Differential Mechanisms in Insect Immune Response: Terminal Investment in Low-Dose Infections

Innate immune defences exhibit variable effectiveness, a phenomenon not yet fully understood. Recent research indicates that organisms may employ fundamentally different mechanisms to combat low-dose topical infections common in nature than severe infections. Here, we show that insects respond to low-dose topical infections by triggering terminal investment. Using simple methods for topical inoculations, we find that exposing fruit flies, <i>Drosophila melanogaster</i>, to low or sexually transmitted doses of the indigenous fungus <i>Aspergillus austwickii</i> boosts egg-to-adult viability, thereby maintaining lifetime reproductive output. By varying infection doses, we describe a pattern of correlations between reproductive success and mortality rate consistent with the threshold model of terminal investment. Quantitative analysis of age-dependent reproductive and mortality patterns reveals a misunderstanding of fundamental assumptions in life history theory: theories of senescence inadequately explain life history trade-offs induced by infections. Residual Reproductive Value may not necessarily be the evolutionary rationale underlying terminal investment. Our study shows that terminal investment involves an immediate trade-off between egg-to-adult viability and survival post-infection, rather than being driven by age-dependent trade-offs. The plasticity of life history traits in response to low-dose infections constrains the evolution of immunity, maintaining negative phenotypic correlations. Using the Gal4/UAS RNAi candidate gene knockdown approach, we compare the life history consequences of a canonical innate immune gene,<i> Dorsal</i>-related immunity factor. This comparison confirms that immune gene-mediated antagonistic pleiotropy drives insects to shift from reproductive to survival mechanisms of protection, depending on the mode of infection. Furthermore, we characterise a novel terminal investment mechanism encoded by <i>Turandot</i> C gene, which helps females minimise the costs of defence against the entomopathogenic fungus <i>Metarhizium robertsii</i> by shifting reproductive output post-infection. Our findings highlight the need for more research on common infections in nature to inform important non-immunological defences in a broader ecological context.<br>