The development of the piercing mouth during the last molt of the diseases-transmitting aphids and mosquitoes as revealed by synchrotron X-ray microtomography

Abstract

Piercing-sucking insects are extremely efficient vectors of animal and plant pathogens. This group is polyphyletic with the piercing organ highly heterogenous in its structure and morphogenesis, adapted to a specific host and feeding mechanism. For instance, hemimetabolous aphids feed on plant sap from nymphs to adults and they renew their stylets at each molt, thanks to specialized secreting glands. Distinctly, holometabolous mosquitoes have two feeding modes: larvae feed in water by filtering and scraping surfaces with their mouths, while female adults can acquire blood from vertebrate hosts. The pupal metamorphosis allows switching from one feeding habit to another. Here, we present a deep characterization of the biogenesis of the adult mouthparts in parthenogenetic females of the pea aphid Acyrthosiphon pisum (Harris 1776) (Hemiptera: Aphididae) and in females of the mosquito Aedes albopictus (Skuse 1895) (Diptera: Culicidae), investigated using non-invasive X-ray synchrotron-based microtomography. Comparing datasets collected from aphid juvenile and adult stages and from preimaginal and adult stages of the mosquito, we were able to track the morphological changes of secreting glands and the synthesis of the adult stylet in aphid heads and to follow the de novo formation of mosquito mouthparts in pupae. Our study provides a baseline for investigating the evolution and the development of piercing-sucking mouthparts and to better understand how morphogenesis works in insects.