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Molecular mechanisms underpinning buoyancy control in the aquatic larvae of Chaoborus evolved from tracheal fluid clearing functionality

Matthews, Benjamin

Aquatic larvae belonging to the midge genus Chaoborus are the only truly pelagic insects, possessing the ability to regulate their buoyancy and position in the water column. They achieve this buoyancy control using two pairs of closed, air-filled sacs which are derived from the longitudinal trunks of their tracheal system. Previous work has revealed that the volume of these air-sacs is controlled using a unique mechanochemical system, where bands of the protein resilin alternate with bands of tracheal cuticle in the air-sac wall to produce a composite material which expands and contracts when exposed to changes in pH. While a simple epithelium enveloping each air-sac is known to control the pH of the resilin bands, the molecular mechanisms underpinning its ability to regulate pH, and thus control the air-sac’s volume, are unknown. To reveal these mechanisms, and how this functionality evolved, we compare the transcriptomes of air-sacs from Chaoborus trivitattus larvae with tracheal tissue from the aquatic larvae of two other genera within the Chaoboridae: Eucorethra underwoodi whose larvae possess an unmodified tracheal system which they use to breathe air using a posterior respiratory siphon, and Mochlonyx cinctipes whose larvae possess a tracheal system with dilated anterior and posterior sac-like regions, but which remains open through a posterior siphon. We found that Chaoborus air-sac epithelia show strong expression of ion channels related to pH regulation relative to Eucorethra tracheal tissue, including orthologs of NHA1, Nhe2, Ae2, and pHCl-2, as well as high levels of transcript abundance of the aquaporin water channel, Drip. This suggests that the tracheal epithelium of the ancestral chaoborid possesses all the functionality required to control pH and deal with the flux of water associated with the swelling and contraction of the resilin as part of the ancestral liquid-clearing function of the tracheal epithelium, setting the stage for the evolution of a novel buoyancy control mechanism.

Dataset

University of British Columbia Library

10.14288/1.0449210

https://doi.org/10.5683/SP2/E8YKXW

Dataverse