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Dissecting the nature of subtle phenotypic variation in wing colour elements of Müllerian co-mimics

Published online by Cambridge University Press:  10 April 2017

Márcio Zikán Cardoso*
Affiliation:
Department of Ecology, Federal University of Rio Grande do Norte, Natal-RN, 59078–900, Brazil
Luciana Lopes Ferreira de Lima
Affiliation:
Department of Ecology, Federal University of Rio Grande do Norte, Natal-RN, 59078–900, Brazil
*
*Corresponding author. Email: [email protected]

Abstract:

Polymorphism is common in nature, but few Heliconius species are polymorphic for wing colour patterns. Eastern Brazil H. erato phyllis populations are polymorphic for hindwing elements (red raylets) and studies suggest that trait distribution varies seasonally. We carried a 3-y sampling to evaluate the hypothesis that season, wing length and pollen foraging were associated with morph diversity. Individual phenotypes were scored with regards to number of red elements in the dry and in the wet seasons. Co-mimic H. melpomene nanna was also analysed. We scored 432 H. erato and 513 H. melpomene. Our results confirm polymorphism in H. erato, with individuals showing from one to eight elements, with a mode between five and six. We found that H. melpomene is polymorphic for red dots, varying from two to five (mode = 2). Red basal dots were mostly invariant in H. erato. Even though we found a seasonal change in pollen loads, we found no association between individual phenotypes and season, pollen load scores, or wing length. We reject the hypothesis of ecological correlates of morph frequency, and suggest that trait colour variation in the two species is linked to and constrained by effects on mate recognition.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

