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No Evidence that Male Choice Contributes to the Maintenance of a Shared, Sex-Limited Trait in Mimetic and Non-mimetic Female Tiger Swallowtail Butterflies, Papilio glaucus

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Abstract

In animal species that have morphological polymorphisms maintained by unique or divergent selection pressures, understanding the preservation of shared traits is important for identifying the factors that are influencing overall evolutionary processes. In the Eastern tiger swallowtail butterfly, Papilio glaucus, females are dimorphic. One morph (‘dark-morph’) is mostly black and mimics the toxic pipevine swallowtail, Battus philenor. These females have large amounts of blue coloration on the dorsal hind wings that enhances their mimetic resemblance. Conversely, the alternate female type (‘yellow-morph’) is similar to males in coloration with the exception of extensive dorsal blue coloration, comparable to dark-morph females. Such coloration is almost completely absent in males. We examined dorsal blue coloration in P. glaucus to determine if mimetic resemblance in dark morphs is predominantly responsible for the maintenance of dorsal blue color in both female types, or whether mate recognition and/or sexual selection by males has a stronger influence on this trait. We measured the relative amount and variance of dorsal and ventral blue coloration in females of both color morphs, as well as males. We also compared these measurements to similar ones taken in the sister species, P. canadensis (which does not exhibit female dimorphism). Lastly, we investigated mate recognition and preferences of wild males. Our results suggest that mimetic resemblance may be more important than sexual selection for sustaining dorsal blue coloration in dark-morph females and that yellow-morphs could have elevated levels of blue due to currently unknown genetic associations. Although trait correlation between sexes is common, intrasexual trait correlation in a sex-limited, polymorphic species has not been frequently observed.

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References

  • Abramoff, M. D., Magelhaes, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.

    Google Scholar 

  • Allen, C. E., Zwaan, B. J., & Brakefield, P. M. (2010). Evolution of sexual dimorphism in the Lepidoptera. Annual Review of Entomology, 56, 445–464.

    Article  Google Scholar 

  • Arms, K., Feeny, P., & Lederhouse, R. C. (1974). Sodium: Stimulus for puddling behavior by tiger swallowtail butterflies, Papilio glaucus. Science, 185, 372–374.

    Article  PubMed  CAS  Google Scholar 

  • Bonduriansky, R. (2001). The evolution of male mate choice in insects: A synthesis of ideas and evidence. Biological Review, 76, 305–309.

    Article  CAS  Google Scholar 

  • Bosi, S. G., Hayes, J., Large, M. C. J., & Poladian, L. (2008). Color, iridescence, and thermoregulation in Lepidoptera. Applied Optics, 47, 5235–5241.

    Article  PubMed  Google Scholar 

  • Brower, J. V. Z. (1958). Experimental studies of mimicry in some North American butterflies: Part II. Battus philenor and Papilio Troilus, P. polyxenes, and P. glaucus. Evolution, 12, 123–136.

    Article  Google Scholar 

  • Brower, L. P. (1959). Speciation in butterflies of the Papilio glaucus group. II. Ecological relationships and interspecific sexual behavior. Evolution, 13, 212–228.

    Article  Google Scholar 

  • Brower, L. P., & Brower, J. V. Z. (1962). The relative abundance of model and mimic butterflies in natural populations of the Battus philenor mimicry complex. Ecology, 42, 154–158.

    Google Scholar 

  • Cardoso, G. C., & Mota, P. G. (2010). Evolution of female carotenoid coloration by sexual constraint in Carduelis finches. BMC Evolutionary Biology, 10, 82.

    Article  PubMed  Google Scholar 

  • Chamberlin, N. L., Hill, R. I., Kapan, D. D., Gilbert, L. E., & Kronforst, M. R. (2009). Polymorphic butterfly reveals the missing link in ecological speciation. Science, 326, 847–850.

    Article  Google Scholar 

  • Chen, D., Collins, J. S., & Goldsmith, T. H. (1984). The UV receptor of bird retinas. Science, 225, 337–339.

