Skip to main content
SpringerLink
Log in

Variation in Male Courtship Song Traits in Drosophila virilis: The Effects of Selection and Drift on Song Divergence at the Intraspecific Level

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

Abstract

Genetic and phenotypic divergence of Drosophila virilis laboratory strains originating from different parts of the species range were studied with the aid of microsatellite markers and by analysing male courtship songs. The strains from America, Europe, continental Asia and Japan showed moderate geographic clustering both at the genetic level and in several traits of the male song. The genetic distances and the song divergence of the strains did not show significant association, which suggests that the songs have not diverged solely as a side-effect of genetic divergence. Comparison of the songs of the laboratory strains to those of freshly collected strains showed that pulse characters of the song are quite sensitive to culture conditions. While laboratory rearing of the flies had no effect on the number of pulses in a pulse train or the pulse train length, the tendency of the sound pulses to become longer during laboratory maintenance could explain the lack of geographic variation in pulse length and inter pulse interval. Sensitivity of songs to culturing conditions should be taken in account in studies on song divergence.

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
Fig. 3

Similar content being viewed by others

References

  • Andolfatto P (2001) Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol 18:279–290

    PubMed  CAS  Google Scholar 

  • Aspi J (2000) Inbreeding and outbreeding depression in male courtship song characters in Drosophila montana. Heredity 84:273–282

    Article  PubMed  Google Scholar 

  • Aspi J, Hoikkala A (1995) Male mating success and survival in the field with respect to size and courtship song characters in Drosophila littoralis and D. montana (Diptera: Drosophilidae). J Insect Behav 8:67–87

    Article  Google Scholar 

  • Begun D, Aquadro CF (1993) African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365:548–550

    Article  PubMed  CAS  Google Scholar 

  • Bowcock AM, Ruiz-Lineares A, Tonfohrde J, Minch E, Kidd JR, Cavall-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  PubMed  CAS  Google Scholar 

  • Butlin RK, Tregenza T (1998) Levels of genetic polymorphism: marker loci versus quantitative traits. Phil Trans R Soc Lond B 353:187–198

    Article  CAS  Google Scholar 

  • Campesan S, Dubrova Y, Hall J, Kyriacou CP (2001) The nonA gene in Drosophila conveys species-specific behavioral characteristics. Genetics 158:1535–1543

    PubMed  CAS  Google Scholar 

  • Capy P, Pla E, David JR (1993) Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. I. Geographic variation. Genet Sel Evol 25:517–536

    Article  Google Scholar 

  • Capy P, Veuille M, Paillette M, Jallon J-M, Vouibidio J, David JR (2000) Sexual isolation of genetically differentiated sympatric populations of Drosophila melanogaster in Brazaville, Congo: the first step towards speciation? Heredity 84:468–475

    Article  PubMed  Google Scholar 

  • Colegrave N, Hollocher H, Hinton K, Ritchie MG (2000) The courtship song of African Drosophila melanogaster. J Evol Biol 13:143–150

    Article  Google Scholar 

  • Corander J, Marttinen, B (2005) BAPS: Bayesian Analysis of Population Structure. Manual v. 3.2. Department of Mathematics, University of Helsinki

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Corander J, Waldmann P, Marttinen P, Sillanpää MJ (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20:2363–2369

    Article  PubMed  CAS  Google Scholar 

  • Corander J, Marttinen P, Mäntyniemi S (2006) A Bayesian method for identification of stock mixtures from molecular marker data. Fish Bull 104:550–558

    Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Dobzhansky Th, Levene H (1948) Genetics of natural populations. Xvii. Proof of operation of natural selection in wild populations of Drosophila pseudoobscura. Genetics 33:537–547

    Google Scholar 

  • Etges WJ, Over KF, Cardoso de Oliveira C, Ritchie M (2006) Inheritance of courtship song variation among geographically isolated populations of Drosophila mojavensis. Anim Behav 71:1205–1214

    Article  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Applications to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP phylogeny inference package, version 3.5c. Technical report. University of Washington, Seattle

  • Ferveur JF, Cobb M, Boukella H, Jallon J-M (1996) World-wide variation in Drosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences. Genetica 97:73–80

    Article  PubMed  CAS  Google Scholar 

  • Hancock JM (1998) Microsatellites and other simple sequences: genomic context and mutational mechanisms. In: Goldstein DB, Schlötterer C (eds) Microsatellites evolution and applications. Oxford University Press, pp 1–9

  • Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101

    Article  PubMed  Google Scholar 

  • Hoikkala A (1985) Genetic variation in the male courtship sound of Drosophila littoralis. Behav Genet 15:135–142

