Adaptation of pre-existing developmental mechanisms during the morphological evolution of an organ

Abstract

Organs tend to be remarkably homogeneous among individuals of the same species due to the robust mechanisms controlling organogenesis. In contrast, shape differences can be frequently observed when comparing organs among related species, reflecting the adaptation to life in diverse environments. Although such differences imply that the selective pressure can modify the mechanisms controlling organogenesis, we know little about how developmental modifications drive organ evolution. Here we study the genetic and developmental mechanisms controlling the formation of the posterior spiracles, the external respiratory organ of the larva, whose shape varies among diptera. We find that the protruding shape of the Drosophila posterior spiracle was acquired by the independent recruitment to the spiracle gene-network of two main developmental transcription factor regulators, the spalt and engrailed genes, through the evolution of organ specific enhancers. Engrailed recruitment to the anterior compartment cells resulted in spiracle elongation by the specific redeployment of cell behaviours normally used for embryonic dorsal closure. Comparative analysis of the genes required for spiracle formation in three diptera species shows a morphological correlation between organ shape and En anterior recruitment. Our work provides an example of how natural selection may control organ evolution by selecting novel cis-regulatory elements that recruit key transcription factors to a previously existing organogenetic gene-network redeploying pre-existing cellular behaviours into new functions.