Developmental heat stress interrupts spermatogenesis inducing early male sterility in Drosophila melanogaster

Thermal stress leads to fertility reduction, can cause temporal sterility and thus results in fitness loss with severe ecological and evolutionary consequences, e.g., threatening species persistence already at sub-lethal temperatures. For males we here tested which developmental stage is particularly sensitive to heat stress in the model species Drosophila melanogaster. As developmental stages characterize the different steps of sperm development, we could narrow down which particular processes are heat sensitive. We studied early male reproductive ability and, by following recovery dynamics after a move to benign temperatures, we investigated the mechanisms behind a subsequent gain of fertility. We found strong support to suggest that the last steps of spermatogenesis are particularly sensitive to heat stress, as processes occurring during the pupal stage were mostly interrupted, delaying both sperm production and sperm maturation. Moreover, further measurements in the testes and for proxies of sperm availability indicating the onset of adult reproductive capacity matched the expected heat-induced delay in completing spermatogenesis.  We discuss these results within the context of how heat stress affects reproductive organ function and the consequences for male reproductive potential.

Methods
We exposed Drosophila males to different stressful temperatures throughout development with the opportunity to recover as adults or not. We measured several sperm-related traits like availability of mature sperm to infer causes of fertility loss and sterility. We also allowed individuals to start recovery at different time points during development, from the egg to the pupariation phase and hence, identified the stages most vulnerable to heat stress. All developmental stages from the fertilization of an egg representing the development of the testes until the production and maturation of sperm were considered.