The Functional Basis of Wing Patterning inHeliconiusButterflies: The Molecules Behind Mimicry

Abstract

Wing-pattern mimicry in butterflies has provided an important example of adaptation since Charles Darwin and Alfred Russell Wallace proposed evolution by natural selection .150 years ago. The neotropical butterfly genus Heliconius played a central role in the development of mimicry theory and has since been studied extensively in the context of ecology and population biology, behavior, and mimicry genetics. Heliconius species are notable for their diverse color patterns, and previous crossing experiments revealed that much of this variation is controlled by a small number of large-effect, Mendelian switch loci. Recent comparative analyses have shown that the same switch loci control wing-pattern diversity throughout the genus, and a number of these have now been positionally cloned. Using a combination of comparative genetic mapping, association tests, and gene expression analyses, variation in red wing patterning throughout Heliconius has been traced back to the action of the transcription factor optix. Similarly, the signaling ligand WntA has been shown to control variation in melanin patterning across Heliconius and other butterflies. Our understanding of the molecular basis of Heliconius mimicry is now providing important insights into a variety of additional evolutionary phenomena, including the origin of supergenes, the interplay between constraint and evolvability, the genetic basis of convergence, the potential for introgression to facilitate adaptation, the mechanisms of hybrid speciation in animals, and the process of ecological speciation.

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

“…Butterflies of the Heliconius genus provide a rich phylogenetic template for such micro-evo-devo studies (Papa et al 2008;Supple et al 2014;Kronforst and Papa 2015;Merrill et al 2015). They display a range of highly variable wing color pattern phenotypes involved in Müllerian mimicry (the collaborative display of similar morphologies to predators from multiple unpalatable species) and sexual selection that are amenable to hybrid crosses followed by linkage mapping.…”

“…Importantly, this multiallelism probably acts as a prerequisite for the formation of complex alleles, as it is likely that adjacent regulatory regions evolve by recombination between blocks that exist as standing variation, rather than solely by cumulative de novo mutations on the same DNA molecule (Rebeiz et al 2011;Martin and Orgogozo 2013). A chimeric, polyallelic origin can explain the cis-regulatory evolution of optix (Wallbank et al 2015) (see also chapter by CD Jiggins in this volume), a transcription factor locus that, like WntA, shows extensive parallelism and multiallelism in the Heliconius genus (Reed et al 2011;Papa et al 2013;Kronforst and Papa 2015;Zhang et al 2016). We expect that further examples of phenotypic radiations will uncover a multiallelic basis, as recently proposed in cichlid fishes (Roberts et al 2016).…”

Genetic Basis of Melanin Pigmentation in Butterfly Wings

“…Third, in many species, pigments play important adaptive functions and show clear phylogenetic patterns of gain and loss, thus providing a link between developmental genetics and evolutionary biology. Finally, ongoing work by multiple research groups continues to define genes and regulatory networks involved in wing pattern evolution (Beldade and Brakefield 2002;Kronforst and Papa 2015;Monteiro 2015;Wallbank et al 2016), thus providing a foundation for work aimed at understanding the upstream processes that regulate pigmentation genes. In this study, we directly test the function of a suite of pigmentation genes in the painted lady butterfly, Vanessa cardui, the buckeye Junonia coenia, the squinting bush brown Bicyclus anynana, and the Asian swallowtail Papilio xuthus.…”

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

“…This largely involves evolutionary diversification in gene regulation, providing a promising system for dissecting the process of cis-regulatory evolution [11,12]. The patterns have arisen recently enough that it is feasible to identify the exact DNA changes that produce different patterns.…”