Skip to main content
Log in

Sexual isolation between Drosophila simulans and D. mauritiana: D. simulans females do not discriminate against intact-wing D. mauritiana males

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript
  • 1 Altmetric

Abstract

Female mate choice plays an important role in sexual isolation. The present study examined sexual isolation using D. simulans and D. mauritiana in conditions where females had no opportunity to compare males versus where females were able to choose males. The sound produced by wing vibration in males (courtship song) affects female receptivity in Drosophila. Females of both species copulated with intact conspecific males more than intact heterospecific males and wingless conspecific and heterospecific males. Drosophila mauritiana females copulated only with intact conspecific males within 30-min observations period without comparing other males, suggesting that absolute criteria are used for decision-making to accept courting males. Females of D. simulans copulated with intact D. mauritiana males as well as wingless D. simulans or D. mauritiana males in no-choice conditions. In a choice situation, D. simulans females copulated with intact D. mauritiana males as well as wingless D. mauritiana males when the females were courted by both types of males, suggesting that D. simulans females accept intact D. mauritiana males as if they are mute. Females of D. simulans copulated with intact D. simulans males as well as intact D. mauritiana males when they were courted by males of either type, whereas they copulated with intact D. simulans males more than intact D. mauritiana males in true choice situations. These results suggest that females make a comparative review of courting males before accepting a male and that conspecific song is a factor in criteria affecting female selectivity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnold SJ, Verrell PA, Tilley SG (1996) The evolution of asymmetry in sexual isolation: a model and a test case. Evolution 50:1024–1033

    PubMed  Google Scholar 

  • Ashburner M, Golic KG, Hawley RS (2005) The melanogaster species subgroup. Drosophila: a laboratory handbook, 2nd edn, chap 33. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 1255–1283

    Google Scholar 

  • Barnard GA (1947) Significance tests for 2 X 2 tables. Biometrika 34:123–138

    CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bennet-Clark HC, Ewing AW (1969) Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster. Anim Behav 17:755–759

    Google Scholar 

  • Cobb M, Jallon JM (1990) Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster species sub-group. Anim Behav 39:1058–1067

    Google Scholar 

  • Cobb M, Burnet B, Connolly K (1988) Sexual isolation and courtship behavior in Drosophila simulans, D. mauritiana, and their interspecific hybrids. Behav Genet 18:211–225

    CAS  PubMed  Google Scholar 

  • Cobb M, Burnet B, Blizard R, Jallon JM (1989) Courtship in Drosophila sechellia its structure, functional aspects, and relationship to those of other members of the Drosophila melanogaster species subgroup. J Insect Behav 2:63–89

    Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Elrbaum Associates, Hillsdale

    Google Scholar 

  • Collins SA, Luddem ST (2002) Degree of male ornamentation affects female preference for conspecific versus heterospecific males. Proc R Soc B 269:111–117

    PubMed  Google Scholar 

  • Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765

    CAS  PubMed  Google Scholar 

  • Cowling DE, Burnet B (1981) Courtship songs and genetic control of their acoustic characteristics in sibling species of the Drosophila melanogaster subgroup. Anim Behav 29:924–935

    Google Scholar 

  • Coyne JA (1989) Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci USA 86:5464–5468

    CAS  PubMed  Google Scholar 

  • Coyne JA (1992) Genetics of sexual isolation in females of the Drosophila simulans species complex. Genet Res 60:25–31

    CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Coyne JA, Elwyn S, Rolán-Alvarez E (2005) Impact of experimental design on Drosophila sexual isolation studies: direct effects and comparison to field hybridization data. Evolution 59:2588–2601

    PubMed  Google Scholar 

  • Deering MD, Scriber JM (2002) Field bioassays show heterospecific mating preference asymmetry between hybridizing north American Papilio butterfly species (Lepidoptera: Papilionidae). J Ethol 20:25–33

    Google Scholar 

  • Doi M, Matsuda M, Tomaru M, Matsubayashi H, Oguma Y (2001) A locus for female discrimination behavior causing sexual isolation in Drosophila. Proc Natl Acad Sci USA 98:6714–6719

