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. © 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...

Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex

“…Our analysis of nucleotide sequence and protein structure of dsx revealed modular molecular evolution in its gene organization. Although evolution of new functions in many conserved genes is associated with evolution of noncoding regulatory regions ( 4 , 5 ), we found strong signatures of purifying as well as positive evolution within coding regions of dsx . We propose that structural and functional partitioning, as evident in dsx coding sequence, may explain contrasting functions of dsx in producing critical adaptations that are, in parts, sex-limited, polymorphic, developmentally conserved, and rapidly evolving even across closely related species.…”

“…It is increasingly recognized that the genetics of adaptation can take myriad forms, where complex genetic architecture, sequence evolution, and developmental regulation may strongly influence the tempo and mode of adaptation. On the basis of recent discoveries, it appears that several pleiotropic genes accommodate diverse functions that should be under contrasting selection pressures ( 5 ). We addressed this problem with a key developmental gene, dsx , that performs both conserved early developmental and highly divergent late developmental functions ( 11 – 18 , 22 , 29 ).…”

“…How do these highly conserved master regulators also facilitate rapidly evolving ecological adaptations that are often divergent in sister species? Some of these adaptations evolve as a consequence of co-option of gene regulatory networks and spatial or temporal modulation of expression ( 4 , 5 ). However, evolution of sequences and structures of transcription factors themselves are increasingly shown to regulate divergent phenotypic variation and adaptations ( 1 , 6 , 7 ).…”

The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterflyElymnias hypermnestra

“…Single genes of large effect are often found to be responsible for striking examples of adaptive variation [1,2]. Thus, much morphological diversity is derived from genetic variation at a relatively small number of genetic loci [3][4][5][6]. Mimetic butterflies are models for studying the relationship between exceptional phenotypic diversity resulting from limited genetic diversity for a number of reasons, including the manifest adaptive value of mimetic phenotypes, the fecundity and ease of rearing butterflies, and the incredible morphological diversity of butterflies [7,8].…”

Molecular evolution and developmental expression of melanin pathway genes in Lepidoptera

“…In several cases, emergence of sexual dimorphism and polymorphism is also linked to the evolution and differential expression of pigmentation genes (Wittkopp et al, 2009; Miyazaki et al, 2014; Yassin et al, 2016). Among Lepidoptera, wing coloration and patterning are remarkably diverse, which have shaped several adaptations such as aposematism, crypsis, mimicry, and thermoregulation (True, 2003; Hegna et al, 2013; Olofsson et al, 2013; Kronforst and Papa, 2015; Nadeau, 2016; Deshmukh et al, 2018; van’t Hof et al, 2019). In insects, melanins, ommochromes, and pterins are three major biosynthesized pigments deposited in developing wing scales (Wittkopp and Beldade, 2009).…”