Skip to main content
Log in

Female mate choice determines reproductive isolation between sympatric butterflies

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Animal courtship rituals are important for species recognition, and a variety of cues might be utilized to recognize conspecific mates. In this paper, we investigate different species-recognition mechanisms between two sympatric butterfly sister species: the wood white (Leptidea sinapis) and Real’s wood white (Leptidea reali). We show that males of both species frequently court heterospecific females both under laboratory and field conditions. The long-lasting elaborate courtships impose energetic costs, since the second courtship of males that were introduced to two subsequent conspecific females lasted on average only one fourth as long as the first courtship. In this paper, we demonstrate that premating reproductive isolation is dependent on female unwillingness to accept heterospecific mates. We studied female and male courtship behavior, chemical signaling, and the morphology of the sexually dimorphic antennae, one of the few male traits visible for females during courtship. We found no differences in ultraviolet (UV) reflectance and only small differences in longer wavelengths and brightness, significant between-species differences, but strongly overlapping distributions of male L. sinapis and L. reali antennal morphology and chemical signals and minor differences in courtship behavior. The lack of clear-cut between-species differences further explains the lack of male species recognition, and the overall similarity might have caused the long-lasting elaborate courtships, if females need prolonged male courtships to distinguish between con- and heterospecific suitors.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Amiet JL (2004) Ecological niche partitioning between two sympatric sibling Leptidea species (Lepidoptera, Pieridae). Rev Ecol (Terre Vie) 59:433–452

    Google Scholar 

  • Andersson J, Borg-Karlson AK, Wiklund C (2003) Antiaphrodisiacs in pierid butterflies: a theme with variation!. J Chem Ecol 29:1489–1499

    Article  PubMed  CAS  Google Scholar 

  • Andersson J, Borg-Karlson AK, Vongvanich N, Wiklund C (2007) Male sex pheromone release and female mate choice in a butterfly. J Exp Biol 210:964–970

    Article  PubMed  CAS  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Beneš J, Konvika M, Vrabec V, Zámečník J (2003) Do the sibling species of small whites, Leptidea sinapis and L. reali (Lepidoptera, Pieridae) differ in habitat preferences. Biol Brat 58:943–951

    Google Scholar 

  • Brunton CFA (1998) The evolution of ultraviolet patterns in European Colias butterflies (Lepidoptera, Pieridae): a phylogeny using mitochondrial DNA. Heredity 80:611–616

    Article  CAS  Google Scholar 

  • Butlin RK (1995) Reinforcement—an idea evolving. Trends Ecol Evol 10:432–434

    Article  Google Scholar 

  • Costanzo K, Monteiro A (2007) The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc R Soc Lond, B 274:845–851

    Article  Google Scholar 

  • Coyne JA, Orr HA (1997) ‘Patterns of speciation in Drosophila’ revisited. Evolution 51:295–303

    Article  Google Scholar 

  • Dieckmann U, Doebeli M (2004) Adaptive dynamics of speciation: sexual populations. In: Dieckmann U, Doebeli M, Metz JAJ, Tautz D (eds) Adaptive speciation. CambridgeUniversity Press, Cambridge, UK, pp 76–111

    Google Scholar 

  • Eliasson CU, Ryrholm N, Holmer M, Jilg K, Gärdenfors U (2005) Nationalnyckeln till Sveriges flora och fauna Fjärilar: Dagfjärilar Hesperiidae-Nymphalidae. Uppsala, Sweden: Artdatabanken SLU

    Google Scholar 

  • Fordyce JA, Nice CC, Forister M, Shapiro AM (2002) The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. J Evol Biol 15:871–879

    Article  Google Scholar 

  • Forsberg J, Wiklund C (1989) Mating in the afternoon—time-saving in courtship and remating by females of a polyandrous butterfly Pieris napi L. Behav Ecol Sociobiol 25:349–356

    Article  Google Scholar 

  • Freese A, Fiedler K (2002) Experimental evidence for species distinctness of the two wood white butterfly taxa, Leptidea sinapis and L. reali (Pieridae). Nota lepid 25:39–59

    Google Scholar 

  • Friberg M, Bergman M, Kullberg J, Wahlberg N, Wiklund C (2007) Niche separation in space and time between two sympatric sister species—a case of ecological pleiotropy. Evol Ecol doi:10.1007/s10682-007-9155-y

  • Gavrilets S (2003) Models of speciation: What have we learned in 40 years? Evolution 57:2197–2215

    PubMed  Google Scholar 

  • Gwynne DT (1991) Sexual competition among females: What causes courtship-role reversal? Trends Ecol Evol 6:118

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Kemp DJ (2006) Heightened phenotypic variation and age-based fading of ultraviolet butterfly wing coloration. Evol Ecol Res 8:515–527

    Google Scholar 

  • Kemp DJ, Rutowski RL, Mendoza M (2005) Colour pattern evolution in butterflies: a phylogenetic analysis of structural ultraviolet and melanic markings in North American sulphurs. Evol Ecol Res 7:133–141

    Google Scholar 

  • Kemp DJ, Macedonia JM (2006) Structural ultraviolet ornamentation in the butterfly Hypolimnas bolina L. (Nymphalidae): visual, morphological and ecological properties. Aust J Zool 54:235–244

    Article  Google Scholar 

  • Kemp D, Vukusic JP, Rutowski R (2006) Stress mediated covariance between nanostructural architecture and ultraviolet butterfly colouration. Funct Ecol 20:282–289

    Article  Google Scholar 

  • Lorkovic´ Z (1993) “Leptidea reali REISSINGER 1989 (=lorkovicii REAL 1988), a new European species (Lepid., Pieridae). Nat Croat 2:1–26

    Google Scholar 

  • Löfstedt C, Herrebout WM, Menken SBJ (1991) Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecol 2:20–28

    Article  Google Scholar 

  • Marshall JL, Arnold ML, Howard DJ (2002) Reinforcement: the road not taken. Trends Ecol Evol 17:558

    Article  Google Scholar 

  • Martin J-F, Gilles A, Descimon H (2003) Species concepts and sibling species: the case of Leptidea sinapis and Leptidea reali. In: Boggs CL, Watt WB Ehrlich PR (eds) Butterflies—ecology and evolution—taking flight. University of Chicago Press, Chicago, Illinois, pp 459–476

    Google Scholar 

  • Mazel R (2002) Répartition géographique de Leptidea sinapis (L., 1758) et L. reali Reissinger, 1989 au nord de l’Europe, en Russie et dans quelqes pays d’Asie (Lepidoptera: Pieridae, Dismorphiinae). Linn Belg 18:373–376

    Google Scholar 

  • Mazel R (2005) Éléments de phylogénie dans le genre Leptidea Bilberg 1820 (Lepidoptera, Pieridae, Dismorphiinae). Rev l’Ass Roussill d’Entomol 14:98–111

    Google Scholar 

  • Mazel R, Eitschberger U (2003) Biogéographie de Leptidea reali Reissinger, 1989 en Europe et en Turquie/Die Verbreitung von Leptidea reali Reissinger, 1989 in Europa und in der Türkei. Rev l’Ass Roussill d’Entomol 12:91–109

    Google Scholar 

  • Obara Y (1964) Mating behaviour of the cabbage white, Pieris rapae crucivora II: the ‘mate-refusal’ posture of the female. Zool Mag 73:175–178

    Google Scholar 

  • Parker GA, Partridge L (1998) Sexual conflict and speciation. Philos Trans R Soc Lond, B 353:261–274

    Article  CAS  Google Scholar 

  • Pfennig KS, Pfennig DW (2005) Character displacement as the “best of a bad situation": Fitness trade-offs resulting from selection to minimize resource and mate competition. Evolution 59:2200–2208

    PubMed  Google Scholar 

  • Phelan PL, Baker TC (1987) Evolution of male pheromones in moths—reproductive isolation through sexual selection. Science 235:205–207

    Article  PubMed  Google Scholar 

  • Rundle HD, Schluter D (1998) Reinforcement of stickleback mate preferences: Sympatry breeds contempt. Evolution 52:200–208

    Article  Google Scholar 

  • Rutowski RL (1978) The courtship behaviour of the small sulphur butterfly, Eurema lisa. Anim Behav 26:892–903

    Article  Google Scholar 

  • Rutowski RL (1981) Courtship behavior of the dainty sulfur butterfly, Nathalis iole with a description of a new, facultative male display (Pieridae). J Res Lepid 20:161–169

    Article  Google Scholar 

  • Rutowski RL (1983) The wing-waving display of Eurema daira males (Lepidoptera: Pieridae): its structure and role in succssful courtship. Anim Behav 31:985–989

    Article  Google Scholar 

  • Rutowski RL (1985) Evidence for mate choice in a sulphur butterfly (Colias eurytheme). Z Tierpsychol 70:103–114

    Google Scholar 

  • Schluter D (1988) Character displacement and the adaptive divergence of finches on islands and continents. Am Nat 131:799–824

    Article  Google Scholar 

  • Silberglied RE, Taylor OR (1973) Ultraviolet differences between sulfur butterflies Colias eurythreme and C. phliodice, and a possible isolating mechanism. Nature 241:406–408

    Article  Google Scholar 

  • Silberglied RE, Taylor OR (1978) Ultraviolet reflection and its behavioral role in the courtship of the sulphur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behav Ecol Sociobiol 3:203–243

    Article  Google Scholar 

  • StatSoft (2005)STATISTICA (data analysis software system) version 71. www.statsoft.com

  • Taylor OR (1973) Reproductive isolation in Colias eurytheme and C. philodice (Lepidoptera: Pieridae): use of olfaction in mate selection. Ann Entomol Soc Am 66:621–626

    Google Scholar 

  • Tolman T, Lewington R (1997) Collins field guide butterflies Britain and Europe. Harper Collins, London

    Google Scholar 

  • Vane-Wright RI, Boppre M (1993) Visual and chemical signalling in butterflies: functional and phylogenetic perspectives. Philos Trans R Soc Lond, B 340:197–205

    Article  Google Scholar 

  • Wasserman M, Koepfer HR (1977) Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 31:812–823

    Article  Google Scholar 

  • Wiklund C (1977) Courtship behaviour in relation to female monogamy in Leptidea sinapis (Lepidoptera). Oikos 29:275–283

    Article  Google Scholar 

  • Wiklund C, Forsberg J (1986) Courtship and male discrimination between virgin and mated females in the orange tip butterfly Anthocharis cardamines. Anim Behav 34:328–332

    Article  Google Scholar 

  • Wiklund C, Lindfors V, Forsberg J (1996) Early male emergence and reproductive phenology of the adult overwintering butterfly Gonepteryx rhamni in Sweden. Oikos 75:227–240

    Article  Google Scholar 

  • Vila R, Viader S, Jubany J (2003) Leptidea sinapis (Linnaeus, 1758) i L. reali (Reissinger 1988): dues ecpécies “bessones” a Catalunya i Andorra (Lepidoptera: Pieridae). Buttl Soc Cat Lepid 90:25–47

    Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgements

We thank Bertil Borg, Karin Norén, Veronica Nyström and two anonymous reviewers for useful comments on earlier drafts of this manuscript, and Moa Lönn for illustrations. The study was funded by The Swedish Research Council to Christer Wiklund and Anna-Karin Borg-Karlson.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Magne Friberg.

Additional information

Communicated by D. Gwynne

Rights and permissions

Reprints and permissions

About this article

Cite this article

Friberg, M., Vongvanich, N., Borg-Karlson, AK. et al. Female mate choice determines reproductive isolation between sympatric butterflies. Behav Ecol Sociobiol 62, 873–886 (2008). https://doi.org/10.1007/s00265-007-0511-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0511-2

Keywords

Navigation