The temperature dependence of infection reflects changes in performance of parasites and hosts. High temperatures often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit endothermic thermoregulation—rare among insects—that can favor resistance to parasites. However, viruses are heavily host-dependent, suggesting that viral infection could be supported—not threatened—by optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape infection, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied <2-fold over a > 30 °C interval spanning temperatures typical of ectothermic insects and honey bees. In contrast, honey bee performance peaked at high (≥ 35 °C) temperatures and was highly temperature-sensitive. Although these results suggested that increasing temperature would favor hosts over viruses, the temperature dependence of pupal infection matched that of pupal development, falling only near pupae’s upper thermal limits. Our results reflect the host-dependent nature of viruses, suggesting that infection is accelerated—not curtailed—by optimum host function, contradicting predictions based on relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival that limit the viability of bee ‘fever’.

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The temperature dependence of infection reflects changes in the performance of parasites and hosts. High temperatures (i.e., fever) often mitigate infection by favoring heat–tolerant hosts over heat–sensitive parasites. Honey bees exhibit an endothermic, colony-level temperature regulation that is exceptional among insects and favors resistance to several parasites. However, proliferation of viruses is heavily host–dependent, suggesting that viral infection could be linked to—not threatened by—optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape virus proliferation, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied by <2-fold over a >30°C interval that spanned the temperatures typical of ectothermic insects and honey bees. In contrast, metrics of honey bee performance peaked at high (≥35°C) temperatures and were highly temperature-sensitive, with respiration varying 8-fold over a 20°C interval and successful development requiring a narrow 8°C temperature range. Although these results suggested that hosts would gain a relative advantage over viruses with increasing temperature, the temperature dependence of pupal infection matched that of pupal development, falling only near pupae`s upper thermal limits. Our results reflect the host-dependent nature of virus proliferation, suggesting that infection is accelerated—not curtailed—by optimum host function, contradicting predictions of infection based on the relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival. Despite a 98% reduction in infection at the upper end of the colony temperature range, the narrow thermal safety margin for honey bee development might preclude the effectiveness of `fever` for controlling viruses.

Temperature affects growth, metabolism, and interspecific interactions in microbial communities. Within animal hosts, gut bacterial symbionts can provide resistance to parasitic infections. Infection can also be shaped by host body temperature. However, the effects of temperature on the antiparasitic activities of gut symbionts have seldom been explored. The Lactobacillus-rich gut microbiota of facultatively endothermic honey bees is subject to seasonal and ontogenetic changes in host temperature that could alter the effects of symbionts against parasites. We used cell cultures of a Lactobacillus symbiont and an important trypanosomatid gut parasite of honey bees to test the potential for temperature to shape parasite-symbiont interactions. We found that symbionts showed greater heat tolerance than parasites and chemically inhibited parasite growth via production of acids. Acceleration of symbiont growth and acid production at high temperatures resulted in progressively stronger antiparasitic effects across a temperature range typical of bee colonies. Consequently, the presence of symbionts reduced both peak growth rate and heat tolerance of parasites. Results suggest that the endothermic behavior of honey bees could potentiate the effectiveness of gut symbionts that limit parasite ability to withstand high temperature, implicating thermoregulation as a reinforcer of core symbioses and possibly microbiome-mediated antiparasitic defense. Importance: Two factors that shape the resistance of animals to infection are body temperature and gut microbiota. However, temperature can also alter interactions among microbes, raising the question of whether and how temperature changes the antiparasitic effects of gut microbiota. Honey bees are agriculturally important hosts of diverse parasites and infection-mitigating gut microbes. They can also socially regulate their body temperatures to an extent unusual for an insect. We show that high temperatures found in honey bee colonies augment the ability of a gut bacterial symbiont to inhibit growth of a common bee parasite and reduce the parasite&#39s ability to grow at high temperatures. This suggests that fluctuations in colony and body temperatures across life stages and seasons could alter the protective value of bees&#39 gut microbiota against parasites, and that temperature-driven changes in gut microbiota could be an underappreciated mechanism by which temperature— including endothermy and fever— alters animal infection.

The temperature dependence of infection reflects changes in performance of parasites and hosts. High temperatures often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit endothermic thermoregulation—rare among insects—that can favor resistance to parasites. However, viruses are heavily host-dependent, suggesting that viral infection could be supported—not threatened—by optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape infection, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied <2-fold over a >30 °C interval spanning temperatures typical of ectothermic insects and honey bees. In contrast, honey bee performance peaked at high (≥ 35 °C) temperatures and was highly temperature-sensitive. Although these results suggested that increasing temperature would favor hosts over viruses, the temperature dependence of pupal infection matched that of pupal development, falling only near pupae’s upper thermal limits. Our results reflect the host-dependent nature of viruses, suggesting that infection is accelerated—not curtailed—by optimum host function, contradicting predictions based on relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival that limit the viability of bee ‘fever’.