    Article  PubMed  CAS  Google Scholar 

  • Hoikkala A (1988) The importance of different courtship stimuli in the mating behaviour of European species of the Drosophila virilis group. Ann Zool Fenn 25:257–263

    Google Scholar 

  • Hoikkala A (2005) Inheritance of male sound characteristics in Drosophila species. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. Taylor & Francis, pp 167–177

  • Hoikkala A, Lumme J (1987) The genetic basis of evolution of the male courtship sounds in the Drosophila virilis group. Evolution 41:827–845

    Article  Google Scholar 

  • Hollocher H, Ting C-I, Pollack F, Wu C-I (1997a) Incipient speciation by sexual isolation in Drosophila melanogaster: variation in mating preference and correlation between sexes. Evolution 51:1175–1181

    Article  Google Scholar 

  • Hollocher H, Ting C-I, Wu M-L, Wu C-I (1997b) Incipient speciation by sexual isolation in Drosophila melanogaster: extensive genetic divergence without reinforcement. Genetics 147:1191–1201

    PubMed  CAS  Google Scholar 

  • Huttunen S, Aspi J (2003) Complex inheritance of male courtship song characters in Drosophila virilise. Behav Genet 33:17–24

    Article  PubMed  Google Scholar 

  • Huttunen S, Schlötterer C (2002) Isolation and characterisation of microsatellites in Drosophila virilis and their cross species amplification in members of the D virilis group. Mol Ecol Notes 2:593–597

    Article  CAS  Google Scholar 

  • Huttunen S, Vieira J, Hoikkala A (2002) Nucleotide repeat variation at the nonA gene of the Drosophila virilis group species and its effects on male courtship song. Genetica 15:159–167

    Article  Google Scholar 

  • Huttunen S, Aspi J, Hoikkala A, Schlötterer C (2004) QTL analysis of variation in male courtship song characters in Drosophila virilis. Heredity 92:263–269

    Article  PubMed  CAS  Google Scholar 

  • Isoherranen E, Aspi J, Hoikkala A (1999) Variation and consistency of female preferences for simulated courtship songs in Drosophila virilis. Anim Behav 57:619–625

    Article  PubMed  Google Scholar 

  • Kauer M, Zangerl B, Dieringer D, Schlötterer C (2002) Chromosomal patterns of microsatellite variability contrast sharply in African and non-African population of Drosophila melanogaster. Genetics 160:247–256

    PubMed  CAS  Google Scholar 

  • Lakovaara S (1969) Malt as a culture medium for Drosophila species. Dros Inf Serv 44:128

    Google Scholar 

  • Lambert DM, Henderson NR (1986) The stability of the specific-mate recognition system of Drosophila melanogaster. Behav Genet 16:369–373

    Article  PubMed  CAS  Google Scholar 

  • Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:214–334

    Article  Google Scholar 

  • Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725

    Article  PubMed  CAS  Google Scholar 

  • Long AD, Singh RS (1995) Molecules versus morphology: the detection of selection acting on morphological characters along a cline in Drosophila melanogaster. Heredity 74:569–581

    PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Article  Google Scholar 

  • Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215

    Article  PubMed  CAS  Google Scholar 

  • Mirol PM, Schäfer MA, Orsini L, Routtu J, Schlötterer C, Hoikkala A, Butlin R (2007) Phylogeographic patterns in Drosophila montana. Mol Ecol 16:1085–1097

    Article  PubMed  CAS  Google Scholar 

  • Orsini L, Huttunen S, Schlötterer C (2004) A multilocus microsatellite phylogeny of the Drosophila virilis group. Heredity 93:161–165

    Article  PubMed  CAS  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Prout T, Baker JSF (1993) F statistics in Drosophila buzzattii: selection, population size and inbreeding. Genetics 134:369–375

    PubMed  CAS  Google Scholar 

  • Päällysaho S, Aspi J, Liimatainen JO, Hoikkala A (2003) The role of X chromosomal song genes in the evolution of species-specific courtship songs in Drosophila virilis group species. Behav Genet 33:25–32

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249 (http://www.wbiomed.curtin.edu.au/genepop)

  • Ritchie MG, Yate VH, Kyriacou CP (1994) Genetic variability of the interpulse interval of courtship song among some European populations of Drosophila melanogaster. Heredity 71:59–464

    Google Scholar 

  • Routtu J, Mazzi D, Van der Linde K, Mirol P, Butlin R, Hoikkala A (2007) The extent of variation in male song, wing and genital characters among allopatric Drosophila montana populations. J Evol Biol 20:1591–1601

