A perspective on insect–microbe holobionts facing thermal fluctuations in a climate‐change context

Abstract

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.

Thermal sensitivity and seasonal change in the gut microbiome of a desert ant, Cephalotes rohweri

“…Such experiments have been conducted in Drosophila melanogaster and aphids and have demonstrated that the effects of past exposure to temperature on the microbiome can be inherited and have consequences for the host phenotype (Moghadam et al 2018;Heyworth, Smee and Ferrari 2020). Transplant experiments have linked temperaturedriven microbiome changes to improved temperature tolerance, but beneficial or detrimental microbiome compositional shifts may occur in a much wider array of animals (Sepulveda and Moeller 2020;Iltis et al 2021). This type of experiment may be difficult to conduct in Cephalotes spp., as microbiomes are believed to be largely isolated from external contamination after formation of the proventriculus in newly enclosed adults, leaving only a short window in which to perform experimental microbiome transplants (Lanan et al 2017).…”

“…Ectotherm responses to temperatures of different extremes or duration may also guide expectations of microbiome thermal sensitivity (Iltis et al 2021). Acclimation, a gradual improvement in ability to tolerate temperature deviations from optimum following exposure, is very common among ectotherms (Gaston et al 2009).…”

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

“…The distinction here made between long-and short-term heat stress is artificial, but it could shed light on the thermal sensitivity of mechanisms underpinning symbiont-mediated tolerance to high temperatures. The results suggesting how impactful the temporal dynamic of temperatures is for aphid-symbiont associations should prompt further efforts to probe into the responses of these systems to patterns of temperature fluctuations hitherto unexplored, both along temporal (e.g., diurnal and seasonal temperature cycles) and spatial axes (e.g., (micro)climatic gradients) (17,19,36). This should be of great relevance for general predictions about the evolutionary fate of insectmicrobe partnerships facing climate change, which will alter both mean temperature and variability around that mean, this latter thermal parameter having already documented impacts on the outcomes of other kinds of biotic interactions (57,58).…”

“…Temperature has been rapidly identified as a key environmental parameter determining the net fitness consequences of carrying a particular symbiont genotype (for obligate and facultative symbionts) or species (for facultative symbionts) (for reviews, see [17][18][19][20]. Indeed, the insect resilience to stressful high temperatures can be curtailed by a single mutation affecting a gene encoding the production of heat protective molecules by the obligate symbiont (21,22), while improved by the presence of some facultative symbionts bestowing physiological tolerance to heat (23,24).…”

“…These different lines of evidence raise concern about the short-and long-term maintenance of symbiotic associations enduring changing thermal conditions, such as increased mean temperature and frequency of heat events forecasted under climate change (28). Several putative evolutionary scenarios have been proposed to anticipate the fate of insect-microbe mutualisms in this climatic context, depending on the potential for symbiotic relationships to maintain sustainable insect performance and evolutionary capacity under heat stress (7,19,29). As empirical evidence has accumulated over the last two decades, it would be now valuable to draw first general patterns about the thermal sensitivity of insect-microbe partnerships and their implications for understanding the ecological and evolutionary trajectories of these mutualistic associations under a changing climate.…”