Termite queen physogastry and associated mechanisms shaping a high lifetime fecundity

Abstract

Termites are eusocial insects whose colonies are usually headed by a pair of reproductives (queen and king). During its lifespan, the royal couple faces an age-dependent increase in fecundity. In queens, it reflects on the disproportional development of the ovaries and enlargement of the abdominal cuticle, a phenomenon referred to as physogastry. Beyond the impact on the ovaries and egg production, physogastry requires the morphological and physiological reprogramming of other systems such as the digestive, tracheal, muscular, and circulatory, resulting in a process that takes years to happen. Given the sampling difficulty and the absence of physogastric queens in some model species, such a topic is overlooked, and a comprehensive review has not been provided to date. Here we aim to review the process of physogastry in termite queens, from the pioneer studies on the morphological changes accompanying this process to recent advances in the molecular mechanisms underlying fecundity and the remarkable longevity reached by mature queens (e.g., TI-J-LiFe framework). Intrinsic and extrinsic factors driving this phenomenon, its impact on colony growth, and the current knowledge gaps are also discussed. We expect that our approach paves the way for further studies of termite physogastry, especially given the advances of molecular tools and recent termite phylogenies, and comparative analyses with other eusocial insects and the mechanisms driving this phenomenon in the different groups. Physogastry is a rare process in adult insects and remarkable in termite queens, offering a unique opportunity to unravel the basis of a highly fecund life.