    Article  PubMed  CAS  Google Scholar 

  • Church, S. C., Bennett, A. T. D., Cuthill, I. C., & Partridge, J. C. (1998). Ultraviolet cues affect the foraging behavior of blue tits. Proceedings of the Royal Society B, 265, 1509–1514.

    Article  Google Scholar 

  • Clarke, C. A., & Sheppard, P. M. (1959). The genetics of some mimetic forms of Papilio dardanus, Brown, and Papilio glaucus, Linn. Journal of Genetics, 56, 236–260.

    Article  Google Scholar 

  • Codella, S. G., & Lederhouse, R. C. (1989). Intersexual selection constraints the evolution of the dorsal pattern of male black swallowtail butterflies, Papilio polyxenes. Evolution, 50, 717–722.

    Google Scholar 

  • Codella, S. G., & Lederhouse, R. C. (1990). The effect of wing orientation on aposematic signaling in the pipevine swallowtail butterfly, Battus philenor. Animal Behaviour, 40, 404–406.

    Article  Google Scholar 

  • Cooper, I. A. (2010). Ecology of sexual dimorphism and clinal variation of coloration in a damselfly. American Naturalist, 176, 566–572.

    Article  PubMed  Google Scholar 

  • Cuthill, I. C., & Bennett, A. T. D. (1993). Mimicry and the eye of the beholder. Proceedings of the Royal Society B, 243, 203–204.

    Article  Google Scholar 

  • Darwin, C. (1871). The descent of man, and selection in relation to sex. London: John Murray.

    Book  Google Scholar 

  • Deering, M. D., & Scriber, J. M. (2002). Field bioassays show heterospecific mating preference asymmetry between hybridizing North American Papilio butterfly species (Lepidoptera: Papilionidae). Journal of Ethology, 20, 25–33.

    Article  Google Scholar 

  • Delhey, K., & Peters, A. (2008). Quantifying variability of avian colours: are signaling traits more variable? PLoS ONE, 3, e168.

    Article  Google Scholar 

  • Douglas, M. M. (1981). Thermoregulatory significance of thoracic lobes in the evolution of insect wings. Science, 211, 84–86.

    Article  PubMed  CAS  Google Scholar 

  • Gray, S. M., & McKinnon, J. S. (2007). Linking color polymorphism maintenance and speciation. Trends in Ecology & Evolution, 22, 71–79.

    Article  Google Scholar 

  • Hagen, R. H., & Scriber, J. M. (1989). Sex-linked diapause, color, and allozyme loci in Papilio glaucus—Linkage analysis and significance in a hybrid zone. Journal of Heredity, 80, 179–185.

    Google Scholar 

  • Hereau, H., & Scriber, J. M. (2003). Interspecific copulation of a dark morph Papilio glaucus female and a male P. polyxenes (Papilionidae): Observation and significance. Journal of the Lepidopterists Society, 57, 71–74.

    Google Scholar 

  • Holloway, G., Gilbert, F., & Brandt, A. (2002). The relationship between mimetic imperfection and phenotypic variation in insect colour patterns. Proceedings of the Royal Society B, 269, 411–416.

    Article  PubMed  Google Scholar 

  • Holm, S. (1979). A simple sequentially rejective Bonferroni test procedure. Scandinavian Journal of Statistics, 6, 65–70.

    Google Scholar 

  • Jiggins, C. D., Naisbit, R. E., Coe, R. L., & Mallet, J. (2001). Reproductive isolation caused by colour pattern mimicry. Nature, 411, 302–305.

    Article  PubMed  CAS  Google Scholar 

  • Kemp, D. J., & Rutowski, R. L. (2011). The role of coloration in mate choice and sexual interactions in butterflies. Advances in the Study of Behavior, 43, 55–91.

