A recurrent regulatory change underlying altered expression and Wnt response of the stickleback armor plates gene EDA

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Abstract

Armor plate changes in sticklebacks are a classic example of repeated adaptive evolution. Previous studies identified ectodysplasin (EDA) gene as the major locus controlling recurrent plate loss in freshwater fish, though the causative DNA alterations were not known. Here we show that freshwater EDA alleles have cis-acting regulatory changes that reduce expression in developing plates and spines. An identical T->G base pair change is found in EDA enhancers of divergent low-plated fish. Recreation of the T->G change in a marine enhancer strongly reduces expression in posterior armor plates. Bead implantation and cell culture experiments show that Wnt signaling strongly activates the marine EDA enhancer, and the freshwater T->G change reduces Wnt responsiveness. Thus parallel evolution of low-plated sticklebacks has occurred through a shared DNA regulatory change, which reduces the sensitivity of an EDA enhancer to Wnt signaling, and alters expression in developing armor plates while preserving expression in other tissues.

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Natasha M O'Brown

Department of Developmental Biology, Stanford University School of Medicine, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Brian R Summers

General Practice Dentistry, Albany, United States

Competing interests
The authors declare that no competing interests exist.
Felicity C Jones

Friedrich Miescher Laboratory, Max Planck Institute for Developmental Biology, Tuebingen, Germany

Competing interests
The authors declare that no competing interests exist.
Shannon D Brady

Department of Developmental Biology, Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
David M Kingsley

Department of Developmental Biology, Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, United States

For correspondence
kingsley@stanford.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#13834) of Stanford University, in animal facilities accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC).

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.