Population- and Individual-Level Dynamics of the Intestinal Microbiota of a Small Primate

Aivelo, Tuomas; Laakkonen, Juha; Jernvall, Jukka

doi:10.1128/aem.00559-16

Cited by 48 publications

(54 citation statements)

References 51 publications

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“…Host-microbiota interactions are, thus, an important factor in vertebrate ecology and evolution (Amato, 2016). However, in contrast to numerous studies on humans and laboratory animals, few studies have investigated the causes and consequences of microbiota variation in wild vertebrates, and studies based on repeated sampling of individually recognizable animals are especially rare (but see Aivelo, Laakkonen, & Jernvall, 2016;Amato et al, 2014Amato et al, , 2015.…”

Section: Introductionmentioning

confidence: 99%

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

Springer

Fichtel

Al‐Ghalith

et al. 2017

Ecology and Evolution

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The intestinal microbiota plays a major role in host development, metabolism, and health. To date, few longitudinal studies have investigated the causes and consequences of microbiota variation in wildlife, although such studies provide a comparative context for interpreting the adaptive significance of findings from studies on humans or captive animals. Here, we investigate the impact of seasonality, diet, group membership, sex, age, and reproductive state on gut microbiota composition in a wild population of group‐living, frugi‐folivorous primates, Verreaux's sifakas (Propithecus verreauxi). We repeatedly sampled 32 individually recognizable animals from eight adjacent groups over the course of two different climatic seasons. We used high‐throughput sequencing of the 16S rRNA gene to determine the microbiota composition of 187 fecal samples. We demonstrate a clear pattern of seasonal variation in the intestinal microbiota, especially affecting the Firmicutes‐Bacteroidetes ratio, which may be driven by seasonal differences in diet. The relative abundances of certain polysaccharide‐fermenting taxa, for example, Lachnospiraceae, were correlated with fruit and fiber consumption. Additionally, group membership influenced microbiota composition independent of season, but further studies are needed to determine whether this pattern is driven by group divergences in diet, social contacts, or genetic factors. In accordance with findings in other wild mammals and primates with seasonally fluctuating food availability, we demonstrate seasonal variation in the microbiota of wild Verreaux's sifakas, which may be driven by food availability. This study adds to mounting evidence that variation in the intestinal microbiota may play an important role in the ability of primates to cope with seasonal variation in food availability.

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Section: Introductionmentioning

confidence: 99%

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

Springer

Fichtel

Al‐Ghalith

et al. 2017

Ecology and Evolution

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“…Our previous study has shown that there is pervasive within-individual variation in mouse lemur microbiota (Aivelo et al 2016). Thus, it is understandable why we did not identify statistically significant host variables in microbiota variation (Appendix 4 Table A2).…”

Section: Discussionmentioning

confidence: 99%

“…The national park consist of lowland to montane rainforest between 500 and 1500 meters of elevation. We collected samples and data for nematodes, cestodes, eimeriids and ectoparasites from September to December 2011 and 2012 and microbiota from September to December 2012 along previously described protocol (Aivelo et al 2015; Aivelo, Laakkonen & Jernvall 2016) Shortly, we trapped mouse lemurs nightly on two transects, the first within the park boundaries in secondary forest and the second in peripheral zone in highly degraded campsite area. We measured mouse lemurs, collected samples and tagged previously unseen mouse lemurs for later identification with microchips.…”

Section: Methodsmentioning

confidence: 99%

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Parasite-microbiota interactions potentially affect intestinal communities in wild mammals

Aivelo

Norberg

2016

Preprint

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SummaryDetecting interaction between species is notoriously difficult, and disentangling species associations in host-related gut communities is especially challenging. Nevertheless, due to contemporary methods, including metabarcoding and 16S sequencing, collecting observational data on community composition has become easier and much more common. We studied the previously collected data sets of intestinal microbiota and parasite compositions within longitudinally followed mouse lemurs by analysing the potential interactions with diversity metrics and novel joint species distribution modelling. Both methods showed consistent statistical association between certain parasite species and microbiotal composition. Both unicellular Eimeria sp. and cestode Hymenolepis diminuta had an effect on diversity of gut microbiota. These parasite species also had negative associations with several bacterial orders. In comparison, closely related species H. nana did not have an effect on diversity, and it had positive associations with several bacterial orders. Our results reveal potential interactions between some, but not all, intestinal parasites and gut microbiota. While environmental variables explained almost half of the total variation, of which almost half could be explained by traits of parasites and microbiota, there were no clear patterns regarding mouse lemur individual variables explaining variation in the occurrence patterns of parasite and microbiota significantly. Our results provide new hypothesis for interactions between and among parasites and microbiota to be tested further with experimental studies.

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“…DNA metabarcoding of fecal samples (i.e., molecular scatology) has been employed to understand several types of data in mammalian taxa, including the genotype of the individual (De Barba et al, 2017), its diet (De Barba et al, 2014;Quemere et al, 2013;Shehzad et al, 2012;Soininen et al, 2013;Zeale, Butlin, Barker, Lees, & Jones, 2011), and its pathogens/parasites (Aivelo, Laakkonen, & Jernvall, 2016;Aivelo, Medlar, Löytynoja, Laakkonen, & Jernvall, 2015;Springer et al, 2017). While most previous studies generally investigated only a single attribute of a population, combining assays for multiple classes of data for a species in a metabarcoding study (i.e., multifaceted DNA metabarcoding; MDM) would likely be an efficient approach to gain an in-depth picture of the diverse ecological interactions of a target species.…”

Section: Introductionmentioning

confidence: 99%

Multifaceted DNA metabarcoding: Validation of a noninvasive, next‐generation approach to studying bat populations

Swift

Lance

Guan

et al. 2018

Evolutionary Applications

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As multiple species of bats are currently experiencing dramatic declines in populations due to white‐nose syndrome (WNS) and other factors, conservation managers have an urgent need for data on the ecology and overall status of populations of once‐common bat species. Standard approaches to obtain data on bat populations often involve capture and handling, requiring extensive expertise and unavoidably resulting in stress to the bats. New methods to rapidly obtain critical data are needed that minimize both the stress on bats and the spread of WNS. Guano provides a noninvasive source of DNA that includes information from the bat, but also dietary items, parasites, and pathogens. DNA metabarcoding is a high‐throughput, DNA‐based identification technique to assess the biodiversity of environmental or fecal samples. We investigated the use of multifaceted DNA metabarcoding (MDM), a technique combining next‐generation DNA sequencing (NGS), DNA barcodes, and bioinformatic analysis, to simultaneously collect data on multiple parameters of interest (bat species composition, individual genotype, sex ratios, diet, parasites, and presence of WNS) from fecal samples using a single NGS run. We tested the accuracy of each MDM assay using samples in which these parameters were previously determined using conventional approaches. We found that assays for bat species identification, insect diet, parasite diversity, and genotype were both sensitive and accurate, the assay to detect WNS was highly sensitive but requires careful sample processing steps to ensure the reliability of results, while assays for nectivorous diet and sex showed lower sensitivity. MDM was able to quantify multiple data classes from fecal samples simultaneously, and results were consistent whether we included assays for a single data class or multiple data classes. Overall, MDM is a useful approach that employs noninvasive sampling and a customizable suite of assays to gain important and largely accurate information on bat ecology and population dynamics.

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Population- and Individual-Level Dynamics of the Intestinal Microbiota of a Small Primate

Cited by 48 publications

References 51 publications

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

Parasite-microbiota interactions potentially affect intestinal communities in wild mammals

Multifaceted DNA metabarcoding: Validation of a noninvasive, next‐generation approach to studying bat populations

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