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Open Access Research

Co-option of a coordinate system defined by the EGFr and Dpp pathways in the evolution of a morphological novelty

Barbara MI Vreede1*, Jeremy A Lynch34, Siegfried Roth3 and Élio Sucena12*

Author Affiliations

1 Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, Oeiras, Portugal

2 Departamento da Biologia Animal, Universidade de Lisboa, Faculdade de Ciências, Lisbon, Portugal

3 Institute for Developmental Biology, Biocenter, University of Cologne, Zülpicher Strasse 47b, Cologne, Germany

4 Present address: Dept. of Biological Sciences, University of Illinois at Chicago, 900 S. Ashland Avenue, Chicago, IL, USA

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EvoDevo 2013, 4:7  doi:10.1186/2041-9139-4-7

Published: 1 March 2013

Abstract

Background

Morphological innovation is an elusive and fascinating concept in evolutionary biology. A novel structure may open up an array of possibilities for adaptation, and thus is fundamental to the evolution of complex multicellular life. We use the respiratory appendages on the dorsal-anterior side of the Drosophila eggshell as a model system for morphological novelty. To study the co-option of genetic pathways in the evolution of this novelty we have compared oogenesis and eggshell patterning in Drosophila melanogaster with Ceratitis capitata, a dipteran whose eggs do not bear dorsal appendages.

Results

During the final stages of oogenesis, the appendages are formed by specific groups of cells in the follicular epithelium of the egg chamber. These cells are defined via signaling activity of the Dpp and EGFr pathways, and we find that both pathways are active in C. capitata oogenesis. The transcription factor gene mirror is expressed downstream of EGFr activation in a dorsolateral domain in the D. melanogaster egg chamber, but could not be detected during C. capitata oogenesis. In D. melanogaster, mirror regulates the expression of two important genes: broad, which defines the appendage primordia, and pipe, involved in embryonic dorsoventral polarity. In C. capitata, broad remains expressed ubiquitously throughout the follicular epithelium, and is not restricted to the appendage primordia. Interestingly pipe expression did not differ between the two species.

Conclusions

Our analysis identifies both broad and mirror as important nodes that have been redeployed in the Drosophila egg chamber patterning network in the evolution of a morphologically novel feature. Further, our results show how pre-existing signals can provide an epithelium with a spatial coordinate system, which can be co-opted for novel patterns.

Keywords:
Evolutionary novelty; Drosophila melanogaster; Ceratitis capitata; Oogenesis; Pattern formation; Dorsal appendages; Genetic network