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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.

Author information

Authors and Affiliations

  1. Department of Anthropology, Northwestern University, Evanston, USA

    Katherine R. Amato

  2. Department of Anthropology, University of Colorado, Boulder, Boulder, CO, USA

    Steven R. Leigh

  3. BioFrontiers Institute, University of Colorado Boulder, Boulder, CO, USA

    Katherine R. Amato & Elijah Lovelace

  4. Department of Anthropology, University of Illinois, Urbana, IL, USA

    Rodolfo Martinez-Mota, Nicoletta Righini, Melissa Raguet-Schofield & Rebecca M. Stumpf

  5. Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz, Mexico

    Nicoletta Righini

  6. Department of Anthropology, Colorado State University, Fort Collins, CO, USA

    Melissa Raguet-Schofield

  7. Dipartimento di Scienze della Vita e dell’Ambiente, Sezione di Neuroscienze e Antropologia, Università di Cagliari, Cagliari, Italy

    Fabiana Paola Corcione & Elisabetta Marini

  8. Department of Pediatrics, University of California, San Diego, San Diego, CA, USA

    Greg Humphrey, Grant Gogul, James Gaffney & Rob Knight

  9. Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ, USA

    LaShanda Williams

  10. Department of Medicine, New York University, New York, NY, USA

    Albert Luong & Maria Gloria Dominguez-Bello

  11. Institute for Genomic Biology, University of Illinois, Urbana, IL, USA

    Rebecca M. Stumpf & Bryan White

  12. Department of Animal Sciences, University of Illinois, Urbana, IL, USA

    Bryan White

  13. J. Craig Venter Institute, Rockville, MD, USA

    Karen E. Nelson

Authors
  1. Katherine R. Amato
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  2. Rodolfo Martinez-Mota
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  4. Melissa Raguet-Schofield
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  6. Elisabetta Marini
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  13. Maria Gloria Dominguez-Bello
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Corresponding author

Correspondence to Katherine R. Amato.

Additional information

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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  • DOI: https://doi.org/10.1007/s00442-015-3507-z

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