You are more than what you eat: potentially adaptive enrichment of microbiome functions across bat dietary niches.

BACKGROUND: Animals evolved in a microbial world, and their gut microbial symbionts have played a role in their ecological diversification. While many recent studies report patterns of phylosymbiosis between hosts and their gut bacteria, fewer studies examine the potentially adaptive functional contributions of these microbes to the dietary habits of their hosts. In this study, we examined predicted metabolic pathways in the gut bacteria of more than 500 individual bats belonging to 60 species and compare the enrichment of these functions across hosts with distinct dietary ecologies. RESULTS: We found that predicted microbiome functions were differentially enriched across hosts with different diets. Using a machine-learning approach, we also found that inferred microbiome functions could be used to predict specialized host diets with reasonable accuracy. We detected a relationship between both host phylogeny and diet with respect to microbiome functional repertoires. Because many predicted functions could potentially fill nutritional gaps for bats with specialized diets, we considered pathways discriminating dietary niches as traits of the host and fit them to comparative phylogenetic models of evolution. Our results suggest that some, but not all, predicted microbiome functions may evolve toward adaptive optima and thus be visible to the forces of natural selection operating on hosts over evolutionary time. CONCLUSIONS: Our results suggest that bats with specialized diets may partially rely on their gut microbes to fulfill or augment critical nutritional pathways, including essential amino acid synthesis, fatty acid biosynthesis, and the generation of cofactors and vitamins essential for proper nutrition. Our work adds to a growing body of literature suggesting that animal microbiomes are structured by a combination of ecological and evolutionary processes and sets the stage for future metagenomic and metabolic characterization of the bat microbiome to explore links between bacterial metabolism and host nutrition.

Thermoregulatory variation among populations of bats along a latitudinal gradient.

Most studies of hibernation physiology sample individuals from populations within a single geographic area, yet some species have large ranges meaning populations likely experience area-specific levels of energetic challenges. As well, few studies have assessed within-season variation. Since physiological adjustments often are influenced by environmental factors, and the types of environments vary with geography, we expected variance in hibernation patterns among geographically separated populations. Our specific goal was to measure intraspecific variation in torpid metabolic rate (TMR) and body temperature (T (b)) as a function of ambient temperature (T (a)) for a non-migratory and migratory species to determine whether there is a continuum in physiological responses based on latitude. We chose big brown (Eptesicus fuscus) and eastern red bats (Lasiurus borealis) as model species and sampled individuals from populations throughout each species' winter range. In both species, individuals from southern populations maintained higher TMR at cooler T (a)s and lower TMR at warmer T (a)s than those from northern populations. Big brown bats from southern populations regulated T (b) during torpor at higher levels and there was no significant difference in T (b) between populations of eastern red bats. Although metabolic responses were similar across the gradient between species, the effect was more dramatic in big brown bats. Our data demonstrate a continuum in thermoregulatory response, ranging from classic hibernation in northern populations to a pattern more akin to daily torpor in southern populations. Our research highlights the potential usefulness of bats as model organisms to address questions about within-species physiological variation in wild populations.

Energy availability influences microclimate selection of hibernating bats.

Many species hibernate to conserve energy during periods of low food and water availability. It has long been assumed that the optimal hibernation strategy involves long, deep bouts of torpor that minimize energy expenditure. However, hibernation has ecological (e.g. decreased predator avoidance) and physiological (e.g. sleep deprivation) costs that must be balanced with energy savings; therefore, individuals possessing sufficient energy reserves may reduce their use of deep torpor. We tested the hypothesis that energy (fat) availability influences temperature selection of two fat-storing bat species during hibernation. We predicted that individuals with small energy reserves would select colder temperatures for hibernation in order to minimize energy expenditure, while individuals with larger energy reserves would choose warmer temperatures to minimize the costs of hibernation. Results from our field experiment indicate that little brown myotis (Myotis lucifugus) hibernating in warm microclimates were significantly heavier than individuals hibernating in cooler microclimates. To determine if energy availability was mediating this relationship, we limited fatty acid availability with mercaptoacetate (MA) and quantified its effect on torpid metabolic rate (TMR) and thermal preference of big brown bats (Eptesicus fuscus). Administration of MA caused a 43% drop in TMR at 10 degrees C and caused bats to choose significantly colder temperatures for hibernation. Our results suggest that fat-storing bats minimize torpor expression using both physiological and behavioral mechanisms.