Abstract

Developmental processes have to be robust but also flexible enough to respond to genetic and environmental variations. Different mechanisms have been described to explain the apparent antagonistic nature of developmental robustness and plasticity. Here, we present a “self-sufficient” molecular model to explain the development of a particular flight organ that is under the control of the Hox gene Ultrabithorax (Ubx) in the fruit fly Drosophila melanogaster. Our model is based on a candidate RNAi screen and additional genetic analyses that all converge to an autonomous and cofactor-independent mode of action for Ubx. We postulate that this self-sufficient molecular mechanism is possible due to an unusually high expression level of the Hox protein. We propose that high dosage could constitute a so far poorly investigated molecular strategy for allowing Hox proteins to both innovate and stabilize new forms during evolution.

Highlights

  • Hox genes are well-known master developmental regulators that have extensively been exploited for diversifying animal body forms during evolution (Pearson et al, 2005; Pick and Heffer, 2012)

  • Insects display an astonishing level of morphological diversity, as exemplified in their flight appendages, which differ from one order to the other

  • (Irvine et al, 1993), and recent (Delker et al, 2019) work showed that a negative autoregulatory loop contributes to the stabilization of distinct Ubx expression levels along the proximal-distal axis within the haltere imaginal disc of Drosophila melanogaster

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Summary

Introduction

Hox genes are well-known master developmental regulators that have extensively been exploited for diversifying animal body forms during evolution (Pearson et al, 2005; Pick and Heffer, 2012). Morphological innovations can result from changes in the Hox protein sequence itself, as described for abdominal leg repression in arthropods (Galant and Carroll, 2002; Ronshaugen et al, 2002; Pearson et al, 2005; Saadaoui et al, 2011). Insects display an astonishing level of morphological diversity, as exemplified in their flight appendages, which differ from one order to the other. Ancestral insects had two pairs of wings on their second (T2, forewing) and third (T3, hindwing) thoracic segments (Carroll et al, 1995), most often of identical or highly similar morphology, as observed in damselflies and dragonflies (Odonata order).

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