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1. The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

   https://doi.org/10.1002/ajp.22974  

   Greene, Lydia K.; Bornbusch, Sally L.; McKenney, Erin A.; Harris, Rachel L.; Gorvetzian, Sarah R.; Yoder, Anne D.; Drea, Christine M. (April 2019, American Journal of Primatology)

   Abstract Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host–microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure. Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage‐specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research. We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent‐gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host–microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis‐driven research. 

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2. Antibiotic perturbation of gut bacteria does not significantly alter host responses to ocular disease in a songbird species

   https://doi.org/10.7717/peerj.13559  

   Weitzman, Chava L.; Belden, Lisa K.; May, Meghan; Langager, Marissa M.; Dalloul, Rami A.; Hawley, Dana M. (January 2022, PeerJ)

   Bacterial communities in and on wild hosts are increasingly appreciated for their importance in host health. Through both direct and indirect interactions, bacteria lining vertebrate gut mucosa provide hosts protection against infectious pathogens, sometimes even in distal body regions through immune regulation. In house finches ( Haemorhous mexicanus ), the bacterial pathogen Mycoplasma gallisepticum (MG) causes conjunctivitis, with ocular inflammation mediated by pro- and anti-inflammatory cytokines and infection triggering MG-specific antibodies. Here, we tested the role of gut bacteria in host responses to MG by using oral antibiotics to perturb bacteria in the gut of captive house finches prior to experimental inoculation with MG. We found no clear support for an impact of gut bacterial disruption on conjunctival pathology, MG load, or plasma antibody levels. However, there was a non-significant trend for birds with intact gut communities to have greater conjunctival pathology, suggesting a possible impact of gut bacteria on pro-inflammatory cytokine stimulation. Using 16S bacterial rRNA amplicon sequencing, we found dramatic differences in cloacal bacterial community composition between captive, wild-caught house finches in our experiment and free-living finches from the same population, with lower bacterial richness and core communities composed of fewer genera in captive finches. We hypothesize that captivity may have affected the strength of results in this experiment, necessitating further study with this consideration. The abundance of anthropogenic impacts on wildlife and their bacterial communities, alongside the emergence and spread of infectious diseases, highlights the importance of studies addressing the role of commensal bacteria in health and disease, and the consequences of gut bacterial shifts on wild hosts. 

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3. Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

   https://doi.org/10.1186/s42523-022-00176-x  

   Bornbusch, Sally L.; Greene, Lydia K.; Rahobilalaina, Sylvia; Calkins, Samantha; Rothman, Ryan S.; Clarke, Tara A.; LaFleur, Marni; Drea, Christine M. (April 2022, Animal Microbiome)

   Abstract BackgroundInter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia. ResultsThe diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota. ConclusionsAs one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes. 

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4. 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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5. A comparison of great ape life histories in captivity

   Harwell, Faye; Knott, Cheryl D. (November 2020, 6th Annual Meeting of the Northeastern Evolutionary Primatologists)

   null (Ed.)

   Primates, especially great apes, have slow life histories and long lifespans compared to other mammalian groups. Data pertaining to life history variables can be difficult to collect in the wild considering that species can have longer lifespans than the duration of a field site’s existence. Here, we examine life history variables for captive-born great apes housed in the United States. Using studbook data, we investigate stillbirth rates, age at first birth (AFB), interbirth intervals, number of offspring, twinning rates, mean lifespan and maximum lifespans. Analyses presented here exclude individuals with estimated birthdates. The oldest maximum lifespan was recorded for gorillas (60.07yrs (female); n= 656) followed by chimpanzees (57.40yrs (female); n= 559), orangutans (54.88yrs (female); n= 660), and bonobos (52.15yrs (female); n= 144). Excluding individuals living ≤10 years of age, mean lifespan is similar for all great apes in captivity (F(3,417)= 0.849, p= 0.467; bonobos: 23.5 ± 9.8yrs; chimpanzees: 25.2 ± 10.6yrs; gorillas: 26.2 ± 10.2yrs; orangutans: 24.2 ± 10.0yrs). The stillbirth rate is highest in chimpanzees (0.147; n=559) then gorillas (0.144; n=658), bonobos (0.125; n=144), and orangutans (0.010; n=681). Gorillas (11.4 ± 3.7yrs) have a younger AFB, on average, than chimpanzees (15.9 ± 6.9yrs), bonobos (14.3 ± 6.9yrs), or orangutans (14.4 ± 5.1yrs) (F(3,377)= 13.97, p< 0.0001). We discuss how our findings are influenced by changes in husbandry practices as well as the captive environment. By examining the life histories of captive populations, we highlight the plasticity these species exhibit in relation to the timing of developmental and reproductive events. 

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