Segmented organisms have serially repeated structures [1] that become specialized in some segments [2]. We show here that the Drosophila corpora allata, prothoracic glands, and trachea have a homologous origin and can convert into each other. The tracheal epithelial tubes develop from ten trunk placodes [3, 4], and homologous ectodermal cells in the maxilla and labium form the corpora allata and the prothoracic glands. The early endocrine and trachea gene networks are similar, with STAT and Hox genes inducing their activation. The initial invagination of the trachea and the endocrine primordia is identical, but activation of Snail in the glands induces an epithelial-mesenchymal transition (EMT), after which the corpora allata and prothoracic gland primordia coalesce and migrate dorsally, joining the corpora cardiaca to form the ring gland. We propose that the arthropod ectodermal endocrine glands and respiratory organs arose through an extreme process of divergent evolution from a metameric repeated structure.

Hox proteins belong to a family of transcription factors with similar DNA binding specificities that control animal differentiation along the antero-posterior body axis. Hox proteins are expressed in partially overlapping regions where each one is responsible for the formation of particular organs and structures through the regulation of specific direct downstream targets. Thus, explaining how each Hox protein can selectively control its direct targets from those of another Hox protein is fundamental to understand animal development. Here we analyse a cis regulatory module directly regulated by seven different Drosophila Hox proteins and uncover how different Hox class proteins differentially control its expression. We find that regulation by one or another Hox protein depends on the combination of three modes: Hox-cofactor dependent DNA-binding specificity; Hox-monomer binding sites; and interaction with positive and negative Hox-collaborator proteins. Additionally, we find that similar regulation can be achieved by Amphioxus orthologs, suggesting these three mechanisms are conserved from insects to chordates.

Many organs are specified far from the location they occupy when functional, having to migrate long distances through the heterogeneous and dynamic environment of the early embryo. We study the formation of the main Drosophila endocrine organ, the ring gland, as a new model to investigate in vivo the genetic regulation of collective cell migration. The ring gland results from the fusion of three independent gland primordia that migrate from the head towards the anterior aorta as the embryo is experiencing major morphogenetic movements. To complete their long-range migration, the glands extend filopodia moving sequentially towards a nearby intermediate target and from there to more distal ones. Thus, the apparent long-range migration is composed of several short-range migratory steps that facilitate reaching the final destination. We find that the target tissues react to the gland's proximity by sending filopodia towards it. Our finding of a succession of independent migration stages is consistent with the stepwise evolution of ring gland assembly and fits with the observed gland locations found in extant crustaceans, basal insects and flies.

During evolution, bilateral animals have experienced a progressive process of cephalization with the anterior concentration of nervous tissue, sensory organs and the appearance of dedicated feeding structures surrounding the mouth. Cephalization has been achieved by the specialization of the unsegmented anterior end of the body (the acron) and the sequential recruitment to the head of adjacent anterior segments. Here we review the key developmental contribution of Hox1–5 genes to the formation of cephalic structures in vertebrates and arthropods and discuss how this evolved. The appearance of Hox cephalic genes preceded the evolution of a highly specialized head in both groups, indicating that Hox gene involvement in the control of cephalic structures was acquired independently during the evolution of vertebrates and invertebrates to regulate the genes required for head innovation.