Perfect mimicry between Heliconius butterflies is constrained by genetics and development.

Steven M. Van Belleghem,Brian A. Counterman,Riccardo Papa,Heriberto Carbia Gutierrez,Paola A. Alicea Roman

doi:10.1098/rspb.2020.1267

Abstract

Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. Here, we first quantify wing colour pattern differences in the forewing region of 14 co-mimetic colour pattern morphs of the butterfly species Heliconius erato and Heliconius melpomene and measure the extent to which mimicking colour pattern morphs are not perfectly identical. Next, using gene-editing CRISPR/Cas9 KO experiments of the gene WntA, which has been mapped to colour pattern diversity in these butterflies, we explore the exact areas of the wings in which WntA affects colour pattern formation differently in H. erato and H. melpomene. We find that, while the relative size of the forewing pattern is generally nearly identical between co-mimics, the CRISPR/Cas9 KO results highlight divergent boundaries in the wing that prevent the co-mimics from achieving perfect mimicry. We suggest that this mismatch may be explained by divergence in the gene regulatory network that defines wing colour patterning in both species, thus constraining morphological evolution even between closely related species.

Highlights

Adaptation is the product of natural selection on the genetic and phenotypic diversity within a population [1]
We used Heliconius butterflies to investigate the interplay of selection and genetics and provide a tentative explanation on the causes that limit perfect wing mimicry after several million years of strong natural selection towards a mutual anti-predatory signal
We propose that phenotypic 8 patterns of adaptation and convergence between Heliconius co-mimics is biased by divergence in the gene regulatory network underlying the mimicry trait

Summary

Introduction

Adaptation is the product of natural selection on the genetic and phenotypic diversity within a population [1]. In the butterfly Bicyclus anynana, artificial selection has suggested that there is great potential for independent change in size and shape of different eyespots [9] This observation has been used to argue that natural selection plays a dominant role over developmental constraints in the observed eyespot diversity among Bicyclus species [9]. In Drosophila, artificial selection experiments have shown that changes to wing shape can be rapidly induced from standing genetic variation present in the populations [10] These induced phenotypes are lost when selection is suspended, presumably due to pleiotropic links to other traits that result in negative fitness consequences [11]

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