    Article  PubMed  CAS  Google Scholar 

  • Saarikettu M., Liimatainen JO, Hoikkala A (2005) Intraspecific variation in mating behaviour does not cause sexual isolation between Drosophila virilis strains. Anim Behav 70:417–426

    Article  Google Scholar 

  • Schlötterer C (1998) Microsatellites. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. Oxford University Press, pp 237–261

  • Schlötterer C, Harr B (2000) Drosophila virilis has long and highly polymorphic microsatellites. Mol Biol Evol 17:1641–1645

    PubMed  Google Scholar 

  • Schlötterer C, Zangerl B (1999) The use of imperfect microsatellites for DNA fingerprinting and population genetics. In: Epplen JT, Lubjuhn T (eds) DNA profiling and DNA fingerprinting. Birkhäuser, Basel, pp 153–165

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory University of Geneva, Switzerland

    Google Scholar 

  • Spitze K (1993) Population structure in Daphnia obtusa – quantitative genetic and allozymic variation. Genetics 135:367–374

    PubMed  CAS  Google Scholar 

  • Throckmorton LH (1982) The virilis species group. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila, vol. 3b. Academic Press, London, pp 227–296

    Google Scholar 

  • Tregenza T, Pritchard VL, Butlin RK (2000) Patterns of trait divergence between populations of the meadow grasshopper Chorthippus parallelus. Evolution 54:574–585

    PubMed  CAS  Google Scholar 

  • Veuille M, Bènassi V, Aulard S, Depaulis F (1998) Allele-specific population structure of Drosophila melanogaster Alcohol dehydrogenase at the molecular level. Genetics 149:971–981

    PubMed  CAS  Google Scholar 

  • Vieira J, Charlesworth B (1999) X chromosome DNA variation in Drosophila virilis. Proc R Soc Lond B 266:1905–1912

    Article  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wu CI, Hollocher H, Begun DJ, Aquadro CF, Xu Y, Wu ML (1995) Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci USA 92:2519–2523

    Article  PubMed  CAS  Google Scholar 

  • Yamada H, Sakai T, Tomaru M, Doi M, Muneo M, Oguma Y (2002) Search for species-specific mating signal in courtship songs of sympatric sibling species Drosophila ananassae and D. pallidosa. Genes Genet Syst 77:97–106

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Many thanks to Zhang Wenxia, Hisaki Takamori, Michael Evgen’ev, Jorge Vieira and Bowling Green stock center for providing the D. virilis strains. Special thanks to Mari Saarikettu for help in rearing and sexing the flies for song recording and Max Kauer, Jaana Liimatainen, Emily Knott and Maaria Kankare for discussions and critiques. This work was supported by grants from the Finnish Cultural Foundation, Emil Aaltonen Foundation and University of Oulu to S. H. and from the Academy of Finland to A.H (project 44960 and the Centre of Excellence in Evolutionary Research). Co-operation between laboratories has been supported by the EU Research Training Network ‘Genetic analysis of complex co-evolved behavioural traits’ (HPRN-CT-2002-00266).

Author information

Authors and Affiliations

  1. Department of Biology, University of Oulu, Oulu, Finland

    Susanna Huttunen & Jouni Aspi

  2. Institut für Tierzucht und Genetik, Veterinärmedizinische Universität, Wien, Austria

    Christian Schlötterer

  3. Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, 40014, Jyvaskyla, Finland

    Jarkko Routtu & Anneli Hoikkala

Authors
  1. Susanna Huttunen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jouni Aspi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Schlötterer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jarkko Routtu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anneli Hoikkala
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anneli Hoikkala.

Additional information

Edited by Young-Kyu Kim.

Appendix 1

Appendix 1

Geographical origin and collection year (if known) of D. virilis strains and the means ± standard deviations of their song traits. Number of males analysed for each strain is five. Abbreviations: PN = number of pulses in a pulse train, PTL = length of a pulse train, PL = length of a pulse, IPI = length of an inter pulse interval, CN = number of cycles in a pulse and FRE = carrier frequency of the song.

Appendix 1  
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huttunen, S., Aspi, J., Schlötterer, C. et al. Variation in Male Courtship Song Traits in Drosophila virilis: The Effects of Selection and Drift on Song Divergence at the Intraspecific Level. Behav Genet 38, 82–92 (2008). https://doi.org/10.1007/s10519-007-9173-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10519-007-9173-0

Keywords

Search

Navigation