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Genetics. Mar 2004; 166(3): 1303–1311.
PMCID: PMC1470780

Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL?

Abstract

The genetic architecture of traits influencing sexual isolation can give insight into the evolution of reproductive isolation and hence speciation. Here we report a quantitative trait loci (QTL) analysis of the difference in mean interpulse interval (IPI), an important component of the male courtship song, between Drosophila simulans and D. sechellia. Using a backcross analysis, we find six QTL that explain a total of 40.7% of the phenotypic variance. Three candidate genes are located in the intervals bounded by two of the QTL and there are no significant QTL on the X chromosome. The values of mean IPI for hybrid individuals imply the presence of dominant alleles or epistasis. Because unisexual hybrid sterility prevents an F(2) analysis, we cannot distinguish dominant from additive genetic effects at the scale of QTL. A comparison with a study of QTL for intraspecific variation in D. melanogaster shows that, for these strains, the QTL we have identified for interspecific variation cannot be those that contribute to intraspecific variation. We find that the QTL have bidirectional effects, which indicates that the genetic architecture is compatible with divergence due to genetic drift, although other possibilities are discussed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Haag ES, True JR. Perspective: From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology. Evolution. 2001 Jun;55(6):1077–1084. [PubMed]
  • Henry Charles S, Martínez Wells Marta Lucía, Holsinger Kent E. The inheritance of mating songs in two cryptic, sibling lacewing species (Neuroptera: Chrysopidae: Chrysoperla). Genetica. 2002 Nov;116(2-3):269–289. [PubMed]
  • Huttunen Susanna, Vieira Jorge, Hoikkala Anneli. Nucleotide and repeat length variation at the nonA gene of the Drosophila virilis group species and its effects on male courtship song. Genetica. 2002 Jun;115(2):159–167. [PubMed]
  • Jansen RC, Stam P. High resolution of quantitative traits into multiple loci via interval mapping. Genetics. 1994 Apr;136(4):1447–1455. [PMC free article] [PubMed]
  • Joly D, Bazin C, Zeng LW, Singh RS. Genetic basis of sperm and testis length differences and epistatic effect on hybrid inviability and sperm motility between Drosophila simulans and D. sechellia. Heredity (Edinb) 1997 Apr;78(Pt 4):354–362. [PubMed]
  • Kim SC, Rieseberg LH. Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics. 1999 Oct;153(2):965–977. [PMC free article] [PubMed]
  • Kopp Artyom, Graze Rita M, Xu Shizhong, Carroll Sean B, Nuzhdin Sergey V. Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics. 2003 Feb;163(2):771–787. [PMC free article] [PubMed]
  • Kulkarni SJ, Steinlauf AF, Hall JC. The dissonance mutant of courtship song in Drosophila melanogaster: isolation, behavior and cytogenetics. Genetics. 1988 Feb;118(2):267–285. [PMC free article] [PubMed]
  • Kyriacou Charalambos P. Single gene mutations in Drosophila: what can they tell us about the evolution of sexual behaviour? Genetica. 2002 Nov;116(2-3):197–203. [PubMed]
  • Kyriacou CP, Hall JC. Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6729–6733. [PMC free article] [PubMed]
  • Bradshaw HD, Jr, Otto KG, Frewen BE, McKay JK, Schemske DW. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics. 1998 May;149(1):367–382. [PMC free article] [PubMed]
  • Lai C, Lyman RF, Long AD, Langley CH, Mackay TF. Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science. 1994 Dec 9;266(5191):1697–1702. [PubMed]
  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA, Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. [PubMed]
  • Campesan S, Dubrova Y, Hall JC, Kyriacou CP. The nonA gene in Drosophila conveys species-specific behavioral characteristics. Genetics. 2001 Aug;158(4):1535–1543. [PMC free article] [PubMed]
  • Laurie CC, True JR, Liu J, Mercer JM. An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. Genetics. 1997 Feb;145(2):339–348. [PMC free article] [PubMed]
  • Churchill GA, Doerge RW. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. [PMC free article] [PubMed]
  • Colson I, Goldstein DB. Evidence for complex mutations at microsatellite loci in Drosophila. Genetics. 1999 Jun;152(2):617–627. [PMC free article] [PubMed]
  • Macdonald SJ, Goldstein DB. A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics. 1999 Dec;153(4):1683–1699. [PMC free article] [PubMed]
  • Coyne JA, Crittenden AP, Mah K. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science. 1994 Sep 2;265(5177):1461–1464. [PubMed]
