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Metabarcoding Gastrointestinal Nematodes in Sympatric Endemic and Nonendemic Species in Ranomafana National Park, Madagascar

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Abstract

Sympatric species are known to host the same parasites species. Nevertheless, surveys examining parasite assemblages in sympatric species are rare. To understand how parasite assemblages in sympatric host species differ in a given locality, we used a noninvasive identification method based on high-throughput sequencing. We collected fecal samples from sympatric species in Ranomafana National Park, Madagascar, from September to December in 2010, 2011, and 2012 and identified their parasites by metabarcoding, sequencing a region of the small ribosomal subunit (18S) gene. Our survey included 11 host species, including endemic primates, rodents, frogs, gastropods, and nonendemic rats and dogs. We collected 872 samples, of which 571 contained nematodes and 249 were successfully sequenced. We identified nine putative species of parasites, although their correspondence to actual parasite species is not clear as the resolution of the marker gene differs between nematode clades. For the host species that we successfully sampled with 10 or more positive occurrences of nematodes, i.e., mouse lemurs (Microcebus rufus), black rats (Rattus rattus), and frogs (Anura), the parasite assemblage compositions differed significantly among host species, sampling sites, and sampling years. Our metabarcoding method shows promise in interrogating parasite assemblages in sympatric host species and our results emphasize the importance of choosing marker regions for parasite identification accuracy.

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Acknowledgments

We thank the handling editor and two anonymous reviewers for their valuable comments. We also thank Eric Hoberg, Holly Bik and three anonymous reviewers for their comments on the previous drafts of this article. We thank Madagascar National Parks, Madagascar Institute pour la Conservation des Ecosystèmes Tropicaux, and the Institute for the Conservation of Tropical Environments and research station Centre Valbio for logistical help and facilitation of research. Victor Rasendry, Herman Rafalinirina, Hannah Price, Kendall Harris, and Kelsey DeZalia helped with sample collection in the field and Anu Näreaho, Jukka T. Lehtonen, and Carina Holmberg gave us additional nematode specimens. Ritva Rice, Raija Savolainen, and Agnes Viherä assisted with the laboratory work. We also thank Voitto Haukisalmi for helpful comments. Funding was provided by Suoma Loimaranta-Airila Fund, Science Foundation of University of Helsinki, Otto A. Malm Fund, and Oskar Öflunds Foundation to T. Aivelo and Academy of Finland to J. Jernvall.

T. Aivelo, J. Jernvall, and J. Laakkonen designed the overall study and data collection. Samples were collected and amplified by T. Aivelo. A. Medlar, and A. Löytynoja developed the sequence analysis method. All authors participated in analysis of the results. T. Aivelo wrote the first draft with major contributions from A. Medlar. All authors commented on the draft and approved the final article.

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Authors and Affiliations

  1. Institute of Biotechnology, University of Helsinki, 00014, Helsinki, Finland

    Tuomas Aivelo, Alan Medlar, Ari Löytynoja & Jukka Jernvall

  2. Department of Biosciences, University of Helsinki, 00014, Helsinki, Finland

    Tuomas Aivelo

  3. Department of Evolutionary Biology and Environmental Studies, University of Zürich, CH-8057, Zürich, Switzerland

    Tuomas Aivelo

  4. Department of Veterinary Biosciences, University of Helsinki, 00014, Helsinki, Finland

    Juha Laakkonen

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  1. Tuomas Aivelo
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  2. Alan Medlar
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Correspondence to Tuomas Aivelo.

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Aivelo, T., Medlar, A., Löytynoja, A. et al. Metabarcoding Gastrointestinal Nematodes in Sympatric Endemic and Nonendemic Species in Ranomafana National Park, Madagascar. Int J Primatol 39, 49–64 (2018). https://doi.org/10.1007/s10764-017-0010-x

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