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Mazo-Vargas, Anyi; Langmüller, Anna M.; Wilder, Alexis; van der Burg, Karin R. L.; Lewis, James J.; Messer, Philipp W.; Zhang, Linlin; Martin, Arnaud; Reed, Robert D.
Science (American Association for the Advancement of Science), 10/2022, Volume: 378, Issue: 6617Journal Article
Butterfly wing patterns derive from a deeply conserved developmental ground plan yet are diverse and evolve rapidly. It is poorly understood how gene regulatory architectures can accommodate both deep homology and adaptive change. To address this, we characterized the cis-regulatory evolution of the color pattern gene WntA in nymphalid butterflies. Comparative assay for transposase-accessible chromatin using sequencing (ATAC-seq) and in vivo deletions spanning 46 cis-regulatory elements across five species revealed deep homology of ground plan–determining sequences, except in monarch butterflies. Furthermore, noncoding deletions displayed both positive and negative regulatory effects that were often broad in nature. Our results provide little support for models predicting rapid enhancer turnover and suggest that deeply ancestral, multifunctional noncoding elements can underlie rapidly evolving trait systems. The butterfly’s grand ground plan In the 1920s, biologists proposed that butterfly wing pattern diversity evolved as variations of a ground plan of pattern elements that vary in color, shape, and position between different species. Mazo-Vargas et al . found that major aspects of this ground plan are determined by an ancient array of deeply conserved noncoding DNA sequences (see the Perspective by Espeland and Podsiadlowski). These regulatory sequences can have both positive and negative effects, and nuanced interactions between noncoding regions sculpt wing patterns. Deep homology of complex, rapidly evolving traits can thus be reflected in noncoding genomic sequences. —LMZ and DJ Ancient multifunctional regulatory elements underlie the evolution of butterfly wing color patterns.
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