  • Doi M, Matsuda M, Tomaru M, Matsubayashi H, Oguma Y. A locus for female discrimination behavior causing sexual isolation in Drosophila. Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6714–6719. [PMC free article] [PubMed]
  • Michalakis Y, Veuille M. Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics. 1996 Aug;143(4):1713–1725. [PMC free article] [PubMed]
  • Fishman Lila, Kelly Alan J, Willis John H. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution. 2002 Nov;56(11):2138–2155. [PubMed]
  • Nuzhdin SV, Reiwitch SG. Are the same genes responsible for intra- and interspecific variability for sex comb tooth number in Drosophila? Heredity (Edinb) 2000 Jan;84(Pt 1):97–102. [PubMed]
  • Orr HA. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics. 1998 Aug;149(4):2099–2104. [PMC free article] [PubMed]
  • Goldstein DB, Clark AG. Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acids Res. 1995 Oct 11;23(19):3882–3886. [PMC free article] [PubMed]
  • Panhuis TM, Butlin R, Zuk M, Tregenza T. Sexual selection and speciation. Trends Ecol Evol. 2001 Jul 1;16(7):364–371. [PubMed]
  • Takahashi A, Tsaur SC, Coyne JA, Wu CI. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3920–3925. [PMC free article] [PubMed]
  • Pugh AR, Ritchie MG. Polygenic control of a mating signal in Drosophila. Heredity (Edinb) 1996 Oct;77(Pt 4):378–382. [PubMed]
  • Ritchie MG, Kyriacou CP. Reproductive isolation and the period gene of Drosophila. Mol Ecol. 1994 Dec;3(6):595–599. [PubMed]
  • Villella A, Hall JC. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics. 1996 May;143(1):331–344. [PMC free article] [PubMed]
  • Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics. 1997 Nov;147(3):1107–1130. [PMC free article] [PubMed]
  • Ritchie MG, Yate VH, Kyriacou CP. Genetic variability of the interpulse interval of courtship song among some European populations of Drosophila melanogaster. Heredity (Edinb) 1994 May;72(Pt 5):459–464. [PubMed]
  • Von Schilcher F. The behavior of cacophony, a courtship song mutant in Drosophila melanogaster. Behav Biol. 1976 Jun;17(2):187–196. [PubMed]
  • Ritchie MG, Townhill RM, Hoikkala A. Female preference for fly song: playback experiments confirm the targets of sexual selection. Anim Behav. 1998 Sep;56(3):713–717. [PubMed]
  • Ritchie MG, Halsey EJ, Gleason JM. Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim Behav. 1999 Sep;58(3):649–657. [PubMed]
  • von Schilcher F. A mutation which changes courtship song in Drosophila melanogaster. Behav Genet. 1977 May;7(3):251–259. [PubMed]
  • Wheeler DA, Fields WL, Hall JC. Spectral analysis of Drosophila courtship songs: D. melanogaster, D. simulans, and their interspecific hybrid. Behav Genet. 1988 Nov;18(6):675–703. [PubMed]
  • Schug MD, Mackay TF, Aquadro CF. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat Genet. 1997 Jan;15(1):99–102. [PubMed]
  • Williams MA, Blouin AG, Noor MA. Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences. Heredity (Edinb) 2001 Jan;86(Pt 1):68–77. [PubMed]
  • Schug MD, Wetterstrand KA, Gaudette MS, Lim RH, Hutter CM, Aquadro CF. The distribution and frequency of microsatellite loci in Drosophila melanogaster. Mol Ecol. 1998 Jan;7(1):57–70. [PubMed]
  • Shaw Kerry L, Parsons Yvonne M. Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am Nat. 2002 Mar;159 (Suppl 3):S61–S75. [PubMed]
  • Yamada Hirokazu, Matsuda Muneo, Oguma Yuzuru. Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa. Genetica. 2002 Nov;116(2-3):225–237. [PubMed]
  • Shorey HH. Nature of the Sound Produced by Drosophila melanogaster during Courtship. Science. 1962 Aug 31;137(3531):677–678. [PubMed]
  • Yokokura T, Ueda R, Yamamoto D. Phenotypic and molecular characterization of croaker, a new mating behavior mutant of Drosophila melanogaster. Jpn J Genet. 1995 Feb;70(1):103–117. [PubMed]
  • Stanewsky R, Fry TA, Reim I, Saumweber H, Hall JC. Bioassaying putative RNA-binding motifs in a protein encoded by a gene that influences courtship and visually mediated behavior in Drosophila: in vitro mutagenesis of nonA. Genetics. 1996 May;143(1):259–275. [PMC free article] [PubMed]
  • Zeng ZB. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. [PMC free article] [PubMed]
  • Zeng ZB, Liu J, Stam LF, Kao CH, Mercer JM, Laurie CC. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics. 2000 Jan;154(1):299–310. [PMC free article] [PubMed]
  • Sucena E, Stern DL. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4530–4534. [PMC free article] [PubMed]

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