Mimicry in butterflies: co-option and a bag of magnificent developmental genetic tricks

Abstract

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. WIREs Dev Biol 2018, 7:e291. doi: 10.1002/wdev.291 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms Comparative Development and Evolution > Regulation of Organ Diversity Comparative Development and Evolution > Evolutionary Novelties.