    Article  Google Scholar 

  • Keselman, H. J., Games, P. A., & Clinch, J. J. (1979). Tests for homogeneity of variance. Communications in Statisitcs-Simulation and Computation, B8, 113–129.

    Article  Google Scholar 

  • Knüttel, H., & Fiedler, K. (2001). Host plant-derived variation in ultraviolet wing patterns influences mate selection by male butterflies. Journal of Experimental Biology, 204, 2447–2459.

    PubMed  Google Scholar 

  • Koch, P. B., Keys, D. N., Rocheleau, T., Aronstein, K., Blackburn, M., Carroll, S. B., et al. (1998). Regulation of dopa decarboxylase expression during colour pattern formation in wild-type and melanic tiger swallowtail butterflies. Development, 125, 2303–2313.

    PubMed  CAS  Google Scholar 

  • Krebs, R. A. (1988). The mating behavior of Papilio glaucus (Papilionidae). Journal of Research on the Lepidoptera, 26, 27–31.

    Google Scholar 

  • Krebs, R. A., & West, D. A. (1988). Female mate preference and the evolution of female-limited Batesian mimicry. Evolution, 42, 1101–1104.

    Article  Google Scholar 

  • Kunte, K. (2008). Mimetic butterflies support Wallace’s model of sexual dimorphism. Proceedings of the Royal Society B, 275, 1617–1624.

    Article  PubMed  Google Scholar 

  • Kunte, K. (2009). Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection. Animal Behaviour, 78, 1029–1036.

    Article  Google Scholar 

  • Lande, R. (1980). Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution, 34, 292–305.

    Article  Google Scholar 

  • Landini, G. (2010). Threshold_Color, Version 1.12 for ImageJ. Available from http://www.dentistry.bham.ac.uk/landinig/software. Accessed on May 10, 2010.

  • Lederhouse, R. C., Ayres, M. P., & Scriber, J. M. (1990). Adult nutrition affects male virility in Papilio glaucus L. Functional Ecology, 4, 743–751.

    Article  Google Scholar 

  • Lederhouse, R. C., & Scriber, J. M. (1996). Intrasexual selection constrains the evolution of the dorsal color pattern of male black swallowtail butterflies, Papilio polyxenes. Evolution, 50, 717–722.

    Article  Google Scholar 

  • Morris, W. A. (1953). The chipmunk as a predator of the adult yellow swallowtail butterfly. Journal of Mammalogy, 34, 510–511.

    Google Scholar 

  • Naisbit, R. E., Jiggins, C. D., & Mallet, J. (2001). Disruptive selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomenei. Proceedings of the Royal Society B, 268, 1849–1854.

    Article  PubMed  CAS  Google Scholar 

  • Nijhout, H. F. (2003). Polymorphic mimicry in Papilio dardanus: Mosaic dominance, big effects and origins. Evolution & Development, 5, 579–592.

    Article  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 B, 276, 2369–2375.

    Article  PubMed  Google Scholar 

  • Platt, A. P., Harrison, S. J., & Williams, T. F. (1984). Absence of differential mate selection in the North American Tiger Swallowtail Papilio glaucus. In R. I. Vane-Wright & P. R. Ackery (Eds.), The biology of butterflies (pp. 245–250). London: Academic Press.

    Google Scholar 

  • Pomiankowski, A., & Møller, A. P. (1995). A resolution of the lek paradox. Proceedings of the Royal Society B, 260, 21–29.

    Article  Google Scholar 

  • R Core Development Team. (2011). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org.

  • Rawson, G. W., & Bellinger, P. F. (1953). Sparrows feeding on congregating Papilio. Lepidopterists’ News, 7, 27.

    Google Scholar 

  • Rutowski, R. L. (1997). Sexual dimorphism, mating systems, and ecology in butterflies. In J. C. Choe & B. J. Crespi (Eds.), The evolution of mating systems in insects and arachnids (pp. 257–272). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Rutowski, R. L., Nahm, A. C., & Macedonia, J. M. (2010). Iridescent hindwing patches in the Pipevine Swallowtail: Differences in dorsal and ventral surfaces relate to signal function and context. Functional Ecology, 24, 767–775.

    Article  Google Scholar 

  • Scriber, J. M. (1987). Puddling by female Florida tiger swallowtail butterflies, Papilio-glaucus-australis (Lepidoptera: Papilionidae). Great Lakes Entomologist, 20, 21–23.

    Google Scholar 

  • Scriber, J. M. (1996). Tiger tales: natural history of native North American swallowtails. American Naturalist, 42, 19–32.

    Google Scholar 

  • Scriber, J. M., Hagen, R. H., & Lederhouse, R. C. (1996). Genetics of mimicry in the tiger swallowtail butterflies, Papilio glaucus and P. canadensis (Lepidoptera: Papilionidae). Evolution, 50, 222–236.

    Article  Google Scholar 

  • Shine, R. (1989). Ecological causes for the evolution of sexual dimorphism: A review of the evidence. The Quarterly Review of Biology, 64, 419–461.

    Article  PubMed  CAS  Google Scholar 

  • Svensson, E. I., Abbott, J. K., Gosden, T. P., & Coreau, A. (2007). Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evolutionary Ecology, 23, 93–108.

    Article  Google Scholar 

  • Van Valen, L. (2005). The statistics of variation. In B. Hallgrímsson & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 29–48). Burlington, MA: Elsevier Academic Press.

    Google Scholar 

  • Wallace, A. R. (1864). On the phenomenon of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Transactions of the Linnean Society, 25, 1–71.

    Article  Google Scholar 

  • Welch, B. L. (1951). On the comparison of several mean values: An alternative approach. Biometrika, 38, 330–336.

    Google Scholar 

  • Wiernasz, D. C., & Kingsolver, J. G. (1992). Wing melanin pattern mediates species recognition in Pieris occidentalis. Animal Behavior, 43, 89–94.

    Article  Google Scholar 

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Acknowledgments

We thank M. Schumer and K. Kunte for helpful comments on earlier drafts of this work. Additionally, two anonymous reviewers provided many useful comments. We would also like to thank R. Mercader and G. Ording for project advice, S. Ryan for field assistance, and A. Kosnick and B. Sonke for assistance with rearing females. H. Romack and B. Houtz provided pupae for experimentation. H. Romack also provided Vermont males and females for wing analysis. J. Maudsley provided Georgia specimens for wing analysis. M. Aardema was supported by an MSU Plant Sciences Fellowship, a Scriber Scholars award in Butterfly Biology and Conservation, and a Jeffery Boettcher travel grant. Partial support was also provided by MAES project #01644, NSF DEB-0716683, and NSF DEB-0918879.

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Correspondence to Matthew L. Aardema.

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11692_2012_9190_MOESM1_ESM.jpg

Figure 1. A dark-morph female P. glaucus (top left). A yellow-morph female P. glaucus (top right). A male Battus philenor (bottom left). A male P. glaucus (bottom right). B. philenor is presumed to be a model for many mimetic butterflies including dark-morph female P. glaucus. All images are of the dorsal side of the butterfly. Note the near absence of blue coloration in the P. glaucus male. (JPEG 766 kb)

11692_2012_9190_MOESM2_ESM.jpg

Figure 2. Representative reflectance curves of three female P. glaucus wings in a predominately blue area, black area and a blue area that has been masked by black ink. The reflectance of the blue-covered areas is very similar to the naturally black areas. Also note the high peak between 300 and 400 nm for the blue coloration. This area indicates UV reflectance. (JPEG 730 kb)

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Aardema, M.L., Scriber, J.M. No Evidence that Male Choice Contributes to the Maintenance of a Shared, Sex-Limited Trait in Mimetic and Non-mimetic Female Tiger Swallowtail Butterflies, Papilio glaucus . Evol Biol 40, 108–116 (2013). https://doi.org/10.1007/s11692-012-9190-7

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