Experimental depletion of gut microbiota diversity reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm

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.

Diving in hot water: a meta-analytic review of how diving vertebrate ectotherms will fare in a warmer world

ABSTRACTDiving ectothermic vertebrates are an important component of many aquatic ecosystems, but the threat of climate warming is particularly salient to this group. Dive durations typically decrease as water temperatures rise; yet, we lack an understanding of whether this trend is apparent in all diving ectotherms and how this group will fare under climate warming. We compiled data from 27 studies on 20 ectothermic vertebrate species to quantify the effect of temperature on dive durations. Using meta-analytic approaches, we show that, on average, dive durations decreased by 11% with every 1°C increase in water temperature. Larger increases in temperature (e.g. +3°C versus +8–9°C) exerted stronger effects on dive durations. Although species that respire bimodally are projected to be more resilient to the effects of temperature on dive durations than purely aerial breathers, we found no significant difference between these groups. Body mass had a weak impact on mean dive durations, with smaller divers being impacted by temperature more strongly. Few studies have examined thermal phenotypic plasticity (N=4) in diving ectotherms, and all report limited plasticity. Average water temperatures in marine and freshwater habitats are projected to increase between 1.5 and 4°C in the next century, and our data suggest that this magnitude of warming could translate to substantial decreases in dive durations, by approximately 16–44%. Together, these data shed light on an overlooked threat to diving ectothermic vertebrates and suggest that time available for underwater activities, such as predator avoidance and foraging, may be shortened under future warming.

Life history trade-offs in ectotherms impart a pseudo-hormetic response, not hormesis

All organisms are faced with survival and fitness challenges. However, differences in how ectotherms and endotherms deal with these challenges causes confusion when theoretical explanations are proposed. Herein, an immunochallenged, immature ectothermic vertebrate increased growth in the face of immunochallenge, reminiscent of up-regulated physiological efficiency termed hormesis. The immunochallenged subjects increased food intake relative to control animals, a largely ignored possibility in previous studies. This likely led to an energy surplus that fueled additional growth. Although there was increased resource demand from the immune response that exceeded internal stores, the acceptably sized food items contained more resources than immunologically-driven demand required. We theorize that because ectotherms lack significant internally-stored resources compared to endotherms, they must feed to fuel increased physiological demand. This can lead to excess resource intake because the minimum acceptably sized prey contains more available resources than upregulation required. This creates a pseudo-hormetic hormetic response, fueled by excess food intake rather than significant improved physiological efficiency. Further, we speculate that lifespan and/or maturity may interact with resource management ectotherms, though our data are inconclusive on this matter. Ultimately, our data suggest additional growth when ectotherms face stressors is a pseudo-hormetic response stemming from increased food intake instead of upregulated physiological efficiency.