Abstract
In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex, has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knockouts in multiple Heliconius species and show that cortex is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified cis-regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the H. melpomene/timareta lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that cis-regulatory structural variation underlies these mimetic adaptations. Our work shows that cortex functionally controls scale colour fate and that its cis-regulatory regions control a phenotypic switch in a modular and pattern-specific fashion.
Highlights
Wing pattern diversity provides a window into the ways genetic changes underlie phenotypic variation that is spatially limited to specific parts or regions of the organism (McMillan et al, 2020; Orteu and Jiggins, 2020; Rebeiz et al, 2015)
To identify genes associated with the yellow bar phenotype, we performed differential gene expression (DGE) analysis using developing hindwings sampled from colour pattern morphs in H. erato and H. melpomene differing only in the presence or absence of the hindwing yellow bar (Figures 1b and 2a)
One proposed facilitator of such hotspots is through the action of genes acting as ‘input-output’ modules, whereby complex spatio-temporal information is translated into a co-ordinated cell differentiation program, in a simple switch-like manner
Summary
Wing pattern diversity provides a window into the ways genetic changes underlie phenotypic variation that is spatially limited to specific parts or regions of the organism (McMillan et al, 2020; Orteu and Jiggins, 2020; Rebeiz et al, 2015). Many of the underlying genetic loci controlling differences in colour patterns have been mapped to homologus ‘hotspots’ across disparate taxa. In some cases, this repeated adaptation has occurred through the alteration of downstream effector genes, such as pigment biosynthetic enzymes with functions clearly related to the trait under selection, for example, the genes tan and ebony that control insect melanin pigmentation (reviewed in Massey and Wittkopp, 2016).
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