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Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species

  • Plant-microbe-animal interactions - Original research
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Abstract

Recent studies suggest that variation in diet across time and space results in changes in the mammalian gut microbiota. This variation may ultimately impact host ecology by altering nutritional status and health. Wild animal populations provide an excellent opportunity for understanding these interactions. However, compared to clinical studies, microbial research targeting wild animals is currently limited, and many published studies focus only on a single population of a single host species. In this study we utilize fecal samples from two species of howler monkey (Alouatta pigra and A. palliata) collected at four sites to investigate factors influencing the gut microbiota at three scales: taxonomic (host species), ecosystemic (forest type), and local (habitat disturbance/season). The results demonstrate that the effect of host species on the gut microbiota is stronger than the effect of host forest type, which is stronger than the effect of habitat disturbance or seasonality. Nevertheless, within host species, gut microbiota composition differs in response to forest type, habitat disturbance, and season. Variations in the effect size of these factors are associated both with host species and environment. This information may be beneficial for understanding ecological and evolutionary questions associated with Mesoamerican howler monkeys, as well as determining conservation challenges facing each species. These mechanisms may also provide insight into the ecology of other species of howler monkeys, non-human primates, and mammals.

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Acknowledgments

We would like to thank A. Estrada and the Universidad Nacional Autónoma de México, and Alvaro Molina and the Comité de Manejo Colaborativo del Parque Nacional Volcán Maderas for logistic support in the field, as well as B. Wilkinson and S. Van Belle. Funding was provided by a National Geographic Waitt grant (W139-10), an NSF Graduate Research Fellowship, and a Univ. of IL Dissertation Travel Grant to KRA, as well as the Earth Microbiome Project and NSF grant #0935347 (HOMINID) to SRL, RMS, BAW, and KEN. Thanks to INIFAP and M.C. Antonio Sanchez for permission to work in El Tormento, Mexico. Thanks to CONANP, SEMARNAT, and SAGARPA in Mexico, MARENA in Nicaragua, the Ministerio de Salud in Costa Rica, and the CDC in the US for permits and logistic support. We also appreciate the comments of two anonymous reviewers.

Data accessibility

Raw sequence data can be found in the European Bioinformatics Institute (EBI) nucleotide database under Accession Number ERP012937.

Author contributions

KRA conceived of and designed the project, provided funding, conducted fieldwork, analyzed the data and wrote the manuscript. RMM, NR, and MRS conducted fieldwork and wrote the manuscript. FBC conducted fieldwork. GH, GG, JG, EL, LW, and AL conducted laboratory analyses of samples. EM, MGDB, RMS, BW, KN, RK, and SRL provided funding, logistical support and manuscript revisions.

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Correspondence to Katherine R. Amato.

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Communicated by Joanna E. Lambert.

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Amato, K.R., Martinez-Mota, R., Righini, N. et al. Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species. Oecologia 180, 717–733 (2016). https://doi.org/10.1007/s00442-015-3507-z

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