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. 2003 Aug;164(4):1399–1418. doi: 10.1093/genetics/164.4.1399

Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome.

Yun Tao 1, Zhao-Bang Zeng 1, Jian Li 1, Daniel L Hartl 1, Cathy C Laurie 1
PMCID: PMC1462659  PMID: 12930748

Abstract

Hybrid male sterility (HMS) is a rapidly evolving mechanism of reproductive isolation in Drosophila. Here we report a genetic analysis of HMS in third-chromosome segments of Drosophila mauritiana that were introgressed into a D. simulans background. Qualitative genetic mapping was used to localize 10 loci on 3R and a quantitative trait locus (QTL) procedure (multiple-interval mapping) was used to identify 19 loci on the entire chromosome. These genetic incompatibilities often show dominance and complex patterns of epistasis. Most of the HMS loci have relatively small effects and generally at least two or three of them are required to produce complete sterility. Only one small region of the third chromosome of D. mauritiana by itself causes a high level of infertility when introgressed into D. simulans. By comparison with previous studies of the X chromosome, we infer that HMS loci are only approximately 40% as dense on this autosome as they are on the X chromosome. These results are consistent with the gradual evolution of hybrid incompatibilities as a by-product of genetic divergence in allopatric populations.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  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., 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]
  6. 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]
  7. Dobzhansky T. Analysis of incipient reproductive isolation within a species of Drosophila. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3638–3641. doi: 10.1073/pnas.72.9.3638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eshed Y., Zamir D. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics. 1995 Nov;141(3):1147–1162. doi: 10.1093/genetics/141.3.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Frary A., Nesbitt T. C., Grandillo S., Knaap E., Cong B., Liu J., Meller J., Elber R., Alpert K. B., Tanksley S. D. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science. 2000 Jul 7;289(5476):85–88. doi: 10.1126/science.289.5476.85. [DOI] [PubMed] [Google Scholar]
  11. Fridman E., Pleban T., Zamir D. A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4718–4723. doi: 10.1073/pnas.97.9.4718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Jiang C., Zeng Z. B. Mapping quantitative trait loci with dominant and missing markers in various crosses from two inbred lines. Genetica. 1997;101(1):47–58. doi: 10.1023/a:1018394410659. [DOI] [PubMed] [Google Scholar]
  14. Kao C. H., Zeng Z. B. General formulas for obtaining the MLEs and the asymptotic variance-covariance matrix in mapping quantitative trait loci when using the EM algorithm. Biometrics. 1997 Jun;53(2):653–665. [PubMed] [Google Scholar]
  15. Kao C. H., Zeng Z. B., Teasdale R. D. Multiple interval mapping for quantitative trait loci. Genetics. 1999 Jul;152(3):1203–1216. doi: 10.1093/genetics/152.3.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kao Chen-Hung, Zeng Zhao-Bang. Modeling epistasis of quantitative trait loci using Cockerham's model. Genetics. 2002 Mar;160(3):1243–1261. doi: 10.1093/genetics/160.3.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kliman R. M., Andolfatto P., Coyne J. A., Depaulis F., Kreitman M., Berry A. J., McCarter J., Wakeley J., Hey J. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics. 2000 Dec;156(4):1913–1931. doi: 10.1093/genetics/156.4.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liu J., Mercer J. M., Stam L. F., Gibson G. C., Zeng Z. B., Laurie C. C. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics. 1996 Apr;142(4):1129–1145. doi: 10.1093/genetics/142.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orr H. A., Betancourt A. J. Haldane's sieve and adaptation from the standing genetic variation. Genetics. 2001 Feb;157(2):875–884. doi: 10.1093/genetics/157.2.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Orr H. A., Irving S. Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics. 2001 Jul;158(3):1089–1100. doi: 10.1093/genetics/158.3.1089. [DOI] [PMC free article] [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. 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]
  23. 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]
  24. Tao Y., Hartl D. L., Laurie C. C. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Natl Acad Sci U S A. 2001 Oct 30;98(23):13183–13188. doi: 10.1073/pnas.231478798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tao Yun, Chen Sining, Hartl Daniel L., Laurie Cathy C. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics. 2003 Aug;164(4):1383–1397. doi: 10.1093/genetics/164.4.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ting C. T., Tsaur S. C., Wu C. I. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5313–5316. doi: 10.1073/pnas.090541597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ting C. T., Tsaur S. C., Wu M. L., Wu C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998 Nov 20;282(5393):1501–1504. doi: 10.1126/science.282.5393.1501. [DOI] [PubMed] [Google Scholar]
  28. True J. R., Mercer J. M., Laurie C. C. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. doi: 10.1093/genetics/142.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Xu S., Atchley W. R. Mapping quantitative trait loci for complex binary diseases using line crosses. Genetics. 1996 Jul;143(3):1417–1424. doi: 10.1093/genetics/143.3.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zeng Z. B., Kao C. H., Basten C. J. Estimating the genetic architecture of quantitative traits. Genet Res. 1999 Dec;74(3):279–289. doi: 10.1017/s0016672399004255. [DOI] [PubMed] [Google Scholar]

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