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. 2004 Jul;167(3):1265–1274. doi: 10.1534/genetics.103.024364

Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana.

Amanda J Moehring 1, Jian Li 1, Malcolm D Schug 1, Shelly G Smith 1, Matthew deAngelis 1, Trudy F C Mackay 1, Jerry A Coyne 1
PMCID: PMC1470931  PMID: 15280240

Abstract

Sexual isolating mechanisms that act before fertilization are often considered the most important genetic barriers leading to speciation in animals. While recent progress has been made toward understanding the genetic basis of the postzygotic isolating mechanisms of hybrid sterility and inviability, little is known about the genetic basis of prezygotic sexual isolation. Here, we map quantitative trait loci (QTL) contributing to prezygotic reproductive isolation between the sibling species Drosophila simulans and D. mauritiana. We mapped at least seven QTL affecting discrimination of D. mauritiana females against D. simulans males, three QTL affecting D. simulans male traits against which D. mauritiana females discriminate, and six QTL affecting D. mauritiana male traits against which D. simulans females discriminate. QTL affecting sexual isolation act additively, are largely different in males and females, and are not disproportionately concentrated on the X chromosome: The QTL of greatest effect are located on chromosome 3. Unlike the genetic components of postzygotic isolation, the loci for prezygotic isolation do not interact epistatically. The observation of a few QTL with moderate to large effects will facilitate positional cloning of genes underlying sexual isolation.

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Selected References

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  1. Barbash Daniel A., Siino Dominic F., Tarone Aaron M., Roote John. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A. 2003 Apr 14;100(9):5302–5307. doi: 10.1073/pnas.0836927100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buchner E. Genes expressed in the adult brain of Drosophila and effects of their mutations on behavior: a survey of transmitter- and second messenger-related genes. J Neurogenet. 1991;7(4):153–192. doi: 10.3109/01677069109167432. [DOI] [PubMed] [Google Scholar]
  3. Churchill G. A., Doerge R. W. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. doi: 10.1093/genetics/138.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Civetta Alberto, Cantor Elliott J. F. The genetics of mating recognition between Drosophila simulans and D. sechellia. Genet Res. 2003 Oct;82(2):117–126. doi: 10.1017/s0016672303006360. [DOI] [PubMed] [Google Scholar]
  5. Coyne J. A. Genetics of a difference in male cuticular hydrocarbons between two sibling species, Drosophila simulans and D. sechellia. Genetics. 1996 Aug;143(4):1689–1698. doi: 10.1093/genetics/143.4.1689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coyne J. A. Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5464–5468. doi: 10.1073/pnas.86.14.5464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coyne J. A. Genetics of sexual isolation in females of the Drosophila simulans species complex. Genet Res. 1992 Aug;60(1):25–31. doi: 10.1017/s0016672300030639. [DOI] [PubMed] [Google Scholar]
  8. Coyne J. A. Genetics of sexual isolation in male hybrids of Drosophila simulans and D. mauritiana. Genet Res. 1996 Dec;68(3):211–220. doi: 10.1017/s0016672300034182. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Dittrich R., Bossing T., Gould A. P., Technau G. M., Urban J. The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development. 1997 Jul;124(13):2515–2525. doi: 10.1242/dev.124.13.2515. [DOI] [PubMed] [Google Scholar]
  12. Doerge R. W., Churchill G. A. Permutation tests for multiple loci affecting a quantitative character. Genetics. 1996 Jan;142(1):285–294. doi: 10.1093/genetics/142.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FlyBase Consortium The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 2003 Jan 1;31(1):172–175. doi: 10.1093/nar/gkg094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gockel J., Kennington W. J., Hoffmann A., Goldstein D. B., Partridge L. Nonclinality of molecular variation implicates selection in maintaining a morphological cline of Drosophila melanogaster. Genetics. 2001 May;158(1):319–323. doi: 10.1093/genetics/158.1.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hollocher H., Ting C. T., Wu M. L., Wu C. I. Incipient speciation by sexual isolation in Drosophila melanogaster: extensive genetic divergence without reinforcement. Genetics. 1997 Nov;147(3):1191–1201. doi: 10.1093/genetics/147.3.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hoy R. R., Hahn J., Paul R. C. Hybrid cricket auditory behavior: evidence for genetic coupling in animal communication. Science. 1977 Jan 7;195(4273):82–84. doi: 10.1126/science.831260. [DOI] [PubMed] [Google Scholar]
  17. Inoue H., Yoshioka T., Hotta Y. A genetic study of inositol trisphosphate involvement in phototransduction using Drosophila mutants. Biochem Biophys Res Commun. 1985 Oct 30;132(2):513–519. doi: 10.1016/0006-291x(85)91163-5. [DOI] [PubMed] [Google Scholar]
  18. Kaneko M., Hamblen M. J., Hall J. C. Involvement of the period gene in developmental time-memory: effect of the perShort mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J Biol Rhythms. 2000 Feb;15(1):13–30. doi: 10.1177/074873040001500103. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Lundell M. J., Hirsh J. eagle is required for the specification of serotonin neurons and other neuroblast 7-3 progeny in the Drosophila CNS. Development. 1998 Feb;125(3):463–472. doi: 10.1242/dev.125.3.463. [DOI] [PubMed] [Google Scholar]
  22. Orr H. A. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics. 1998 Aug;149(4):2099–2104. doi: 10.1093/genetics/149.4.2099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Presgraves Daven C. A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics. 2003 Mar;163(3):955–972. doi: 10.1093/genetics/163.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Presgraves Daven C., Balagopalan Lakshmi, Abmayr Susan M., Orr H. Allen. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature. 2003 Jun 12;423(6941):715–719. doi: 10.1038/nature01679. [DOI] [PubMed] [Google Scholar]
  25. Price C. S. Conspecific sperm precedence in Drosophila. Nature. 1997 Aug 14;388(6643):663–666. doi: 10.1038/41753. [DOI] [PubMed] [Google Scholar]
  26. Price C. S., Kim C. H., Posluszny J., Coyne J. A. Mechanisms of conspecific sperm precedence in Drosophila. Evolution. 2000 Dec;54(6):2028–2037. doi: 10.1111/j.0014-3820.2000.tb01246.x. [DOI] [PubMed] [Google Scholar]
  27. Ritchie M. G. Behavioral coupling in tettigoniid hybrids (Orthoptera). Behav Genet. 1992 May;22(3):369–379. doi: 10.1007/BF01066668. [DOI] [PubMed] [Google Scholar]
  28. Saudou F., Hen R. 5-Hydroxytryptamine receptor subtypes in vertebrates and invertebrates. Neurochem Int. 1994 Dec;25(6):503–532. doi: 10.1016/0197-0186(94)90150-3. [DOI] [PubMed] [Google Scholar]
  29. Tao Yun, Zeng Zhao-Bang, Li Jian, Hartl Daniel L., Laurie Cathy C. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome. Genetics. 2003 Aug;164(4):1399–1418. doi: 10.1093/genetics/164.4.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tempel B. L., Livingstone M. S., Quinn W. G. Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3577–3581. doi: 10.1073/pnas.81.11.3577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ting C. T., Takahashi A., Wu C. I. Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6709–6713. doi: 10.1073/pnas.121418898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Wu C. I., Hollocher H., Begun D. J., Aquadro C. F., Xu Y., Wu M. L. Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2519–2523. doi: 10.1073/pnas.92.7.2519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Zeng Z. B., Liu J., Stam L. F., Kao C. H., Mercer J. M., Laurie C. C. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics. 2000 Jan;154(1):299–310. doi: 10.1093/genetics/154.1.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]

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