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1. Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats ( Neotoma spp.)

   https://doi.org/10.1073/pnas.2108787118  

   Weinstein, Sara B.; Martínez-Mota, Rodolfo; Stapleton, Tess E.; Klure, Dylan M.; Greenhalgh, Robert; Orr, Teri J.; Dale, Colin; Kohl, Kevin D.; Dearing, M. Denise (November 2021, Proceedings of the National Academy of Sciences)

   The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genusNeotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. 

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2. Multiple dimensions of dietary diversity in large mammalian herbivores

   https://doi.org/10.1111/1365-2656.13206  

   Kartzinel, Tyler R.; Pringle, Robert M.; Eizaguirre, ed., Christophe (April 2020, Journal of Animal Ecology)

   Abstract Theory predicts that trophic specialization (i.e. low dietary diversity) should make consumer populations sensitive to environmental disturbances. Yet diagnosing specialization is complicated both by the difficulty of precisely quantifying diet composition and by definitional ambiguity: what makes a diet ‘diverse’?We sought to characterize the relationship between taxonomic dietary diversity (TDD) and phylogenetic dietary diversity (PDD) in a species‐rich community of large mammalian herbivores in a semi‐arid East African savanna. We hypothesized that TDD and PDD would be positively correlated within and among species, because taxonomically diverse diets are likely to include plants from many lineages.By using DNA metabarcoding to analyse 1,281 faecal samples collected across multiple seasons, we compiled high‐resolution diet profiles for 25 sympatric large‐herbivore species. For each of these populations, we calculated TDD and PDD with reference to a DNA reference library for local plants.Contrary to our hypothesis, measures of TDD and PDD were either uncorrelated or negatively correlated with each other. Thus, these metrics reflect distinct dimensions of dietary specialization both within and among species. In general, grazers and ruminants exhibited greater TDD, but lower PDD, than did browsers and non‐ruminants. We found significant seasonal variation in TDD and/or PDD for all but four species (Grevy's zebra, buffalo, elephant, Grant's gazelle); however, the relationship between TDD and PDD was consistent across seasons for all but one of the 12 best‐sampled species (plains zebra).Our results show that taxonomic generalists can be phylogenetic specialists, and vice versa. These two dimensions of dietary diversity suggest contrasting implications for efforts to predict how consumers will respond to climate change and other environmental perturbations. For example, populations with low TDD may be sensitive to phylogenetically ‘random’ losses of food species, whereas populations with low PDD may be comparatively more sensitive to environmental changes that disadvantage entire plant lineages—and populations with low dietary diversity in both taxonomic and phylogenetic dimensions may be most vulnerable of all. 

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3. Covariation of diet and gut microbiome in African megafauna

   https://doi.org/10.1073/pnas.1905666116  

   Kartzinel, Tyler R.; Hsing, Julianna C.; Musili, Paul M.; Brown, Bianca R.; Pringle, Robert M. (November 2019, Proceedings of the National Academy of Sciences)

   A major challenge in biology is to understand how phylogeny, diet, and environment shape the mammalian gut microbiome. Yet most studies of nonhuman microbiomes have relied on relatively coarse dietary categorizations and have focused either on individual wild populations or on captive animals that are sheltered from environmental pressures, which may obscure the effects of dietary and environmental variation on microbiome composition in diverse natural communities. We analyzed plant and bacterial DNA in fecal samples from an assemblage of 33 sympatric large-herbivore species (27 native, 6 domesticated) in a semiarid East African savanna, which enabled high-resolution assessment of seasonal variation in both diet and microbiome composition. Phylogenetic relatedness strongly predicted microbiome composition ( r = 0.91) and was weakly but significantly correlated with diet composition ( r = 0.20). Dietary diversity did not significantly predict microbiome diversity across species or within any species except kudu; however, diet composition was significantly correlated with microbiome composition both across and within most species. We found a spectrum of seasonal sensitivity at the diet−microbiome nexus: Seasonal changes in diet composition explained 25% of seasonal variation in microbiome composition across species. Species’ positions on (and deviations from) this spectrum were not obviously driven by phylogeny, body size, digestive strategy, or diet composition; however, domesticated species tended to exhibit greater diet−microbiome turnover than wildlife. Our results reveal marked differences in the influence of environment on the degree of diet−microbiome covariation in free-ranging African megafauna, and this variation is not well explained by canonical predictors of nutritional ecology. 

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4. Movement ecology and sex are linked to barn owl microbial community composition

   https://doi.org/10.1111/mec.15398  

   Corl, Ammon; Charter, Motti; Rozman, Gabe; Toledo, Sivan; Turjeman, Sondra; Kamath, Pauline L.; Getz, Wayne M.; Nathan, Ran; Bowie, Rauri C. K. (April 2020, Molecular Ecology)

   Abstract The behavioural ecology of host species is likely to affect their microbial communities, because host sex, diet, physiology, and movement behaviour could all potentially influence their microbiota. We studied a wild population of barn owls (Tyto alba) and collected data on their microbiota, movement, diet, size, coloration, and reproduction. The composition of bacterial species differed by the sex of the host and female owls had more diverse bacterial communities than their male counterparts. The abundance of two families of bacteria, Actinomycetaceae and Lactobacillaceae, also varied between the sexes, potentially as a result of sex differences in hormones and immunological function, as has previously been found with Lactobacillaceae in the microbiota of mice. Male and female owls did not differ in the prey they brought to the nest, which suggests that dietary differences are unlikely to underlie the differences in their microbiota. The movement behaviour of the owls was associated with the host microbiota in both males and females because owls that moved further from their nest each day had more diverse bacterial communities than owls that stayed closer to their nests. This novel result suggests that the movement ecology of hosts can impact their microbiota, potentially on the basis of their differential encounters with new bacterial species as the hosts move and forage across the landscape. Overall, we found that many aspects of the microbial community are correlated with the behavioural ecology of the host and that data on the microbiota can aid in generating new hypotheses about host behaviour. 

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5. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas

   https://doi.org/10.1186/s40168-020-00977-9  

   Baniel, Alice; Amato, Katherine R.; Beehner, Jacinta C.; Bergman, Thore J.; Mercer, Arianne; Perlman, Rachel F.; Petrullo, Lauren; Reitsema, Laurie; Sams, Sierra; Lu, Amy; et al (December 2021, Microbiome)

   null (Ed.)

   Abstract Background Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. Results Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas ( Theropithecus gelada ). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. Conclusion Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. 

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