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

Abstract

One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis-regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

What Can We Learn About Adaptation from the Wing Pattern Genetics of Heliconius Butterflies?

“…I have reviewed our understanding of wing patterning based on genetic crossing experiments, but have not considered in detail the developmental basis for pattern diversity, which has recently been reviewed elsewhere (Jiggins et al 2017).…”

Perspectives on the history of evo-devo and the contemporary research landscape in the genomics era

“…Major morphological transitions and innovations are considered first with articles on the origins of animal multicellularity from a classical perspective by Cavalier-Smith [52] and illustrating the impact of genomics by Babonis & Martindale [20] and an article on the evolution of land plants by Harrison [53]; the major transition that created the unique mammalian middle ear is discussed by Tucker [46]. The next section focuses on diversification and modifications of morphology as exemplified by tetrapod limbs by Saxena et al [54], flowers by Pam Soltis and co-workers [55], cranial shape in birds by Abzhanov and co-workers [45] and wing coloration patterns in butterflies by Jiggins et al [56]. The last section considers the relatively recent evolution of genetically determined morphological variation within a single species owing to either natural selection, using as examples, cavefish (article by Krishnan & Rohner [57]) and stickleback (article by Piechel & Marques [58]) or artificial selection, using dogs as an example (article by Elaine Ostrander and co-workers [59]) and ends with the article on developmental plasticity by Xu & Zhang [49].…”

“…Several articles in the issue provide examples where the evolution of morphological diversity has been found to involve cis-regulatory regions. The stunning coloured patterns of the wings of the different species of Heliconius butterflies provide outstanding examples in which a gene is expressed in a new context and takes on a completely new function [56]. Striking examples of changes in cis-regulatory regions underlying morphological diversity are also found in natural populations of stickleback [58].…”

“…There are an increasing number of genome-wide analyses aiming to identify differences in gene expression in developing organs of different organisms, including, for example, comparisons between mouse, chimpanzee and human (reviewed in [66]). Interpretation of positional information may often involve fine-tuning morphogenesis and the spatial coordination of various cell activities such as movement, adhesiveness and proliferation to produce for example the specific shapes of the bird cranium [45] or the bones in vertebrate limb digits [54] or the scale structure in Heliconius butterflies [56]. At first sight, the dissection of how such complex processes are fine-tuned seems very daunting but recent work has shown that morphogenesis can proceed-apparently spontaneously-given the right conditions.…”

Camouflage Variations on a Theme of the Nymphalid Ground Plan

“…Are there possibilities that the NGP was broken? The wing pattern of a mimicry butterfly, Heliconius sp., might be considered (Jiggins et al 2017) a possible example of such a situation. Under this consideration, several questions are raised: How was the NGP deconstructed in Heliconius butterflies?…”