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Abstract

Many aquatic animals regulate their position in the water column by controlling their buoyancy. This requires body compartments of regulated volume filled with matter that is less dense than water. However, only one group of insects has achieved this: the aquatic larvae of the midge genus Chaoborus (Diptera), which can alter the volume of four internal air-filled sacs. This thesis reveals the unique mechanochemical system underlying air-sac function, including how it is regulated, its mechanical properties, how it converts changes in pH into mechanical work, and how it has evolved to function at depth. The air-sac wall was found to contain resilin, an insect protein that swells reversibly in response to increases in pH, causing the fusiform air-sacs to expand lengthwise while maintaining a constant radius. Pharmacological investigation demonstrated that the air-sac wall is acidified by proton pumps (VHA) in a surrounding epithelium, shrinking it, while cAMP-signalling mediates alkalinisation and expansion. Finally, disrupting the air-sac epithelium in vivo revealed that the hemolymph has a pH of 7.4 while the air-sacs, without stimulation, are maintained near pH 6, providing the pH range for air-sac operation. Exposing air-sacs to hydrostatic pressure ramps revealed that those of deeper diving species and older instars could withstand more pressure before failure. Transmission electron microscopy showed that deep diving C. edulis had thicker air-sac walls relative to their radius, compared with two shallow diving species. There was no relationship between failure pressure and air-sac radius within species. In air-sacs, resilin imparts compressibility. The deepest diving species, C. edulis, possessed less resilin per length of wall, while deeper diving species, more generally, possessed stiffer air-sacs. Production of mechanical work by air-sac resilin was quantified by manipulating both pH and pressure. Dive depth correlated with work production: air-sacs of the deepest diving species, C. edulis, produced over 10-fold more work than the shallowest. With less resilin lengthwise, the greater work output by air-sacs of C. edulis must be due to differences in resilin composition. This thesis shows that Chaoborus species have adapted the pressure-tolerance and work capacity of their air-sacs to the depth of their aquatic environment.