Skip to main content
SpringerLink
Log in

Natural Genetic Variation in Complex Mating Behaviors of Male Drosophila melanogaster

  • Original Research
  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

Mating behavior, including courtship and copulation, is a main component of male fitness, especially in species with no parental care. Variation in this behavior can thus be a target for mate choice and sexual selection, and can lead to evolution. The fruit fly, Drosophila melanogaster, has well-documented complex male courtship comprised of a sequence behaviors, and is an ideal model for behavior-genetic analysis. In order to evaluate genetic differences in the temporal pattern of mating behavior, we developed a high-throughput method that allows us to document the progression of male courtship and copulation using an ordinal scale (male mating progression scale, MMP). Using this method, we document natural genetic variation in the temporal pattern of behavior that was not detected using other metrics. This method was robust enough to detect genetic variation in this trait for males placed with both virgin and mated female targets.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Anholt RRH, Mackay TFC (2004) Quantitative genetic analyses of complex behaviours in Drosophila. Nat Rev Genet 5(11):838–849

    Article  PubMed  CAS  Google Scholar 

  • Aspi J, Hoikkala A (1993) Laboratory and natural heritabilities of male courtship song characters in Drosophila montana and D. littoralis. Heredity 70(4):400–406

    Article  PubMed  Google Scholar 

  • Balakireva M, Stocker RF, Gendre N, Ferveur JF (1998) Voila, a new Drosophila courtship variant that affects the nervous system: behavioral, neural, and genetic characterization. J Neurosci 18(11):4335–4343

    PubMed  CAS  Google Scholar 

  • Bastock M, Manning A (1955) The courtship of Drosophila melanogaster. Behaviour 8:7–110

    Article  Google Scholar 

  • Beaver LM, Giebultowicz JM (2004) Regulation of copulation duration by period and timeless in Drosophila melanogaster. Curr Biol 14(16):1492–1497

    Article  PubMed  CAS  Google Scholar 

  • Boake CRB, Konigsberg L (1998) Inheritance of male courtship behavior, aggressive success, and body size in Drosophila silvestris. Evolution 52(5):1487–1492

    Article  Google Scholar 

  • Bouletreau J (1978) Ovarian activity and reproductive potential in a natural population of Drosophila melanogaster. Oecologia (Berl) 35:319–342

    Article  Google Scholar 

  • Casares P, Carracedo MC, Miguel ES, Pineiro R, Garciaflorez L (1993) Male mating speed in Drosophila melanogaster – differences in genetic architecture and in relative performance according to female genotype. Behav Genet 23(4):349–358

    Article  PubMed  CAS  Google Scholar 

  • Connolly K, Cook R (1973) Rejection responses by female Drosophila melanogaster – their ontogeny, causality and effects upon behavior of courting male. Behaviour 44(1–2):142–166

    Article  Google Scholar 

  • Drapeau MD, Long AD (2000) The Copulatron, a multi-chamber apparatus for observing Drosophila courtship behaviors. Drosoph Inf Serv 83:194–196

    Google Scholar 

  • Etges WJ (2002) Divergence in mate choice systems: does evolution play by rules? Genetica 116(2–3):151–166

    Article  PubMed  CAS  Google Scholar 

  • Falconer D, Mackay T (1996) Introduction to quantitative genetics. Longman, Essex, England

    Google Scholar 

  • Ferveur JF, Jallon JM (1993) nerd, a locus on chromosome-III, affects male reproductive behavior in Drosophila melanogaster. Naturwissenschaften 80(10):474–475

    Article  PubMed  CAS  Google Scholar 

  • Fujii S, Krishnan P, Hardin P, Amrein H (2007) Nocturnal male sex drive in Drosophila. Curr Biol 17(3):244–251

    Article  PubMed  CAS  Google Scholar 

  • Gailey DA, Jackson FR, Siegel RW (1984) Conditioning mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics 106(4):613–623

    PubMed  Google Scholar 

  • Gefen E, Marlon AJ, Gibbs AG (2006) Selection for desiccation resistance in adult Drosophila melanogaster affects larval development and metabolite accumulation. J Exp Biol 209(Pt 17):3293–3300

    Article  PubMed  Google Scholar 

  • Gleason JM, Ritchie MG (2004) Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL? Genetics 166(3):1303–1311

    Article  PubMed  CAS  Google Scholar 

  • Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232

    Article  PubMed  CAS  Google Scholar 

  • Gromko MH (1987) Genetic constraint on the evolution of courtship behavior in Drosophila melanogaster. Heredity 58:435–441

    Article  Google Scholar 

  • Gromko MH, Markow TA (1993) Courtship and remating in field populations of Drosophila. Anim Behav 45(2):253–262

    Article  Google Scholar 

  • Gromko MH, Briot A, Jensen SC, Fukui HH (1991) Selection on copulation duration in Drosophila melanogaster – predictability of direct response versus unpredictability of correlated response. Evolution 45(1):69–81

    Article  Google Scholar 

  • Hall JC (1994) The mating of a fly. Science 264(5166):1702–1714

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann AA (1999) Is the heritability for courtship and mating speed in Drosophila (fruit fly) low? Heredity 82:151–157

    Article  Google Scholar 

  • Konopka RJ, Kyriacou CP, Hall JC (1996) Mosaic analysis in the Drosophila CNS of circadian and courtship-song rhythms affected by a period clock mutation. J Neurogenet 11(1–2):117–139

    Article  PubMed  CAS  Google Scholar 

  • Kulathinal RJ, Singh RS (2004) The nature of genetic variation in sex and reproduction-related genes among sibling species of the Drosophila melanogaster complex. Genetica 120(1–3):245–252

