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


ABSTRACT: 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.

SUBMITTER: Lewis JJ 

PROVIDER: S-EPMC6883815 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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

Lewis James J JJ   Geltman Rachel C RC   Pollak Patrick C PC   Rondem Kathleen E KE   Van Belleghem Steven M SM   Hubisz Melissa J MJ   Munn Paul R PR   Zhang Linlin L   Benson Caleb C   Mazo-Vargas Anyi A   Danko Charles G CG   Counterman Brian A BA   Papa Riccardo R   Reed Robert D RD  

Proceedings of the National Academy of Sciences of the United States of America 20191111 48


Color pattern mimicry in <i>Heliconius</i> 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 <  ...[more]

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