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Inter-species variation in unpalatability does not explain polymorphism in a mimetic species

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Abstract

Conspicuous colouration in unpalatable organisms acts as a warning signal of their unprofitability, a phenomenon known as aposematism. The protection conferred by such colouration can lead to evolutionary convergence in warning signals between aposematic species, because sharing warning signals reduces the per capita cost of predator learning. Consequently, most aposematic species display a single colour pattern and participate in a single mimetic community (i.e. mimicry ring) at any given locality. However, some, like the Amazonian butterfly Heliconius numata, are polymorphic and participate in several mimicry rings within the same locality. We tested whether the unexpected polymorphism of H. numata could be due to a weak defence against predators. Poorly defended species participating in a mimicry ring are subject to negative frequency dependent selection, because their presence weakens the protection provided by the shared signal. This could promote polymorphism and participation in multiple mimicry rings. Using wild caught great tits (Parus major), we compared the palatability of H. numata to one of its locally monomorphic co-mimics (Mechanitis polymnia) and to two other locally monomorphic Heliconius species (H. melpomene and H. erato). The tested birds strongly rejected the polymorphic species H. numata, as well as the two other Heliconius species. Unexpectedly, a significantly weaker rejection was found towards M. polymnia, which relies on different toxic compounds to Heliconius. Our study demonstrates that the origin of polymorphic mimicry in H. numata is unlikely to stem from low unpalatability and raises new questions on defence variation within mimetic communities.

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Acknowledgments

We thank Diego Llusia for his suggestions on the statistical analyses, Neil Rosser, John Endler, the associated editor and two anonymous reviewers for their helpful comments and suggestions. The authors thank SERFOR and the Peruvian Ministry of Agriculture for collecting permits (RESOLUCION DIRECTORAL No. 289-2014-MINAGRI-DGFFS-DGEFFS). This work was funded by a Labex BcDiv PhD grant to MA (ANR-10-LABX-0003-bcdiv), a young research grant from the French National Agency for Research, DOMEVOL (ANR-13-JSV7-0003-01) to VL and the Centre of Excellence in Biological Interactions at the University of Jyväskylä, Finland to JM.

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  1. Institut de Systématique, Evolution et Biodiversité UMR 7205 (CNRS-MNHN-EPHE-UPMC-Sorbonne université), Museum National d’Histoire Naturelle, 57, rue Cuvier, CP50, 75005, Paris, France

    Mónica Arias & Violaine Llaurens

  2. Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, University of Jyvaskyla, P.O. Box 35, 40014, Jyvaskyla, Finland

    Johanna Mappes

  3. UMR CNRS7179, CNRS-MNHN, MECADEV, 1 avenue du petit château, 91800, Brunoy, France

    Mónica Arias & Marc Théry

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  1. Mónica Arias
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Correspondence to Mónica Arias.

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Arias, M., Mappes, J., Théry, M. et al. Inter-species variation in unpalatability does not explain polymorphism in a mimetic species. Evol Ecol 30, 419–433 (2016). https://doi.org/10.1007/s10682-015-9815-2

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