    CAS  PubMed  Google Scholar 

  • Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654

    PubMed  Google Scholar 

  • Fabre CCG, Hedwig B, Conduit G, Lawrence PA, Goodwin SF, Casal J (2012) Substrate-borne vibratory communication during courtship in Drosophila melanogaster. Curr Biol 22:2180–2185

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goetze E, Kiørboe T (2008) Heterospecific mating and species recognition in the planktonic marine copepods Temora stylifera and T. longicornis. Mar Ecol Prog Ser 375:185–198

    Google Scholar 

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

    Google Scholar 

  • Hoikkala A, Aspi J (1993) Criteria of female mate choice in Drosophila littoralis, D. montana, and D. ezoana. Evolution 47:768–777

    PubMed  Google Scholar 

  • Hoikkala A, Kaneshiro K (1993) Change in the signal-response sequence responsible for asymmetric isolation between Drosophila planitibia and Drosophila silvestris. Proc Natl Acad Sci USA 90:5813–5817

    CAS  PubMed  Google Scholar 

  • Holm S (1979) A simple squentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 14:441–478

    CAS  PubMed  Google Scholar 

  • Jones IL, Hunter FM (1998) Heterospecific mating preferences for a feather ornament in least auklets. Behav Ecol 9:187–192

    Google Scholar 

  • Kaneshiro KY (1976) Ethological isolation and phylogeny in the planitibia subgroup of Hawaiian Drosophila. Evolution 30:740–745

    PubMed  Google Scholar 

  • Kaneshiro KY (1980) Sexual isolation, speciation and the direction of evolution. Evolution 34:437–444

    PubMed  Google Scholar 

  • Kyriacou CP, Hall JC (1982) The function of courtship song rhythms in Drosophila. Anim Behav 30:794–801

    Google Scholar 

  • Lachaise D, David JR, Lemeunier F, Tsacas L, Ashburner M (1986) The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 40:262–271

    PubMed  Google Scholar 

  • Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, Ashburner M (1988) Historical biogeography of the Drosophila melanogaster species subgroup. In: Hecht MK, Wallace B, Prance GT (eds) Evolutionary biology, vol 22. Springer, Boston, pp 159–225

    Google Scholar 

  • Lachaise D, Harry M, Solignac M, Lemeunier F, Benassi V, Cariou ML (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé. Proc R Soc B 267:1487–1495

    CAS  PubMed  Google Scholar 

  • Mazzoni V, Anfora G, Virant-Doberlet M (2013) Substrate vibrations during courtship in three Drosophila species. PloS One 8:e80708

    PubMed  PubMed Central  Google Scholar 

  • Moehring AJ, Boughman JW (2019) Veiled preferences and cryptic female choice could underlie the origin of novel sexual traits. Biol Lett 15:20180878. https://doi.org/10.1098/rsbl.2018.0878

    Article  PubMed  PubMed Central  Google Scholar 

  • Moehring AJ, Li J, Schug MD, Smith SG, DeAngelis M, Mackay TFC, Coyne JA (2004) Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana. Genetics 167:1265–1274

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. Vienna, Austria, https://www.r-project.org/. Accessed 6 Dec 2018

  • Ritchie MG (1996) The shape of female mating preferences. Proc Natl Acad Sci USA 93:14628–14631

    CAS  PubMed  Google Scholar 

  • Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102

    Google Scholar 

  • 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 58:649–657

    CAS  PubMed  Google Scholar 

  • Roberts NS, Mendelson TC (2017) Male mate choice contributes to behavioural isolation in sexually dimorphic fish with traditional sex roles. Anim Behav 130:1–7

    Google Scholar 

  • Robertson HM (1983) Mating behavior and the evolution of Drosophila mauritiana. Evolution 37:1283–1293

    PubMed  Google Scholar 

  • Ruxton GD, Neuhäuser M (2010) Good practice in testing for an association in contingency tables. Behav Ecol Sociobiol 64:1505–1513

    Google Scholar 

  • Ryan MJ, Wagner WE (1987) Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science 236:595–597

