Still standing: The heat protection delivered by a facultative symbiont to its aphid host is resilient to repeated thermal stress

Insects have evolved diverse strategies to resist extreme high temperatures (EHT). The adaptive value of such strategies has to be evaluated when organisms experience multiple EHT events during their lifetime, as predicted in a changing climate. This is particularly the case for associations with facultative microbial partners involved in insect heat tolerance, the resilience of which to repeated heat stress has never been studied. We compared two artificial lines of the pea aphid (Acyrthosiphon pisum) differing by the absence or presence of the heat-protective facultative bacterium Serratia symbiotica. We exposed insect nymphs to a varying number of EHT events (between 0 and 3), and recorded fitness parameters. Except survival traits, fitness estimates were affected by the interaction between aphid infection status (absence/presence of S. symbiotica) and thermal treatment (number of heat shocks applied). Costs of bacterial infection were detected in the absence of thermal stress: symbiont-hosting aphids incurred longer development, decreased fecundity and body size. However, symbiotic infection turned neutral, and even beneficial for some traits (development and body size), as the number of heat shocks increased, and compared to the aposymbiotic strain. Conversely, symbiotic infection mediated aphid response to heat shock(s): fitness decreased only in the uninfected group. These findings suggest that (i) the facultative symbiont may alternatively act as a pathogen, commensal or mutualist depending on thermal environment, and (ii) the heat protection it delivered to its host persists under frequent EHT. We discuss eco-evolutionary implications and the role of potentially confounding factors (stage-specific effects, genetic polymorphism displayed by the obligate symbiont).