Gas exchange in water and air: Revealing fundamental mechanisms underlying the development and control of the insect respiratory system

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Insects are the most numerous and diverse animals on the planet, representing 80% of all known species. Although they are an ancestrally air-breathing group, species from 11 orders have independently evolved the ability to live and breathe underwater as juveniles. This impressive respiratory flexibility underlies the global success of all insects, but fundamental details of how they breathe are still a mystery. The long-term goal of my research program is to reveal how insects sense and regulate their gas exchange in response to hypoxia, hypercapnia, and acid-base balance, and to understand how their gas-exchange system has evolved to function in a range of challenging respiratory environments. The research proposed here addresses two critical gaps in our understanding of insect respiratory physiology by determining 1) where and how insects sense internal levels of O2 and CO2, and 2) how they remove fluid from their tracheal system and replace it with air when they first hatch. My research program will harness the physiological traits of aquatic insects to uncover, for the first time, the mechanisms that underlie these vital processes. Aquatic dragonfly nymphs exhibit a clear ventilatory rhythm, allowing us to locate O2 and CO2-sensitive neurons by measuring the effect of focal stimulation on ventilation. The molecular mechanisms by which these neurons sense O2 or CO2 will then be revealed by chemical stimulation and inhibition. Developing terrestrial insects can pull air into their tracheal system through open spiracles as the tracheal fluid is drawn into their blood, but aquatic insects hatch underwater and possess a closed tracheal system. They must generate a bubble in their tracheal fluid by cavitation, and then expand its volume as the fluid is withdrawn. We aim to reveal how this occurs. Osmosis could drive cavitation and fluid removal, while CO2 production could support bubble expansion. Ion transport must underlie both processes, so using drugs to selectively inhibit ion pumps will show the transport pathways involved. Manipulating hydrostatic pressure to elicit or inhibit cavitation in developing insects will reveal the magnitude of the osmotic and gas pressures generated by the tracheal system. We will also explore the evolutionary plasticity of the insect respiratory system by studying a unique buoyancy control mechanism. Aquatic larvae of the genus Chaoborus have modified their tracheal system into a hydrostatic organ, comprising four air-filled sacs. We have discovered that the larvae do not pump gas into the sacs to regulate buoyancy. Instead they change the pH of bands of resilin protein in the sac wall, which expand and contract in response, thus changing the volume of the sac. Understanding this system will reveal how the ancestral tracheal machinery has been modified to produce this striking evolutionary innovation. All components of this program will rewrite our understanding of how the insect respiratory system functions.