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

Barbara Mi Vreede,Jeremy A Lynch,Élio Sucena,Siegfried Roth

doi:10.1186/2041-9139-4-7

Abstract

BackgroundMorphological 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.ResultsDuring 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.ConclusionsOur 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.

Highlights

Morphological innovation is an elusive and fascinating concept in evolutionary biology
C. capitata oogenesis is a suitable system for comparison The C. capitata eggshell carries no structures that can be identified as homologues of the operculum, outward micropyle and dorsal appendages (Figure 1B)
From an initial observation of C. capitata oogenesis we can conclude first and foremost that it is a suitable system for comparison with D. melanogaster

Summary

Introduction

Morphological innovation is an elusive and fascinating concept in evolutionary biology. The concept of evolutionary novelty is that of a new trait, usually an anatomical or morphological one, that opens up the possibility of a wide adaptive radiation into new niches [1] This definition places an emphasis on adaptation and is illustrative of the central role novel traits may have on shaping life on earth. One of the most important contributions of evo-devo to our understanding of the evolutionary process has been the refinement and experimental validation of the gene recruitment concept (cooption) These are key innovations at the genetic level that may underlie differences in cellular growth and morphogenetic processes between related organisms, which have diverged morphologically [8]. In recent years many examples have demonstrated that evolution largely relies on recycling old genes and pathways to generate novel patterns and morphologies [9,10]

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