LITERATURE CITED

AGRESTI, A. 2002. Categorical data analysis. John Wiley & Sons, New York.CrossRefGoogle Scholar
BOGGS, C. L. 1981. Nutritional and life-history determinants of resource allocation in holometabolous insects. American Naturalist 117:692709.Google Scholar
BOND, A. B. 2007. The evolution of color polymorphism: crypticity, searching images, and apostatic selection. Annual Review of Ecology, Evolution, and Systematics 38:489514.Google Scholar
BROWN, K. S. 1979. Ecologia geográfica e Evolução nas Florestas Neotropicais. Full Professorship Thesis. Universidade Estadual de Campinas, Campinas. Available online at www.ucl.ac.uk/taxome/lit/brown79/brown79.html.Google Scholar
BROWN, K. S. & BENSON, W. W. 1974. Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid. Nymph.). Biotropica 6:205228.CrossRefGoogle Scholar
CARDOSO, M. Z. 2001. Patterns of pollen collection and flower visitation by Heliconius butterflies in southeastern Mexico. Journal of Tropical Ecology 17:763768.CrossRefGoogle Scholar
CARLSON, J. E. & HOLSINGER, K. E. 2010. Natural selection on inflorescence color polymorphisms in wild protea populations: the role of pollinators, seed predators, and intertrait correlations. American Journal of Botany 97:934944.CrossRefGoogle ScholarPubMed
CLABAUT, C., HERREL, A., SANGER, T. J., SMITH, T. B. & ABZHANOV, A. 2009. Development of beak polymorphism in the African seedcracker, Pyrenestes ostrinus. Evolution and Development 11:636646.Google Scholar
COOK, L. M. & SACCHERI, I. J. 2013. The peppered moth and industrial melanism: evolution of a natural selection case study. Heredity 110:207212.Google Scholar
COOK, L. M., GRANT, B. S., SACCHERI, I. J. & MALLET, J. 2012. Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biology Letters 8:609612.CrossRefGoogle ScholarPubMed
CUTHILL, J. F. H. & CHARLESTON, M. 2015. Wing patterning genes and coevolution of Müllerian mimicry in Heliconius butterflies: support from phylogeography, cophylogeny, and divergence times. Evolution 69:30823096.Google Scholar
EMSLEY, M. 1964. The geographical distribution of the color-pattern components of Heliconius erato and Heliconius melpomene with genetical evidence for the systematic relationship between the two species. Zoologica 49:245286.Google Scholar
ESTRADA, C. & JIGGINS, C. D. 2008. Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species? Journal of Evolutionary Biology 21:749760.CrossRefGoogle Scholar
FLANAGAN, N. S., TOBLER, A., DAVISON, A., PYBUS, O. G., KAPAN, D. D., PLANAS, S., LINARES, M., HECKEL, D. & MCMILLAN, W. O. 2004. Historical demography of Müllerian mimicry in the neotropical Heliconius butterflies. Proceedings of the National Academy of Sciences USA 101:97049709.Google Scholar
FORDYCE, J. A., NICE, C. C., FORISTER, M. L. & SHAPIRO, A. M. 2002. The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. Journal of Evolutionary Biology 15:871879.CrossRefGoogle Scholar
GILBERT, L. E. 1983. Coevolution and mimicry. Pp. 263281 in Futuyma, D. J. & Slatkin, M. (eds). Coevolution. Sinauer Associates, Sunderland, MA.Google Scholar
HATADANI, L. M., BAPTISTA, J. C. R., SOUZA, W. N. & KLACZKO, L. B. 2004. Colour polymorphism in Drosophila mediopunctata: genetic (chromosomal) analysis and nonrandom association with chromosome inversions. Heredity 93:525534.Google Scholar
HILL, R. I., GILBERT, L. E. & KRONFORST, M. R. 2013. Cryptic genetic and wing pattern diversity in a mimetic Heliconius butterfly. Molecular Ecology 22:27602770.Google Scholar
JORON, M., WYNNE, I. R., LAMAS, G. & MALLET, J. 1999. Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata . Evolutionary Ecology 13:721754.Google Scholar
KAPAN, D. D. 2001. Three-butterfly system provides a field test of Müllerian mimicry. Nature 409:338340.Google Scholar
KARLSSON, B. 1995. Resource allocation and mating systems in butterflies. Evolution 49:955961.Google Scholar
KRONFORST, M. & PAPA, R. 2015. The functional basis of wing patterning in Heliconius butterflies: the molecules behind the mimicry. Genetics 200:119.Google Scholar
KUNTE, K., ZHANG, W., TENGER-TROLANDER, A., PALMER, D. H., MARTIN, A., REED, R. D., MULLEN, S. P. & KRONFORST, M. R. 2014. doublesex is a mimicry supergene. Nature 507:229233.CrossRefGoogle ScholarPubMed
MOURA, P. A., QUEK, S.-P., CARDOSO, M. Z. & KRONFORST, M. R. 2011. Comparative population genetics of mimetic Heliconius butterflies in an endangered habitat; Brazil's Atlantic forest. BMC Genetics 12:9.Google Scholar
OLIVER, J. C., ROBERTSON, K. A. & MONTEIRO, A. 2009. Accommodating natural and sexual selection in butterfly wing pattern evolution. Proceedings of the Royal Society of London B (Biological Sciences) 276:23692375.CrossRefGoogle ScholarPubMed
PANSERA, M. C. G. & ARAUJO, A. M. 1983. Distribution and heritability of the red raylets in Heliconius erato phyllis (Lepid.; Nymph.). Heredity 51:643652.CrossRefGoogle Scholar
RAMOS, R. R. & FREITAS, A. V. L. 1999. Population biology and wing color variation in Heliconius erato phyllis (Nymphalidae). Journal of the Lepidopterists’ Society 53:1121.Google Scholar
SHEPPARD, P. M., TURNER, J. R. G., BROWN, K. S., BENSON, W. W. & SINGER, M. C. 1985. Genetics and the evolution of Muellerian mimicry in Heliconius butterflies. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 308:433610.Google Scholar
SMITH, T. B. 1993. Disruptive selection and the genetic basis of bill size polymorphism in the African finch Pyrenestes . Nature 363:618620.CrossRefGoogle Scholar
THOMPSON, J. N. 1997. Evaluating the dynamics of coevolution among geographically structures populations. Ecology 78:16191623.CrossRefGoogle Scholar
VENABLES, W. N. & RIPLEY, B. D. 2002. Modern applied statistics with S. Springer, New York. 498 pp.CrossRefGoogle Scholar
WHITE, T. W. & KEMP, D. J. 2016. Colour polymorphism. Current Biology 26:R515–522.Google Scholar