The central aim of conservation biology is to understand and mitigate the effects of human activities on biodiversity. To successfully achieve this objective, researchers must take an interdisciplinary approach that fully considers the effects, both direct and indirect, of anthropogenic disturbances on wildlife physiology and health. A recent surge in research has revealed that host-associated microbiota—the archaeal, bacterial, fungal and viral communities residing on and inside organisms—profoundly influence animal health, and that these microbial communities can be drastically altered by anthropogenic activities. Therefore, conservation practitioners should consider the disruption of host-associated microbial diversity as a serious threat to wildlife populations. Despite the tremendous potential for microbiome research to improve conservation outcomes, few efforts have been made to truly integrate these fields. In this review, we call for the microbial renaissance of conservation biology, where biodiversity of host-associated microbiota is recognized as an essential component of wildlife management practices. Using evidence from the existing literature, we will examine the known effects of anthropogenic activities on the diversity of host-associated microbial communities and integrate approaches for maintaining microbial diversity to successfully achieve conservation objectives.

Environmental temperature and gut microbial communities can both have profound impacts on the digestive performance of ectothermic vertebrates. Additionally, the diversity, composition and function of gut microbial communities themselves are influenced by temperature. It is typically assumed that the temperature-dependent nature of ectotherm digestive performance is due to factors such as host physiological changes and adaptation to local climatic conditions. However, it is also possible that temperature-induced alterations to gut microbiota may influence the relationship between temperature and digestion. To explore the connections between these three factors, we compared digestive performance and gut microbial community diversity and composition in red-backed salamanders housed at three experimental temperatures: 10, 15 and 20°C. We also investigated associations between specific bacterial taxa and temperature or salamander digestive performance. We found that salamander digestive performance was greatest at 15°C, while gut microbial diversity was reduced at 20°C. Further, gut microbial community composition differed among the three temperature treatments. The relative abundance of 25 bacterial genera was dependent on temperature, with high temperatures being associated with reductions in the relative abundance of disease-resistant bacteria and increases in pathogenic taxa. The relative abundance of four bacterial genera was correlated with salamander energy assimilation, two of which are known to digest chitin, a main component of the red-backed salamander diet. These findings suggest that gut microbiota may mediate the relationship between temperature and digestion in ectotherms. We discuss how global climate change may impact ectotherms by altering host-microbe interactions.

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Environmental temperature can alter the composition, diversity, and function of ectothermic vertebrate gut microbial communities, which may result in negative consequences for host physiology, or conversely, increase phenotypic plasticity and persistence in harsh conditions. The magnitude of either of these effects will depend on the length of time animals are exposed to extreme temperatures, and how quickly the composition and function of the gut microbiota can respond to temperature change. However, the temporal effects of temperature on gut microbiota are currently unknown. Here, we investigated the length of time required for increased temperature to alter the composition of gut bacterial communities in tadpoles of two frog species, the green frog, Lithobates clamitans, and its congener, the globally invasive American bullfrog, L. catesbeianus. We also explored the potential functional consequences of these changes by comparing predicted metagenomic profiles across temperature treatments at the last experimental time point. Bullfrog‐associated microbial communities were more plastic than those of the green frog. Specifically, bullfrog communities were altered by increased temperature within hours, while green frog communities took multiple days to exhibit significant changes. Further, over ten times more bullfrog bacterial functional pathways were temperature‐dependent compared to the green frog. These results support our hypothesis that bullfrog gut microbial communities would respond more rapidly to temperature change, potentially bolstering their ability to exploit novel environments. More broadly, we have revealed that even short‐term increases in environmental temperature, expected to occur frequently under global climate change, can alter the gut microbiota of ectothermic vertebrates.

Host-associated microbial communities have profound impacts on animal physiological function, especially nutrition and metabolism. The hypothesis of ‘symmorphosis’, which posits that the physiological systems of animals are regulated precisely to meet, but not exceed, their imposed functional demands, has been used to understand the integration of physiological systems across levels of biological organization. Although this idea has been criticized, it is recognized as having important heuristic value, even as a null hypothesis, and may, therefore, be a useful tool in understanding how hosts evolve in response to the function of their microbiota. Here, through a hologenomic lens, we discuss how the idea of symmorphosis may be applied to host-microbe interactions. Specifically, we consider scenarios in which host physiology may have evolved to collaborate with the microbiota to perform important functions, and, on the other hand, situations in which services have been completely outsourced to the microbiota, resulting in relaxed selection on host pathways. Following this theoretical discussion, we finally suggest strategies by which these currently speculative ideas may be explicitly tested to further our understanding of host evolution in response to their associated microbial communities. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

Phenotypic plasticity is an important strategy that animals employ to respond and adjust to changes in their environment. Plasticity may occur via changes in host gene expression or through functional changes in their microbiomes, which contribute substantially to host physiology. Specifically, the presence and function of host-associated microbes can impact how animals respond to heat stress. We previously demonstrated that “depleted” tadpoles, with artificially disrupted microbiomes, are less tolerant to heat than “colonized” tadpoles, with more natural microbiomes. However, the mechanisms behind these effects are unclear. Here, we compare gene expression profiles of the tadpole gut transcriptome, and tadpole gut microbial metagenome, between colonized and depleted tadpoles under cool or warm conditions. Our goal was to identify differences in host and microbial responses to heat between colonized and depleted tadpoles that might explain their observed differences in heat tolerance. We found that depleted tadpoles exhibited a much stronger degree of host gene expression plasticity in response to heat, while the microbiome of colonized tadpoles was significantly more heat sensitive. These patterns indicate that functional changes in the microbiome in response to heat may allow for a dampened host response, ultimately buffering hosts from the deleterious effects of heat stress. We also identified several specific host and microbial pathways that could be contributing to increased thermal tolerance in colonized tadpoles including amino acid metabolism, vitamin biosynthesis, and ROS scavenging pathways. Our results demonstrate that the microbiome influences host plasticity and the response of hosts to environmental stressors.

Understanding the forces that shape vertebrate gut microbial community assembly and composition throughout development is a major focus of the microbiome field. Here, we utilize the complex life cycle of the eastern newt (Notophthalmus viridescens) as a natural wild model to compare the effects of host and environmental factors on gut microbiome development. We compared bacterial inventories of each of the newt's three physiologically distinct developmental stages to determine if each hosted a unique community, or if the two stages which share an aquatic habitat (larvae and adults) harbored more similar communities than those of the third stage, the terrestrial juvenile eft. Additionally, we assessed how the contribution of selective processes to gut microbial assembly changed through development. We found that structurally, each life stage harbored a distinct community, which may be attributable to host factors. Further, across development, we found that community assembly processes shifted from a predominance of neutral to selective forces. However, habitat may also be important in determining community membership and diversity due the uniqueness of eft communities based on these metrics. Our results are similar to those in other vertebrate taxa, suggesting that gut microbiota assembly processes may be conserved across diverse lineages.

Predicting the responses of ectotherms to climate change is a global conservation priority which requires identifying factors that influence how animals respond physiologically to changing temperature. Host-associated microbial communities impact animal physiology and have been shown to influence host thermal tolerance in invertebrate systems. However, the role of commensal microbiota in thermal tolerance of ectothermic vertebrates is unknown. Here we show that experimentally depleting the diversity of the tadpole gut microbiome through environmental water sterilization reduces the host's acute thermal tolerance to both heat and cold, alters the thermal sensitivity of locomotor performance, and reduces animal survival under acute heat stress. We show that these tadpoles have reduced activities of mitochondrial enzymes and altered metabolic rates compared to tadpoles colonized with a diverse microbiota, which could underlie differences in thermal phenotypes. Our results demonstrate, for the first time, a link between the gut microbiome of an ectothermic vertebrate and the host's thermal tolerance, performance, and fitness, thus highlighting the importance of considering host-associated microbial communities when predicting species' responses to climate change.