Butterfly wing patterns are key adaptations that are controlled by remarkable developmental and genetic mechanisms that facilitate rapid evolutionary change. With swift advancements in the fields of genomics and genetic manipulations, identifying the regulators of wing development and mimetic wing patterns has become feasible even in nonmodel organisms such as butterflies. Recent mapping and gene expression studies have identified single switch loci of major effects such as transcription factors and supergenes as the main drivers of adaptive evolution of mimetic and polymorphic butterfly wing patterns. We highlight several of these examples, with emphasis on doublesex, optix, WntA and other dynamic, yet essential, master regulators that control critical color variation and sex-specific traits. Co-option emerges as a predominant theme, where typically embryonic and other early-stage developmental genes and networks have been rewired to regulate polymorphic and sex-limited mimetic wing patterns in iconic butterfly adaptations. Drawing comparisons from our knowledge of wing development in Drosophila, we illustrate the functional space of genes that have been recruited to regulate butterfly wing patterns. We also propose a developmental pathway that potentially results in dorsoventral mismatch in butterfly wing patterns. Such dorsoventrally mismatched color patterns modulate signal components of butterfly wings that are used in intra-and inter-specific communication. Recent advances-fuelled by RNAi-mediated knockdowns and CRISPR/Cas9-based genomic edits-in the developmental genetics of butterfly wing patterns, and the underlying biological diversity and complexity of wing coloration, are pushing butterflies as an emerging model system in ecological genetics and evolutionary developmental biology. © 2017 Wiley Periodicals, Inc. How to cite this article:WIREs Dev Biol 2018, 7:e291. doi: 10.1002/wdev.291 MIMICRY IN BUTTERFLIES: A SINGULAR ADAPTATIONF ew adaptations in nature are as striking and widely appreciated as bright, diverse wing color patterns of butterflies. These color patterns have evolved to serve diverse and crucial functions in sexual selection, predator avoidance, and thermoregulation. Of these, aposematism and mimicry 1,2 (Box 1) are phylogenetically widespread and exhibit considerable diversification with respect to polymorphism 3 and sex-limitation 4,5 (Figure 1), whereby one or both sexes may have morphological variants that are strongly regulated by allelic variants. 7,8 This morphological diversity reflects diverse ecological regimes, intense selection pressures and molecular mechanisms that have shaped the evolutionary and genomic histories of butterflies. Density-and frequency-dependent Such rich biological detail and the diversity of butterfly wing color patterns themselves provide some unusual advantages as study systems in evolutionary biology and developmental genetics. Butterflies are at a golden point where, like birds, they are large and conspicuous enough to follow in the field to underst...

Pigmentation is involved in a wide array of biological functions across insect orders, including body patterning, thermoregulation, and immunity. The melanin pathway, in particular, has been characterized in several species. However, molecular evolution of the genes involved in this pathway is poorly explored. We traced the molecular evolution of six melanin pathway genes in 53 species of Lepidoptera covering butterflies and moths, and representing over 100 million years of diversification. We compared the rates of synonymous and non-synonymous substitutions within and between these genes to study the signatures of selection at the level of individual sites, genes, and branches of the gene tree. We found that molecular evolution of all six genes was governed by strong purifying selection. Yet, a number of sites showed signs of being under positive selection, including in the highly conserved domain regions of three genes. Further, we traced the expression of these genes across developmental stages, tissues, and sexes in the Papilio polytes butterfly using a developmental transcriptome dataset. We observed that the expression patterns of the genes in P. polytes largely reflected their known tissue-specific function in other species. The expression of sequentially acting genes in the melanin pathway was correlated. Interestingly, melanin pathway genes also showed a sexually dimorphic pattern of developmental heterochrony, i.e., females showed prominent upregulation of melanin pathway genes in pre-pupal stage compared to males, while males showed prominent upregulation in 9-day pupal wings compared to females. Our evolutionary and developmental analyses suggest that the vast diversity of wing patterning and pigmentation in Lepidoptera may have evolved despite largely constrained sequence evolution, with potential contribution from differential developmental expression of genes in a highly conserved pathway.

Gene duplication is a vital process for evolutionary innovation. Functional diversification of duplicated genes is best explored in multicopy gene families such as histones, hemoglobin, and opsins. Rhodopsins are photo-sensitive proteins that respond to different wavelengths of light and contribute to diverse visual adaptations across insects. While there are several instances of gene duplications in opsin lineages, the functional diversification of duplicated copies and their ecological significance is properly characterised only in a few insect groups. We examined molecular and structural evolution that underlies diversification and sub-functionalisation of four opsin genes and their duplicated copies across 132 species of the diverse insect order-Lepidoptera. Opsins have largely evolved under purifying selection with few residues showing signs of episodic and pervasive diversifying selection. Although these do not affect overall protein structures of opsins, substitutions in key amino acids in the chromophore-binding pocket of duplicated copies might cause spectral sensitivity shifts leading to sub-functionalisation or neofunctionalisation. Duplicated copies of opsins also exhibit developmental stage-specific expression in Papilio polytes, suggesting functional partitioning during development. Together, altered spectral sensitivities owing to key substitutions and differential expression of duplicated copies across developmental stages might enable enhanced colour perception and improved discrimination across wavelengths in this highly visual insect group.