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. 1996 Jul;143(3):1287–1298. doi: 10.1093/genetics/143.3.1287

The Broom of the Sorcerer's Apprentice: The Fine Structure of a Chromosomal Region Causing Reproductive Isolation between Two Sibling Species of Drosophila

A W Davis 1, C I Wu 1
PMCID: PMC1207397  PMID: 8807300

Abstract

How many genes contribute to reproductive isolation between closely related species? We determined the number of genes located in the 9D-12B region of the Drosophila mauritiana X chromosome that cause hybrid male sterility in a D. simulans background. Previous low resolution studies suggested that a single hybrid sterility factor was associated with this region. In this study, by taking advantage of a cluster of visible and DNA markers, we identified three D. mauritiana factors in this region and then subjected one of them to detailed analysis. This factor again turned out to be comprised of three factors; one of which, mapped to within 200 kb, may in fact be two factors. The title refers to this exercise of splitting sterile introgressions into ever smaller ones, each of which retains partial or full sterility effects. In a region representing a mere 3% of the Drosophila genome, no fewer than six loci of hybrid sterility were identified between two sibling species that have not shown clear divergence at the molecular level. These results suggest that levels of genetic divergence between closely related species may be quite high for functionally important traits even when the opposite is true for randomly chosen loci.

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Selected References

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  1. Begun D. J., Aquadro C. F. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. doi: 10.1038/365548a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Cooley L., Berg C., Spradling A. Controlling P element insertional mutagenesis. Trends Genet. 1988 Sep;4(9):254–258. doi: 10.1016/0168-9525(88)90032-7. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Coyne J. A. Genetic basis of male sterility in hybrids between two closely related species of Drosophila. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4444–4447. doi: 10.1073/pnas.81.14.4444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eijgenraam F. Yeast chromosome III reveals a wealth of unknown genes. Science. 1992 May 8;256(5058):730–730. doi: 10.1126/science.1589748. [DOI] [PubMed] [Google Scholar]
  7. Garabedian M. J., Shirras A. D., Bownes M., Wensink P. C. The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene. 1987;55(1):1–8. doi: 10.1016/0378-1119(87)90242-3. [DOI] [PubMed] [Google Scholar]
  8. Gertler F. B., Doctor J. S., Hoffmann F. M. Genetic suppression of mutations in the Drosophila abl proto-oncogene homolog. Science. 1990 May 18;248(4957):857–860. doi: 10.1126/science.2188361. [DOI] [PubMed] [Google Scholar]
  9. Hennig W. Untersuchungen zur Struktur und Funktion des Lampenbürsten-Y-Chromosoms in der Spermatogenese von Drosophila. Chromosoma. 1967;22(3):294–357. doi: 10.1007/BF00319879. [DOI] [PubMed] [Google Scholar]
  10. Hill K. K., Bedian V., Juang J. L., Hoffmann F. M. Genetic interactions between the Drosophila Abelson (Abl) tyrosine kinase and failed axon connections (fax), a novel protein in axon bundles. Genetics. 1995 Oct;141(2):595–606. doi: 10.1093/genetics/141.2.595. [DOI] [PMC free article] [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. Jokerst R. S., Weeks J. R., Zehring W. A., Greenleaf A. L. Analysis of the gene encoding the largest subunit of RNA polymerase II in Drosophila. Mol Gen Genet. 1989 Jan;215(2):266–275. doi: 10.1007/BF00339727. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Patel N. H., Ball E. E., Goodman C. S. Changing role of even-skipped during the evolution of insect pattern formation. Nature. 1992 May 28;357(6376):339–342. doi: 10.1038/357339a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Sawamura K., Watanabe T. K., Yamamoto M. T. Hybrid lethal systems in the Drosophila melanogaster species complex. Genetica. 1993;88(2-3):175–185. doi: 10.1007/BF02424474. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. Wu C. I., Palopoli M. F. Genetics of postmating reproductive isolation in animals. Annu Rev Genet. 1994;28:283–308. doi: 10.1146/annurev.ge.28.120194.001435. [DOI] [PubMed] [Google Scholar]
  26. Zeng L. W., Singh R. S. The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. Genetics. 1993 May;134(1):251–260. doi: 10.1093/genetics/134.1.251. [DOI] [PMC free article] [PubMed] [Google Scholar]

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