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).

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

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, insect resilience to stressful high temperatures depends on the genetic identity of the obligate symbiont and the presence of heat-protective facultative symbionts. As extensively studied organisms, aphids and their endosymbiotic bacteria represent valuable models to address eco-evolutionary questions about the thermal ecology of insect-microbe partnerships, with broad relevance to various biological systems and insect models. 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 (resistance to parasitoids) and costs (development, fecundity) of infection by facultative symbionts, which was overall mostly beneficial to the hosts 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. We discuss the implications of these findings for the general understanding of the cost-benefit balance of insect-microbe associations across multiple traits and their eco-evolutionary dynamics faced with climate change.

A perspective on insect-microbe holobionts facing thermal fluctuations in a climate-change context.

Temperature influences the ecology and evolution of insects and their symbionts by impacting each partner independently and their interactions, considering the holobiont as a primary unit of selection. There are sound data about the responses of these partnerships to constant temperatures and sporadic thermal stress (mostly heat shock). However, the current understanding of the thermal ecology of insect-microbe holobionts remains patchy because the complex thermal fluctuations (at different spatial and temporal scales) experienced by these organisms in nature have often been overlooked experimentally. This may drastically constrain our ability to predict the fate of mutualistic interactions under climate change, which will alter both mean temperatures and thermal variability. Here, we tackle down these issues by focusing on the effects of temperature fluctuations on the evolutionary ecology of insect-microbe holobionts. We propose potentially worth-investigating research avenues to (i) evaluate the relevance of theoretical concepts used to predict the biological impacts of temperature fluctuations when applied to holobionts; (ii) acknowledge the plastic (behavioural thermoregulation, physiological acclimation) and genetic responses (evolution) expressed by holobionts in fluctuating thermal environments; and (iii) explore the potential impacts of previously unconsidered patterns of temperature fluctuations on the outcomes and the dynamic of these insect-microbe associations.

Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids.

Pear cultivation accounts for a large proportion of worldwide orchards, but its sustainability is controversial because it relies on intensive use of pesticides. It is therefore crucial and timely to find alternative methods to chemical control in pear orchards. The psyllids Cacopsylla pyri and Cacopsylla pyricola are the most important pests of pear trees in Europe and North America, respectively, because they infest all commercial varieties, causing damage directly through sap consumption or indirectly through the spread of diseases. A set of natural enemies exists, ranging from generalist predators to specialist parasitoids. Trechnites insidiosus (Crawford) is undoubtedly the most abundant specialist parasitoid of psyllids. In our literature review, we highlight the potential of this encyrtid species as a biological control agent of psyllid pests by first reviewing its biology and ecology, and then considering its potential at regulating psyllids. We show that the parasitoid can express fairly high parasitism rates in orchards, and almost perfectly matches the phenology of its host and is present early in the host infestation season, which is an advantage for controlling immature stages of psyllids. We propose new research directions and innovative approaches that would improve the use of T. insidiosus in integrated pest management strategies in the future, regarding both augmentative and conservation biocontrol. We conclude that T. insidiosus has many advantages and should be included as part of integrated biological control strategies of pear psyllids, along with predators, in-field habitat conservation, and the rational use of compatible chemicals. © 2021 Society of Chemical Industry.

How to stand the heat? Post-stress nutrition and developmental stage determine insect response to a heat wave.

Organisms are increasingly confronted with intense and long-lasting heat waves. In insects, the effects of heat waves on individual performance can vary in magnitude both within (e.g. from one larval instar to another) and between life stages. However, the reasons underlying these stage-dependent effects are not fully understood. There are several lines of evidence suggesting that individual ability to withstand a heat stress depends on mechanisms based on nutrition and supporting energetically physiological stress responses. Hence, we tested the hypothesis that the efficiency of these food-based buffering mechanisms may vary between different larval instars of a phytophagous insect. Using larvae of the moth Lobesia botrana, we examined the importance of post-stress food quality in insect response to a non-lethal heat wave at two distinct larval instars. Three major conclusions were drawn from this work. First, heat waves induced an overall decline in larval performance (delayed development, depressed immunity). Second, food quality primarily mediated the insect's ability to respond to the heat stress: the reduction in performance following heat wave application was mostly restricted to individuals with access to low-quality food after the heat stress. Third, larval instars differed in their susceptibility to this combination of thermal and food stressors, but conclusions about the instar being the most vulnerable differed in a trait-specific manner. In a global warming context, this study may shed additional light on the combination of direct and indirect (through alteration of plant nutritional value) effects of rising temperatures on the ecology and the evolution of phytophagous insects.

Where you come from matters: temperature influences host-parasitoid interaction through parental effects.

Temperature alters host suitability for parasitoid development through direct and indirect pathways. Direct effects depend on ambient temperatures experienced by a single host individual during its lifetime. Indirect effects (or parental effects) occur when thermal conditions met by a host parental generation affect the way its offspring will interact with parasitoids. Using the complex involving eggs of the moth Lobesia botrana as hosts for the parasitoid Trichogramma cacoeciae, we developed an experimental design to disentangle the effects of (1) host parental temperature (temperature at which the host parental generation developed and laid host eggs) and (2) host offspring temperature (temperature at which host eggs were incubated following parasitism, i.e. direct thermal effects) on this interaction. The host parental generation was impacted by temperature experienced during its development: L. botrana females exposed to warmer conditions displayed a lower pupal mass but laid more host eggs over a 12-h period. Host parental temperature also affected the outcomes of the interaction. Trichogramma cacoeciae exhibited lower emergence rates but higher hind tibia length on emergence from eggs laid under warm conditions, even if they were themselves exposed to cooler temperatures. Such indirect thermal effects might arise from a low nutritional quality and/or a high immunity of host eggs laid in warm conditions. By contrast with host parental temperature, offspring temperature (direct thermal effects) did not significantly affect the outcomes of the interaction. This work emphasises the importance of accounting for parental thermal effects to predict the future of trophic dynamics under global warming scenarios.

Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling.

Predicting species responses to climate change requires tracking the variation in individual performance following exposure to warming conditions. One ecologically relevant approach consists of examining the thermal responses of a large number of traits, both related with population dynamics and trophic interactions (i.e. a multi-trait approach). Based on in situ climatic data and projections from climate models, we here designed two daily fluctuating thermal regimes realistically reflecting current and future conditions in Eastern France. These models detected an increase in mean temperature and in the range of daily thermal fluctuations as two local facets of global warming likely to occur in our study area by the end of this century. We then examined the responses of several fitness-related traits in caterpillars of the moth Lobesia botrana - including development, pupal mass, survival rates, energetic reserves, behavioral and immune traits expressed against parasitoids - to this experimental imitation of global warming. Increasing temperatures positively affected development (leading to a 31% reduction in the time needed to complete larval stage), survival rates (+19%), and movement speed as a surrogate for larval escape ability to natural enemies (+60%). Conversely, warming elicited detrimental effects on lipid reserves (-26%) and immunity (total phenoloxidase activity: -34%). These findings confirm that traits should differ in their sensitivity to global warming, underlying complex consequences for population dynamics and trophic interactions. Our study strengthens the importance of combining a multi-trait approach with the use of realistic fluctuating regimes to forecast the consequences of global warming for individuals, species and species assemblages.