Functional evolution of a morphogenetic gradient

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Abstract

Bone Morphogenetic Proteins (BMPs) pattern the dorsal-ventral axis of bilaterian embryos; however, their roles in the evolution of body plan are largely unknown. We examined their functional evolution in fly embryos. BMP signaling specifies two extraembryonic tissues, the serosa and amnion, in basal-branching flies such as Megaselia abdita, but only one, the amnioserosa, in Drosophila melanogaster. The BMP signaling dynamics are similar in both species until the beginning of gastrulation, when BMP signaling broadens and intensifies at the edge of the germ rudiment in Megaselia, while remaining static in Drosophila. Here we show that the differences in gradient dynamics and tissue specification result from evolutionary changes in the gene regulatory network that controls the activity of a positive feedback circuit on BMP signaling, involving the tumor necrosis factor alpha homolog eiger. These data illustrate an evolutionary mechanism by which spatiotemporal changes in morphogen gradients can guide tissue complexity.

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Chun Wai Kwan

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, United States

Competing interests
The authors declare that no competing interests exist.
Jackie Gavin-Smyth

Department of Ecology and Evolution, University of Chicago, Chicago, United States

Competing interests
The authors declare that no competing interests exist.
Edwin L Ferguson

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, United States

Competing interests
The authors declare that no competing interests exist.
Urs Schmidt-Ott

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, United States

For correspondence
uschmid@uchicago.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1351-9472

Funding

National Science Foundation (IOS-1121211)

Urs Schmidt-Ott

University of Chicago (Hinds Fund graduate student award)

Chun Wai Kwan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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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.