Divergent origin of the insect cephalic endoskeleton and the trachea from a homologous metameric structure.

Abstract

During animal evolution, organs adapt to perform new functions. In some cases, adaptive changes over large evolutionary distances can lead to divergence that obscures the organs' origin, as is observed in the highly specialized structures formed in the cephalic region. The genetic and cellular analysis of how metamerically repeated organs develop in segmented animals can help us understand the formation of such extremely divergent homologous organs. In this work, we use Drosophila melanogaster to study the origin of the tentorium, the conserved cephalic endoskeleton of insects. We find that the tentorium develops from three groups of cephalic cells specified on the lateral side of the intercalary, maxillary, and labial segments, at positions where the trunk segments form the tracheal primordia. Similar to the tracheae, the three tentorium primordia invaginate and coalesce to form a continuous epithelial tubular structure connected to the external epithelium. This tube serves as an apodeme to which the muscles moving the mouthparts bind. We find that the tentorium expresses and requires similar upstream genes as those required for tracheal specification. Moreover, genetic experiments show that the tentorium can be transformed into trachea, and that the trachea can express tentorial-specific markers, indicating that the two organs evolved from an ancient homologous metamerically repeated structure. Our results show that the tracheae arise from a homology group that in the cephalic segments gives rise to the tentorium, corpora allata, and prothoracic endocrine glands, highlighting the plasticity of homologous structures to diverge into extremely diverse morphological and functional organs.