Impact of heat stress on the fitness outcomes of symbiotic infection in aphids: a meta-analysis

Abstract

Beneficial microorganisms shape the evolutionary trajectories of their hosts, facilitating or constraining the colonization of new ecological niches. One convincing example entails the responses of insect-microbe associations to rising temperatures. Indeed, the insect resilience to stressful high temperatures depends on the genetic identity of the obligate symbiont and the presence of heat protective facultative symbionts. With accumulating empirical evidence, there is a need of integrative studies to draw general patterns about the thermal sensitivity of insect-microbe associations, from an eco-evolutionary perspective. Focusing on aphid-bacteria mutualisms, this meta-analysis aims to quantify the context-dependent impacts of symbionts on host phenotype in benign or stressful heat conditions, across fitness traits, types of heat stress, and symbiont species. We found that warming lowered the benefits (parasitoid resistance) and costs (development, fecundity) of infection by facultative symbionts, which was overall mostly beneficial to the aphids under short-term heat stress (heat shock) rather than extended warming. Heat tolerant genotypes of the obligate symbiont Buchnera aphidicola and some facultative symbionts (Rickettsia sp., Serratia symbiotica) improved or maintained aphid fitness under heat stress. As phytophagous insects are central to terrestrial ecosystems, symbiont-mediated responses to increasing mean temperatures and frequency of heat waves in the context of climate change are key elements that may have cascading effects on food webs and there is an urgent need to continue accumulating data on other models. We discuss the implications of these conclusions for the general understanding of the cost-benefits balance and eco-evolutionary dynamics of insect-microbe associations faced with climate change.

Scientists' warning on climate change and insects

“…For instance, gut microbiome composition can shift across seasons and is concurrent with changes in cold tolerance (Ferguson et al, 2018). Benefits or drawbacks provided by symbionts can be altered by increasing temperatures (Bensadia et al, 2006; Higashi et al, 2020; Tougeron & Iltis, 2022), in part because some symbionts reside in highly heat‐sensitive organs (e.g., bacteriocytes, Shan et al, 2017) and reversely, alteration in the gut or intracellular microbial community can influence insect resistance to temperature variation (Henry & Colinet, 2018; Iltis, Tougeron, et al, 2021; Jaramillo & Castañeda, 2021). Moreover, the microbiome can be totally restructured during diapause in arthropods (Mushegian et al, 2018; Mushegian & Tougeron, 2019), but how modifications in seasonal strategies following climate change actually affect microbial communities merit further investigations.…”