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

Lewis, James, Cornell University, https://orcid.org/0000-0002-4170-9118

Geltman, Rachel, Cornell University

Pollack, Patrick, Cornell University

Rondem, Kathleen, Cornell University

Van Belleghem, Steven, University of Puerto Rico at Río Piedras

Hubisz, Melissa, Cornell University

Munn, Paul, Cornell University

Zhang, Linlin, Cornell University

Benson, Caleb, Mississippi State University

Mazo-Vargas, Anyi, Cornell University, https://orcid.org/0000-0001-9644-2871

Danko, Charles, Cornell University

Counterman, Brian, Mississippi State University

Papa, Riccardo, University of Puerto Rico at Río Piedras

Reed, Robert, Cornell University

jjl336@cornell.edu

Published Nov 11, 2019 on Dryad. https://doi.org/10.5061/dryad.h9w0vt4db

Cite this dataset

Lewis, James et al. (2019). Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry [Dataset]. Dryad. https://doi.org/10.5061/dryad.h9w0vt4db

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.

Funding

Division of Environmental Biology, Award: DEB-1354318

Division of Environmental Biology, Award: DEB-1546049

Division of Integrative Organismal Systems, Award: IOS-1656514

Division of Integrative Organismal Systems, Award: IOS-1656389

National Science Foundation, Award: DGE-1650441

National Science Foundation, Award: OIA-1736026