Gene

Heliconius

Exaptation

Neuroscience

Coevolution

Biology

Enhancer

Selection (genetic algorithm)

Computer science

Gene regulatory network

Evolutionary biology

Genetics

Phylogenetics

Transcription factor

Artificial intelligence

Genetic architecture

Convergent evolution

Mimicry

Zoology

Quantitative trait locus

Gene expression

Natural selection

Adaptation (eye)

Pleiotropy

Phenotype

Proceedings of the National Academy of Sciences

Color pattern mimicry in Heliconius butterflies is a classic case study of complex trait adaptation via selection on a few large effect genes. Association studies have linked color pattern variation to a handful of noncoding regions, yet the presumptive cis-regulatory elements (CREs) that control color patterning remain unknown. Here we combine chromatin assays, DNA sequence associations, and genome editing to functionally characterize 5 cis-regulatory elements of the color pattern gene optix . We were surprised to find that the cis-regulatory architecture of optix is characterized by pleiotropy and regulatory fragility, where deletion of individual cis-regulatory elements has broad effects on both color pattern and wing vein development. Remarkably, we found orthologous cis-regulatory elements associate with wing pattern convergence of distantly related comimics, suggesting that parallel coevolution of ancestral elements facilitated pattern mimicry. Our results support a model of color pattern evolution in Heliconius where changes to ancient, multifunctional cis-regulatory elements underlie adaptive radiation.

Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry