Sense organ formation and identity are controlled by divergent mechanisms in insects

Abstract

Insects and other arthropods utilise external sensory structures for mechanosensory, olfactory and gustatory reception. These sense organs have characteristic shapes related to their function, and in many cases are distributed in a fixed pattern so that they are identifiable individually. In Drosophila melanogaster, the identity of sense organs is regulated by specific combinations of transcription factors. In other arthropods, however, sense organ subtypes cannot be linked to the same code of gene expression. This raises the questions of how sense organ diversity has evolved in arthropods, and if the D. melanogaster subtype identity principle is representative for insects. To address these questions, we analyse sense organ development in another insect, the flour beetle Tribolium castaneum. We show that in contrast to D. melanogaster, T. castaneum sense organs cannot be categorised based on their requirement for individual or combinations of the conserved sense organ transcription factors such as cut and pox-neuro and members of the Achaete-Scute (Tc ASH, Tc asense) and Atonal family (Tc atonal, Tc cato, Tc amos). Rather, these genes are required for the specification of sense organ precursors and the development and differentiation of sensory cell types in diverse external sensilla. Based on our findings and past research, we present an evolutionary scenario suggesting that sensory organs have diversified from a default state through subsequent recruitment of sensory genes to the different sense organ specification processes. A specific role for genes in subtype identity has evolved as a secondary effect of the function of these genes in individual or subsets of sense organs, which can largely not be aligned with morphological or functional categories.