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

Andrea Springer, Claudia Fichtel, Gabriel A. Al-Ghalith, Flávia Koch, Katherine R. Amato, Jonathan B. Clayton, Dan Knights, Peter M. Kappeler

Research output: Contribution to journalArticlepeer-review

31 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)5732-5745
Number of pages14
JournalEcology and Evolution
Volume7
Issue number15
DOIs
StatePublished - Aug 2017

Bibliographical note

Funding Information:
We thank the equipe of the Kirindy field station, especially Rodin Rasoloarison and L?onard Razafimanantsoa, and the Malagasy Minist?re de l'Environnement et des Eaux et For?ts, the D?partement Biologie Animale de l'Universit? d'Antananarivo, and the Centre National de Formation, d'Etudes et de Recherche en Environnement et Foresterie for supporting and authorizing our long-term research in Kirindy. This research was funded by the Deutsche Forschungsgemeinschaft (Ka1082/29-1), the Primate Microbiome Project (www.primatemicrobiome.org), and the German Primate Center and has profited from discussions in the research group ?Sociality and Health in Primates? (FOR2136). This work was supported by the National Institutes of Health through a PharmacoNeuroImmunology Fellowship (NIH/NIDA T32 DA007097-32) awarded to J.B.C. We thank Christina Valeri and James Collins at the University of Minnesota VDL for assistance with shipping permits.

Keywords

  • Firmicutes-Bacteroidetes ratio
  • Propithecus
  • diet
  • folivory
  • intestinal microbiota
  • seasonality

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