    Article  PubMed  CAS  Google Scholar 

  • Lasbleiz C, Ferveur JF, Everaerts C (2006) Courtship behaviour of Drosophila melanogaster revisited. Anim Behav 72:1001–1012

    Article  Google Scholar 

  • Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models, 4 edn. SAS Institute Inc, Cary, NC

    Google Scholar 

  • Mackay TFC, Heinsohn SL, Lyman RF, Moehring AJ, Morgan TJ et al (2005) Genetics and genomics of Drosophila mating behavior. Proc Natl Acad Sci USA 102:6622–6629

    Article  PubMed  CAS  Google Scholar 

  • Markow TA (2002) Perspective: female remating, operational sex ratio, and the arena of sexual selection in Drosophila species. Evolution 56(9):1725–1734

    PubMed  Google Scholar 

  • Markow TA, Hanson SJ (1981) Multivariate analysis of Drosophila courtship. Proc Natl Acad Sci USA 78(1):430–434

    Article  PubMed  Google Scholar 

  • Markow TA, Castrezana S, Pfeiler E (2002) Flies across the water: genetic differentiation and reproductive isolation in allopatric desert Drosophila. Evolution 56(3):546–552

    PubMed  Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Mcrobert SP, Tompkins L (1988) 2 consequences of homosexual courtship performed by Drosophila melanogaster and Drosophila affinis males. Evolution 42(5):1093–1097

    Article  Google Scholar 

  • Moehring A, Mackay T (2004) The quantitative genetic basis of male mating behavior in Drosophila melanogaster. Genetics 167(3):1249–1263

    Article  PubMed  CAS  Google Scholar 

  • Partridge L, Hoffmann A, Jones JS (1987) Male size and mating success in Drosophila melanogaster and Drosophila pseudoobscura under field conditions. Anim Behav 35:468–476

    Article  Google Scholar 

  • Pyle DW, Gromko MH (1981) Genetic basis for repeated mating in Drosophila melanogaster. Am Nat 117(2):133–146

    Article  Google Scholar 

  • Reif M, Linsenmair KE, Heisenberg M (2002) Evolutionary significance of courtship conditioning in Drosophila melanogaster. Anim Behav 63(Part 1):143–155

    Article  Google Scholar 

  • Ritchie MG, Gleason JM (1995) Rapid evolution of courtship song pattern in Drosophila willistoni sibling species. J Evol Biol 8(4):463–479

    Article  Google Scholar 

  • Ritchie MG, Kyriacou CP (1994) Genetic variability of courtship song in a population of Drosophila melanogaster. Anim Behav 48(2):425–434

    Article  Google Scholar 

  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A et al (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87(6):1079–1089

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2006) SAS Online Documentation v. 9.1. Available: http://support.sas.com/91doc/docMainpage.jsp. Accessed 2006

  • Sawamura K, Tomaru M (2002) Biology of reproductive isolation in Drosophila: toward a better understanding of speciation. Popul Ecol 44(3):209–219

    Article  Google Scholar 

  • Service P, Rose M (1985) Genetic covariation among life-history components – the effect of novel environments. Evolution 39(4):943–945

    Article  Google Scholar 

  • Siegel RW, Hall JC (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci USA 76(7):3430–3434

    Article  PubMed  Google Scholar 

  • Stamenkovicradak M, Partridge L, Andjelkovic M (1992) A genetic correlation between the sexes for mating speed in Drosophila melanogaster. Anim Behav 43(3):389–396

    Article  Google Scholar 

  • Stevens J (1992) Applied multivariate statistics for the social sciences. Lawrence Erlbaum Associates, Hillsdale, NJ

    Google Scholar 

  • Stirling DG, Reale D, Roff DA (2002) Selection, structure and the heritability of behaviour. J Evol Biol 15:277–289

    Article  Google Scholar 

  • Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP (2003) Temporal mating isolation driven a behavioral gene in Drosophila. Curr Biol 13(2):140–145

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto D, Nakano Y (1998) Genes for sexual behavior. Biochem Biophys Res Commun 246(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Acknowledgements

We would like to thank the National Science Foundation (NSF DEB 0296177), University of Illinois Program in Ecology, Evolution, and Conservation and the Francis M. and Harlie M. Clark research grant for financial support for this research. We would also like to thank M. M. Reedy and the members of the Hughes lab for help with the flies, and R. M. Reynolds, J. M. Drnevich, A. L. Toth, A. M. Bell, R. Fuller, H. M. Robertson, A. V. Suarez, G. E. Robinson, and three anonymous reviewers for their useful comments on this manuscript.

Author information

Authors and Affiliations

  1. Program in Ecology and Evolutionary Biology, University of Illinois at Urbana-Champaign, 286 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL, 61801, USA

    Elizabeth A. Ruedi

  2. Department of Genetics, North Carolina State University, Campus Box 7614, Raleigh, NC, 27695-7614, USA

    Elizabeth A. Ruedi

  3. Department of Animal Biology, University of Illinois at Urbana-Champaign, 515 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL, 61801, USA

    Kimberly A. Hughes

Authors
  1. Elizabeth A. Ruedi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kimberly A. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth A. Ruedi.

Additional information

Edited by Yong-Kyu Kim.

Appendices

Appendices

Appendix 1 Statistical tests for univariate models of single behaviors
Full size table
Appendix 2 Mean MMP scores averaged over first 15 min of trial, CI, copulation latency and duration for all VT families
Full size table
Appendix 3 Mean MMP scores averaged over first 15 min of trial and CI for all MT families
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruedi, E.A., Hughes, K.A. Natural Genetic Variation in Complex Mating Behaviors of Male Drosophila melanogaster . Behav Genet 38, 424–436 (2008). https://doi.org/10.1007/s10519-008-9204-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10519-008-9204-5

Keywords

Search

Navigation