Behavior Genetics

, 38:195 | Cite as

Sex Combs are Important for Male Mating Success in Drosophila melanogaster

Original Research


The sex comb is one of the most rapidly evolving male-specific traits in Drosophila, making it an attractive model to study sexual selection and developmental evolution. Drosophila males use their sex combs to grasp the females’ abdomen and genitalia and to spread their wings prior to copulation. To test the role of this structure in male mating success in Drosophila melanogaster, we genetically ablated the sex comb by expressing the female-specific isoform of the sex determination gene transformer in the tarsal segments of male legs. This technique does not remove the sex comb entirely, but simply restores the morphology of its constituent bristles to the ancestral condition found in Drosophila species that lack sex combs. Direct observations and differences in long-term insemination rates show that the loss of the sex comb strongly reduces the ability of males to copulate with females. Detailed analysis of video recordings indicates that this effect is not due to changes in the males’ courtship behavior. Rapid evolution of sex comb morphology may be driven either by changes in female preferences, or by co-evolution between sex combs and female external genitalia.


Drosophila Sex comb Sexual dimorphism Sexual selection Courtship Female choice 


  1. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  2. Baker BS, Ridge KA (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94(2):383–423PubMedGoogle Scholar
  3. Barmina O, Gonzalo M, McIntyre L, Kopp A (2005) Sex- and segment-specific modulation of gene expression profiles in Drosophila. Dev Biol 288:528–544PubMedCrossRefGoogle Scholar
  4. Barmina O, Kopp A (2007) Sex-specific expression of a HOX gene associated with rapid morphological evolution. Dev Biol 311:277–286PubMedCrossRefGoogle Scholar
  5. Bastock M, Manning A (1955) The courtship of Drosophila melanogaster. Behaviour 8:85–111Google Scholar
  6. Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39(6):1019–1029PubMedCrossRefGoogle Scholar
  7. Cook RM (1977) Behavioral role of the sexcombs in Drosophila melanogaster and Drosophila simulans. Behav Genet 7(5):349–357PubMedCrossRefGoogle Scholar
  8. Coyne JA (1985) Genetic studies of three sibling species of Drosophila with relationship to theories of speciation. Genet Res 46(2):169–192PubMedCrossRefGoogle Scholar
  9. Coyne JA, Elwyn S, Kim SY, Llopart A (2004) Genetic studies of two sister species in the Drosophila melanogaster subgroup, D. yakuba and D. santomea. Genet Res 84(1):11–26PubMedCrossRefGoogle Scholar
  10. Ferveur JF, Stortkuhl KF, Stocker RF, Greenspan RJ (1995) Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267(5199):902–905PubMedCrossRefGoogle Scholar
  11. Graze RM, Barmina O, Tufts D, Naderi E, Harmon KL, Persianinova M, Nuzhdin SV (2007) New candidate genes for sex comb divergence between Drosophila mauritiana and Drosophila simulans. Genetics 176:2561–2576PubMedCrossRefGoogle Scholar
  12. Hannah-Alavah A (1958) Morphology and chaetotaxy of the legs of Drosophila melanogaster. J Morph 103:281–310CrossRefGoogle Scholar
  13. Hu Y-G, Toda MJ (2001) Polyphyly of Lordiphosa and its relationships in Drosophilinae (Diptera: Drosophilidae). System Entomol 25:1–17Google Scholar
  14. Kopp A, True JR (2002) Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evol Dev 4(4):278–291PubMedCrossRefGoogle Scholar
  15. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446(7135):542–546PubMedCrossRefGoogle Scholar
  16. Lakovaara S, Saura A (1982) Evolution and speciation in the Drosophila obscura group. In: Ashburner, Carson, Thompson (eds) The genetics and biology of Drosophila, vol 3b, pp 1–59Google Scholar
  17. Lemeunier F, David J, Tsacas L, Ashburner M. (1986) The melanogaster species group. In: Ashburner, Carson, Thompson (eds) The genetics and biology of Drosophila, vol 3e, pp 147–256Google Scholar
  18. Macdonald SJ, Goldstein DB (1999) A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153(4):1683–1699PubMedGoogle Scholar
  19. Markow TA, Bustoz D, Pitnick S (1996) Sexual selection and a secondary sexual character in two Drosophila species. Anim Behav 52(4):759–766CrossRefGoogle Scholar
  20. McKeown M (1992) Sex differentiation: the role of alternative splicing. Curr Opin Genet Dev 2(2):299–303PubMedCrossRefGoogle Scholar
  21. Nuzhdin SV, Reiwitch SG (2000) Are the same genes responsible for intra- and interspecific variability for sex comb tooth number in Drosophila? Heredity 84:97–102PubMedCrossRefGoogle Scholar
  22. Polak M, Starmer WT, Wolf LL (2004) Sexual selection for size and symmetry in a diversifying secondary sexual character in Drosophila bipectinata Duda (Diptera: Drosophilidae). Evolution 58(3):597–607PubMedGoogle Scholar
  23. Ritchie MG, Halsey EJ, Gleason JM (1999) Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim Behav 58(3):649–657PubMedCrossRefGoogle Scholar
  24. Simmonds AJ, Brook WJ, Cohen SM, Bell JB (1995) Distinguishable functions for engrailed and invected in anterior–posterior patterning in the Drosophila wing. Nature 376(6539):424–427PubMedCrossRefGoogle Scholar
  25. Spieth HT (1952) Mating behavior within the genus Drosophila (Diptera). Bull Am Museum Nat Hist 99(7):395–474Google Scholar
  26. St Pierre SE, Galindo MI, Couso JP, Thor S (2002) Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same gene encoding functionally distinct zinc finger proteins. Development 129(5):1273–1281PubMedGoogle Scholar
  27. Sturtevant AH (1942) The classification of the genus Drosophila, with descriptions of nine new species. Univ Texas Publ 4231:6–51Google Scholar
  28. Tatsuta H, Takano-Shimizu T (2006) Genetic architecture of variation in sex-comb tooth number in Drosophila simulans. Genet Res 87(2):93–107PubMedCrossRefGoogle Scholar
  29. True JR, Liu J, Stam LF, Zeng ZB, Laurie CC (1997) Quantitative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana. Evolution 51:816–832CrossRefGoogle Scholar
  30. van der Goes van Naters W, Carlson JR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17(7):606–612CrossRefGoogle Scholar
  31. Wiens JJ (2001) Widespread loss of sexually selected traits: how the peacock lost its spots. Trends Ecol Evol 16(9):517–523CrossRefGoogle Scholar
  32. Wong BB, Rosenthal GG (2006) Female disdain for swords in a swordtail fish. Am Nat 167(1):136–140PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Section of Evolution and Ecology and Center for Population BiologyUniversity of California—DavisDavisUSA

Personalised recommendations