Terminal investment provides low-cost defence against low-dose infections

Animals can respond to exposure to lethal pathogenic microbes by enhancing either survival or reproduction. However, it is crucial to assess fitness costs across various infection loads to determine the conditions under which innate immune and terminal investment mechanisms are adaptive for infected hosts. In this study, we demonstrate that terminal investment serves as a low-cost defence mechanism against common low-dose infections. We find that topical exposure of female Drosophila melanogaster to low-dose or sexually transmitted infections (STIs) caused by the indigenous fungus Aspergillus austwickii increases egg-to-adult viability while decreasing survival rates. Notably, we find no evidence supporting impacts on future reproductive potential, which has long been assumed to drive terminal investment in foundational evolutionary theory. Instead, our results indicate that increases in reproduction occur concurrently with heightened mortality rates in the hosts. We identify Turandot C (TotC), a humoral stress response gene upregulated in females exposed to male courtship calls, as a key player in the fecundity compensation response in STI-exposed females. In contrast to the generally weak costs associated with TotC expression on lifetime reproductive success, we show that the expression of the canonical innate immune gene, Dorsal-related immunity factor, results in reproductively costly antagonistic pleiotropy in females exposed to STIs. These findings illustrate that the adaptive evolution of immunity is constrained not only by fitness trade-offs, but also because insects have evolved to capitulate when faced with common low-dose infections.