Host-associated helminth diversity and microbiome composition contribute to anti-pathogen defences in tropical frogs impacted by forest fragmentation

Author:

Neely Wesley J.12,Souza Kassia M. C.3ORCID,Martins Renato A.4,Marshall Vanessa M.1ORCID,Buttimer Shannon M.4,Brito de Assis Ananda5,Medina Daniel46ORCID,Whetstone Ross D.7,Lyra Mariana L.58,Ribeiro José Wagner5,Greenspan Sasha E.1ORCID,Haddad Célio F. B.5,Alves dos Anjos Luciano3,Becker C. Guilherme49ORCID

Affiliation:

1. Department of Biology, The University of Alabama , Tuscaloosa, AL 35487, USA

2. Department of Biology, Texas State University , San Marcos, TX 78666, USA

3. Departamento de Biologia e Zootecnia, Universidade Estadual Paulista, Ilha Solteira , São Paulo 15385-000, Brazil

4. Department of Biology, The Pennsylvania State University , University Park, PA 16803, USA

5. Department of Biodiversity and Aquaculture Center, Universidade Estadual Paulista , Rio Claro, São Paulo 13506-900, Brazil

6. Sistema Nacional de Investigación, SENACYT, City of Knowledge , Clayton, Panama, Republic of Panama

7. Department of Biology, University of Massachusetts Boston , Boston, MA 02125, USA

8. New York University Abu Dhabi , Abu Dhabi, UAE

9. One Health Microbiome Center, Center for Infectious Disease Dynamics, Ecology Institute, Huch Institutes of the Life Sciences, The Pennsylvania State University , University Park, PA 16803, USA

Abstract

Habitat fragmentation can negatively impact wildlife populations by simplification of ecological interactions, but little is known about how these impacts extend to host-associated symbiotic communities. The symbiotic communities of amphibians play important roles in anti-pathogen defences, particularly against the amphibian chytrid fungus Batrachochytrium dendrobatidis ( Bd ). In this study, we analyse the role of macroparasitic helminth communities in concert with microbial communities in defending the host against Bd infection within the context of forest fragmentation. We found that skin microbial and helminth communities are disrupted at fragmented habitats, while gut microbiomes appear more resilient to environmental change. We also detected potential protective roles of helminth diversity and anti-pathogen microbial function in limiting Bd infection. Microbial network analysis revealed strong patterns of structure in both skin and gut communities, with helminths playing central roles in these networks. We reveal consistent roles of microbial and helminth diversity in driving host–pathogen interactions and the potential implications of fragmentation on host fitness.

Funder

The University of Alabama

The National Science Foundation

Publisher

The Royal Society

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