E L Cabot 1, A W Davis 1, N A Johnson 1, C I Wu 1
PMCID: PMC1205934  PMID: 8056308

Abstract

We have analyzed the sterility associated with introgressions of the distal one-fourth of the X chromosome from either Drosophila mauritiana or Drosophila sechellia into the genome of Drosophila simulans using a series of visible and DNA markers. Because in Drosophila hybrids, male sterility is usually complete and is often tightly linked with each of several markers used in crosses, a simple genetic basis has generally been assumed. In our low resolution mapping experiment, we were not able to reject the null hypothesis that a single gene, introgressed from either D. mauritiana or D. sechellia, is the cause of male sterility. High resolution mapping, however, reveals a much more complex picture. At least three distinct factors from D. mauritiana, or two from D. sechellia, were identified that need to be jointly present to confer full sterility. Each individual factor by itself is relatively ineffective in causing sterility, or even a partial spermatogenic defect. Moreover, there appear to be more sterility factors on comparable introgressions from D. mauritiana than from D. sechellia. On the basis of these observations, we propose a model which suggests that multilocus weak allele interactions are a very common cause of reproductive incompatibility between closely related species. We also present theoretical argument and empirical evidence against extrapolating the results of within-species analysis to interpret the genetic basis of species differences. The implications of this model on the theories of evolution of species differences and the attempt to understand the mechanisms of hybrid sterility/inviability at the molecular level are discussed.

Full Text

The Full Text of this article is available as a PDF (4.8 MB).

Selected References

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

  1. Brady J. P., Richmond R. C. Molecular analysis of evolutionary changes in the expression of Drosophila esterases. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8217–8221. doi: 10.1073/pnas.87.21.8217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Castrillon D. H., Gönczy P., Alexander S., Rawson R., Eberhart C. G., Viswanathan S., DiNardo S., Wasserman S. A. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. doi: 10.1093/genetics/135.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  6. Fyrberg E. A., Kindle K. L., Davidson N., Kindle K. L. The actin genes of Drosophila: a dispersed multigene family. Cell. 1980 Feb;19(2):365–378. doi: 10.1016/0092-8674(80)90511-5. [DOI] [PubMed] [Google Scholar]
  7. GRISOLIA S., BURRIS R. H., COHEN P. P. Carbon dioxide and ammonia fixation in the biosynthesis of citrulline. J Biol Chem. 1951 Jul;191(1):203–209. [PubMed] [Google Scholar]
  8. Hennig W. Gene interactions in germ differentiation of Drosophila. Adv Enzyme Regul. 1976;15:363–371. doi: 10.1016/0065-2571(77)90025-5. [DOI] [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. 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]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. Mohler J. D. Developmental genetics of the Drosophila egg. I. Identification of 59 sex-linked cistrons with maternal effects on embryonic development. Genetics. 1977 Feb;85(2):259–272. doi: 10.1093/genetics/85.2.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mounkes L. C., Jones R. S., Liang B. C., Gelbart W., Fuller M. T. A Drosophila model for xeroderma pigmentosum and Cockayne's syndrome: haywire encodes the fly homolog of ERCC3, a human excision repair gene. Cell. 1992 Dec 11;71(6):925–937. doi: 10.1016/0092-8674(92)90389-t. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Naveira H., Fontdevila A. The Evolutionary History of DROSOPHILA BUZZATII. Xii. the Genetic Basis of Sterility in Hybrids between D. BUZZATII and Its Sibling D. SERIDO from Argentina. Genetics. 1986 Nov;114(3):841–857. doi: 10.1093/genetics/114.3.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orita M., Suzuki Y., Sekiya T., Hayashi K. Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics. 1989 Nov;5(4):874–879. doi: 10.1016/0888-7543(89)90129-8. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Pantazidis A. C., Galanopoulos V. K., Zouros E. An autosomal factor from Drosophila arizonae restores normal spermatogenesis in Drosophila mojavensis males carrying the D. arizonae Y chromosome. Genetics. 1993 May;134(1):309–318. doi: 10.1093/genetics/134.1.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Regan C. L., Fuller M. T. Interacting genes that affect microtubule function in Drosophila melanogaster: two classes of mutation revert the failure to complement between haync2 and mutations in tubulin genes. Genetics. 1990 May;125(1):77–90. doi: 10.1093/genetics/125.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Regan C. L., Fuller M. T. Interacting genes that affect microtubule function: the nc2 allele of the haywire locus fails to complement mutations in the testis-specific beta-tubulin gene of Drosophila. Genes Dev. 1988 Jan;2(1):82–92. doi: 10.1101/gad.2.1.82. [DOI] [PubMed] [Google Scholar]
  25. Sawamura K., Yamamoto M. T. Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality. Mol Gen Genet. 1993 Jun;239(3):441–449. doi: 10.1007/BF00276943. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Seeger M. A., Kaufman T. C. Molecular analysis of the bicoid gene from Drosophila pseudoobscura: identification of conserved domains within coding and noncoding regions of the bicoid mRNA. EMBO J. 1990 Sep;9(9):2977–2987. doi: 10.1002/j.1460-2075.1990.tb07490.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  29. Stephenson E. C., Mahowald A. P. Isolation of Drosophila clones encoding maternally restricted RNAs. Dev Biol. 1987 Nov;124(1):1–8. doi: 10.1016/0012-1606(87)90453-2. [DOI] [PubMed] [Google Scholar]
  30. Vigoreaux J. O., Tobin S. L. Stage-specific selection of alternative transcriptional initiation sites from the 5C actin gene of Drosophila melanogaster. Genes Dev. 1987 Dec;1(10):1161–1171. doi: 10.1101/gad.1.10.1161. [DOI] [PubMed] [Google Scholar]
  31. Wu C. I., Beckenbach A. T. Evidence for Extensive Genetic Differentiation between the Sex-Ratio and the Standard Arrangement of DROSOPHILA PSEUDOOBSCURA and D. PERSIMILIS and Identification of Hybrid Sterility Factors. Genetics. 1983 Sep;105(1):71–86. doi: 10.1093/genetics/105.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zeng L. W., Singh R. S. A combined classical genetic and high resolution two-dimensional electrophoretic approach to the assessment of the number of genes affecting hybrid male sterility in Drosophila simulans and Drosophila sechellia. Genetics. 1993 Sep;135(1):135–147. doi: 10.1093/genetics/135.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES