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Analysis of the mating behavior and some possible causes of male copulatory success in Dryas iulia alcionea (Lepidoptera, Nymphalidae, Heliconiinae)

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Abstract

In this study we examined the mating behavior of Dryas iulia and the acceptance and rejection mechanisms of females during courtship activity. An ethogram of mating behavior was organized on the basis of 100 h of observation in an insectarium. Several different behaviors were catalogued and separated into two behavioral repertoires (pre-coupling, post-coupling). The behavioral sequence of mating behavior was also analyzed using a total of 53 pairs of D. iulia. The courtship activities involved interactions between the sexes in three sequential phases—the aerial, air-ground, and ground phases. In 49% of observations the courtship activities led to copulation. The mean time to the occurrence of the first interaction between males and females did not differ between interactions with and without copulation. The behavior of females and males in the two groups were analyzed and differences were found between behavioral activities of both sexes. The results indicate that males’ insistence on courtship does not affect their copulatory success, and that females play a decisive role in copulation occurrence. Analysis of behavioral transitions showed there are many alternative behavioral routines in interactions with and without copulation. The number of behavioral transitions recorded was smaller in the group in which copulation occurred, indicating that males with copulatory success modified their behavior less frequently. Successful males recorded more transitions with a probability of occurrence greater than 0.4, and their behavioral activity was also less reticulated. Analysis using the stereotyping index showed that situations in which copulations occurred were more stereotyped than those in which it did not.

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References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Andersson J, Borg-Karlson AK, Wiklund C (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B Biol Sci 267:1271–1275

    Article  CAS  Google Scholar 

  • Arnqvist G, Rowe L (1995) Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc R Soc Lond B Biol Sci 261:123–127

    Article  Google Scholar 

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

    Google Scholar 

  • Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. Proc Natl Acad Sci USA 97:10460–10464

    Article  CAS  PubMed  Google Scholar 

  • Baker TC, Cardé RT (1979) Courtship behavior of the oriental fruit moth (Grapholita molesta): experimental analysis and consideration of the role of sexual selection in the evolution of courtship pheromones in the Lepidoptera. Ann Entomol Soc Am 72:173–188

    Google Scholar 

  • Blanckenhorn WU, Dixon AFG, Fairbairn DJ, Foellmer MW, Gibert P, van der Linde K, Meier R, Nylin S, Pitnick S, Schoff C, Signorelli M, Teder T, Wiklund C (2007) Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am Nat 169:245–257

    Article  PubMed  Google Scholar 

  • Boggs CL (1981) Selection pressures affecting male nutrient investment at mating in Heliconiine butterflies. Evolution 35:931–940

    Article  Google Scholar 

  • Brower AVZ (1996) Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50:195–221

    Article  CAS  Google Scholar 

  • Brower LP, Brower JVC, Cranston FP (1965) Courtship behavior of the queen butterfly Danaus gilippus berenice. Zoologica 50:1–39

    CAS  Google Scholar 

  • Brown KS Jr (1981) The biology of Heliconius and related genera. Ann Rev Entomol 26:427–456

    Article  Google Scholar 

  • Brown KS Jr, Sheppard PM, Turner JRG (1974) Quaternary refugia in tropical America: evidence from race formation in Heliconius butterflies. Proc R Soc Lond B Biol Sci 187:369–378

    Article  Google Scholar 

  • Chapman T, Arnqvist G, Bahghamm J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  • Crane J (1955) Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoologica 40:167–195

    Google Scholar 

  • Daniels JC (2007) Courtship solicitation by females of the barred sulphur butterfly (Eurema daira)(Lepidoptera: Pieridae). J Insect Behav 20:129–135

    Article  Google Scholar 

  • Davies N, Bermingham E (2002) The historical biogeography of two Caribbean butterflies (Lepidoptera: Heliconiidae) as inferred from genetic variation at multiple loci. Evolution 56:573–589

    CAS  PubMed  Google Scholar 

  • Emsley MG (1963) A morphological study of imagine Heliconiinae (Lepidoptera: Nymphalidae) with consideration of the evolutionary relationships within the group. Zoologica 48:85–131

    Google Scholar 

  • Emsley MG (1970) An observation on the use of color for species-recognition in Heliconius besckei (Nymphalidae). J Lepid Soc 24:25

    Google Scholar 

  • Finch H (2005) Comparison of the performance of nonparametric and parametric MANOVA test statistics when assumptions are violated. Methodology 1:27–38

    Google Scholar 

  • Flanagan N, Tobler A, Kapan D, Davison A, Pybus O, Planas S (2004) Historical demography of Müllerian mimicry in the neotropical Heliconius butterflies. Proc Natl Acad Sci USA 101:9704–9709

    Article  CAS  PubMed  Google Scholar 

  • Garcias G (1983) Aspectos da biologia populacional de cinco espécies de heliconiíneos do anel mimético “laranja” (Lepidotera, Nymphalidae). M.Sc. thesis. Department of Genetics, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS

  • Gilbert LE (1976) Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? Science 193:419–420

    Article  CAS  PubMed  Google Scholar 

  • Girling RD, Cardé RT (2006) Analysis of the courtship behavior of the navel orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae), with a commentary on methods for the analysis of sequences of behavioral transitions. J Insect Behav 19:497–520

    Article  Google Scholar 

  • Haag KL, Araújo AM (1994) Inbreeding, genetic load and morphometric variation in natural populations of Dryas iulia (Lepidoptera, Nymphalidae). Rev Bras Genet 17:35–39

    Google Scholar 

  • Haynes KF, Birch MC (1984) Mate-locating and courtship behaviors of the artichoke plume moth, Platyptilia carduidactyla (Lepidoptera: Pterophoridae). Environ Entomol 13:399–408

    Google Scholar 

  • Hernández MIM, Benson WW (1998) Small-male advantage in the territorial tropical butterfly Heliconius sara (Nymphalidae): a paradoxical strategy? Anim Behav 56:533–540

    Article  PubMed  Google Scholar 

  • Japyassú HF, Alberts CC, Izar P, Sato T (2006) EthoSeq: a tool for phylogenetic analysis and data mining in behavioral sequences. Behav Res Methods 38:549–556

    PubMed  Google Scholar 

  • Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411:302–305

    Article  CAS  PubMed  Google Scholar 

  • Jiggins CD, Estrada C, Rodrigues A (2004) Mimicry and the evolution of pre-mating isolation in Heliconius melpomene. J Evol Biol 17:680–691

    Article  CAS  PubMed  Google Scholar 

  • Jiggins CD, Mavárez J, Beltrán M, McMillan WO, Johnston JS, Bermingham EB (2005) A genetic linkage map of the mimetic butterfly, Heliconius melpomene. Genetics 171:557–570

    Article  CAS  PubMed  Google Scholar 

  • Joron M, Jiggins CD, Papanicolaou A, McMillan WO (2006) Heliconius wing patterns: an evo–devo model for understanding phenotypic diversity. Heredity 97:157–167

    Article  CAS  PubMed  Google Scholar 

  • Kemp DJ (2002) Sexual selection constrained by life history in a butterfly. Proc Biol sci 269:1341–1345

    Article  PubMed  Google Scholar 

  • Krebs RA (1988) The matting behavior of Papilio glaucus (Papilionidae). J Res Lepid 26:27–31

    Google Scholar 

  • Kronforst MR, Young LG, Gilbert LE (2007) Reinforcement of mate preference among hybridizing Heliconius butterflies. J Evol Biol 20:278–285

    Article  CAS  PubMed  Google Scholar 

  • Lutz L (2002) Contextos fenotípicos multifuncionais: influência do padrão de coloração de uma borboleta impalatável (Heliconius erato phyllis) sobre seu sucesso de acasalamento, ritmo diário de atividades e sobrevivência em campo. Ph.D. thesis. Department of Genetics, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS

  • Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M (2006) Speciation by hybridization in Heliconius butterflies. Nature 441:868–871

    Article  PubMed  Google Scholar 

  • McMillan WO, Jiggins CD, Mallet J (1997) What initiates speciation in passion-vine butterflies? Proc Natl Acad Sci USA 94:8628–8633

    Article  CAS  PubMed  Google Scholar 

  • Naisbit RE, Jiggins CD, Mallet J (2001) Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene. Proc Biol Sci 268:1849–1854

    Article  CAS  PubMed  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NB (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp 123–166

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Phelan PL, Baker TC (1990) Comparative study of courtship in twelve Phycitine moths (Lepidoptera: Pyralidae). J Insect Behav 3:303–326

    Article  Google Scholar 

  • Rutowski RL (1980) Courtship solicitation by females of the checkered white butterfly Pieris protodice. Behav Ecol Sociobiol 7:113–117

    Article  Google Scholar 

  • Rutowski RL (1984) Sexual selection and the evolution of butterfly mating behavior. J Res Lepid 23:125–142

    Google Scholar 

  • Rutowski RL (1997) Sexual dimorphism, mating systems and ecology in butterflies. In: Choe JC (ed) The evolution of mating systems in insects and arachnids. Library of Congress, Cambridge, pp 257–272

    Google Scholar 

  • Rutowski RL, Schaefer J (1984) The courtship behavior of the gulf fritillary, Agraulis vanillae (Nymphalidae). J Lepid Soc 38:23–31

    Google Scholar 

  • Schulz S, Estrada C, Yildizhan S, Boppré M, Gilbert LE (2008) An antiaphrodisiac in Heliconius melpomene butterflies. J Chem Ecol 34:82–93

    Article  CAS  PubMed  Google Scholar 

  • Scott JA (1972) Mating of butterflies. J Res Lepid 11:99–127

    Google Scholar 

  • Shields O (1967) Hilltopping. J Res Lepid 6:69–178

    Google Scholar 

  • Slater JB, Ollason JC (1973) The temporal patterning of behaviour in isolated male zebra finches: transition analysis. Behaviour 2:248–269

    Google Scholar 

  • Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

    Article  Google Scholar 

  • Wickman PO (1985) Male determines mating duration in butterflies? J Lepid Soc 39:341–342

    Google Scholar 

  • Wiklund C (2003) Sexual selection and the evolution of butterfly mating systems. In: Boggs C (ed) Butterflies: ecology and evolution taking flight. University of Chicago Press, Chicago, pp 67–90

    Google Scholar 

  • Wiklund C, Forsberg J (1991) Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60:373–381

    Article  Google Scholar 

  • Wiklund C, Kaitala A (1995) Sexual selection for large male size in a polyandrous butterfly: the effect of body size on male versus female reproductive success in Pieris napi. Behav Ecol 6:6–13

    Article  Google Scholar 

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Acknowledgments

We are grateful to J. Zanin, G. Pasqualin, A. Carrion, A. A. Ferreira, P. R. Vieira, and A. L. Klein for help in keeping larvae and adults fed adequately. We thank S. Callegari-Jacques for criticism on the statistics, A. L. Klein and M. P. Almerão for suggestions about previous versions of the manuscript, and M. Mega for editing the figures. We also thank Conselho Nacional de Desenvolvimento Tecnológico (CNPq) and Programa de Apoio a Núcleos de Excelência (PRONEX) for financial support.

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Correspondence to Nicolás Oliveira Mega.

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Mega, N.O., de Araújo, A.M. Analysis of the mating behavior and some possible causes of male copulatory success in Dryas iulia alcionea (Lepidoptera, Nymphalidae, Heliconiinae). J Ethol 28, 123–132 (2010). https://doi.org/10.1007/s10164-009-0163-y

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