The predicted temperature increase caused by climate change is a threat to biodiversity. Across animal taxa, male reproduction is often sensitive to elevated temperatures leading to fertility loss and in more adverse scenarios, this can result in sterility when males reach their upper thermal fertility limit. Here we investigate temperature-induced changes in reproductive tissues, fertility reduction, sterility, and the associated fitness loss during the subsequent recovery phase in male Drosophila melanogaster. We heat-stressed males during development and either allowed them to recover or not in early adulthood, while measuring several determinants of male reproductive success. We found significant differences in recovery rate, organ sizes, sperm production, and other key reproductive traits among males from our different temperature treatments. Sperm maturation was impaired before reaching the upper thermal sterility threshold. While some effects were reversible, this did not compensate for the fitness loss due to damage imposed during development. Surprisingly, developmental heat stress was damaging to accessory gland growth, and female post-mating responses mediated by seminal fluid proteins were impaired regardless of the possibility of recovery. We suggest that sub-lethal thermal sterility and the subsequent fertility reduction is caused by a combination of inefficient functionality of both the accessory gland and testes.

We add to the novel and rapidly increasing field conduction investigations into the consequences of elevated temperature on reproductive performance in insects. We used the model Drosophila melanogaster for a comprehensive study and measured multiple determinants of male reproductive success to understand the impact of elevated temperatures on the functionality of both reproductive tissues: the testis and the accessory gland.