From water-breathing nymphs to air-breathing adults: Insects as a model system to investigate the physiological challenges associated with the transition of life from water to land

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This Discovery Program will take the novel approach of using aquatic insects to examine the physiological challenges associated with the transition from breathing water to breathing air. Aquatic insects support valuable freshwater ecosystems and fisheries, but are highly susceptible to changes in water quality, so understanding their physiology is of crucial importance for successful environmental management. Our current understanding of the respiratory challenges associated with moving between water and air comes from studying how aquatic animals, particularly vertebrates, have adapted their morphology and physiology to function on land. From this perspective, water-breathing is the ancestral condition and air-breathing is a derived state. The insects, however, have performed this feat in reverse, adapting their terrestrial air-breathing physiology to function in water. Although all adult insects are air-breathers, representatives of nine insect orders have evolved to be developmentally amphibious, spending the juvenile proportion of their life cycle as aquatic nymphs or larvae that possess gills and breathe water. These insect groups provide an exceptional opportunity to examine the evolution of adaptations associated with aquatic respiration, and to determine whether environmental constraints have caused gill-bearing insects to converge on a respiratory physiology comparable to other aquatic animals, or whether the phylogenetic constraints of their terrestrial ancestry have resulted in a respiratory physiology similar to air-breathing animals. The physiological consequences of the insects’ return to water are not well understood, but there is tantalizing evidence that water-breathing nymphs possess elevated internal CO2 levels commonly associated with breathing air, an observation that cannot be explained by current textbook dogma. Furthermore, we know nothing of the mechanisms and physiological shifts that enable these insects, during metamorphosis, to change rapidly from breathing with gills to using an air-filled respiratory system. My research program aims to identify and compare the respiratory and acid-base strategies used by water-breathing juvenile insects with those of the air-breathing adults, and to explore the physiological changes that occur during their rapid transition from water to land. I will use a range of techniques, including respirometry, morphometry and histology, to reveal the different strategies used by the aquatic and terrestrial life stages to regulate their internal oxygen and carbon dioxide levels, and their acid-base balance. Thus, this research program addresses a fundamental gap in our understanding of insect physiology and provides insight into the evolution of respiratory adaptations underlying the transition from water to land.