    CAS  PubMed  Google Scholar 

  • Ryan MJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657

    PubMed  Google Scholar 

  • Shorey HH (1962) Nature of the sound produced by Drosophila melanogaster during courtship. Science 137:677–678

    CAS  PubMed  Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Svensson EI, Karlsson K, Friberg M, Eroukhmanoff F (2007) Gender differences in species recognition and the evolution of asymmetric sexual isolation. Curr Biol 17:1943–1947

    CAS  PubMed  Google Scholar 

  • Svetec N (2005) Social experience and pheromonal perception can change male-male interactions in Drosophila melanogaster. J Exp Biol 208:891–898

    PubMed  Google Scholar 

  • Tinghitella RM, Zuk M (2009) Asymmetric mating preferences accommodated the rapid evolutionary loss of a sexual signal. Evolution 63:2087–2098

    PubMed  Google Scholar 

  • Tomaru M, Oguma Y (2000) Mate choice in Drosophila melanogaster and D. sechellia: criteria and their variation depending on courtship song. Anim Behav 60:797–804

    CAS  PubMed  Google Scholar 

  • Tomaru M, Yamada H (2011) Courtship of Drosophila, with a special interest in courtship songs. Low Temp Sci 69:61–85

    Google Scholar 

  • Tomaru M, Matsubayashi H, Oguma Y (1995) Heterospecific inter-pulse intervals of courtship song elicit female rejection in Drosophila biauraria. Anim Behav 50:905–914

    Google Scholar 

  • Tomaru M, Matsubayashi H, Oguma Y (1998) Effects of courtship in interspecific crosses among the species of the Drosophila auraria complex (Diptera: Drosophilidae). J Insect Behav 11:383–398

    Google Scholar 

  • Tomaru M, Doi M, Higuchi H, Oguma Y (2000) Courtship song recognition in the Drosophila melanogaster complex: heterospecific songs make females receptive in D. melanogaster, but not in D. sechellia. Evolution 54:1286–1294

    CAS  PubMed  Google Scholar 

  • Tomaru M, Yamada H, Oguma Y (2004) Female mate recognition and sexual isolation depending on courtship song in Drosophila sechellia and its siblings. Genes Genet Sys 79:145–150

    Google Scholar 

  • Tootoonian S, Coen P, Kawai R, Murthy M (2012) Neural representations of courtship song in the Drosophila brain. J Neurosci 32:787–798

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wasserman M, Koepfer HR (1980) Does asymmetrical mating preference show the direction of evolution? Evolution 34:1116–1124

    CAS  PubMed  Google Scholar 

  • Watanabe TK, Kawanishi M (1979) Mating preference and the direction of evolution of Drosophila. Science 205:906–907

    CAS  PubMed  Google Scholar 

  • Wyman MT, Charlton BD, Locatelli Y, Reby D (2011) Variability of female responses to conspecific vs. heterospecific male mating calls in polygynous deer: an open door to hybridization? PLoS One 6:1–6

    Google Scholar 

  • Wyman MT, Locatelli Y, Charlton BD, Reby D (2014) No preference in female sika deer for conspecific over heterospecific male sexual calls in a mate choice context. J Zool 293:92–99

    Google Scholar 

  • Wyman MT, Locatelli Y, Charlton BD, Reby D (2016) Female sexual preferences toward conspecific and hybrid male mating calls in two species of polygynous deer, Cervus elaphus and C. nippon. Evol Biol 43:227–241

    PubMed  Google Scholar 

  • Yoon J, Matsuo E, Yamada D, Mizuno H, Morimoto T, Miyakawa H, Kinoshita S, Ishimoto H, Kamikouchi A (2013) Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila. PLoS One 8:1–13

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the three anonymous reviewers whose comments and suggestions helped to improve and clarify this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masatoshi Tomaru.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 286 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomaru, M., Hattori, E., Yamada, H. et al. Sexual isolation between Drosophila simulans and D. mauritiana: D. simulans females do not discriminate against intact-wing D. mauritiana males. J Ethol 39, 73–87 (2021). https://doi.org/10.1007/s10164-020-00675-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-020-00675-x

Keywords

Navigation