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

by Zhang, Linlin , Pollak, Patrick C. , Reed, Robert D. , Munn, Paul R. , Papa, Riccardo , Benson, Caleb , Mazo-Vargas, Anyi , Counterman, Brian A. , Hubisz, Melissa J. , Lewis, James J. , Danko, Charles G. , Rondem, Kathleen E. , Van Belleghem, Steven M. , Geltman, Rachel C.

in Adaptation, Physiological - genetics / Adaptive radiation / Animals / Biological Sciences / Butterflies & moths / Butterflies - physiology / Chimera / Chromatin / Coevolution / Color / CRISPR-Cas Systems / Deoxyribonucleic acid / DNA / Enhancer Elements, Genetic / Enhancers / Evolution / Evolution, Molecular / Fragility / Genetic Pleiotropy / Genome, Insect / Genome-Wide Association Study / Genomes / Heliconius / Insect Proteins - genetics / Mimicry / Nucleotide sequence / Patterning / Phylogeny / Pigmentation - genetics / Pigmentation - physiology / Pleiotropy / PNAS Plus / Promoter Regions, Genetic / Regulatory sequences / Regulatory Sequences, Nucleic Acid / Wings, Animal - physiology

2019

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

2019

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

2019

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Journal Article

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

Zhang, Linlin,

Pollak, Patrick C.,

Reed, Robert D.,

Munn, Paul R.,

Papa, Riccardo,

Benson, Caleb,

Mazo-Vargas, Anyi,

Counterman, Brian A.,

Hubisz, Melissa J.,

Lewis, James J.,

Danko, Charles G.,

Rondem, Kathleen E.,

Van Belleghem, Steven M.,

Geltman, Rachel C.

2019

Overview

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.

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Publisher

National Academy of Sciences

Subject

Adaptation, Physiological - genetics

/ Adaptive radiation

/ Animals

/ Biological Sciences

/ Butterflies & moths

/ Butterflies - physiology

/ Chimera