Abstract
Habitat fragmentation and infectious diseases threaten wildlife globally, but the interactions of these threats are poorly understood. For instance, while habitat fragmentation can impact genetic diversity at neutral loci, the impacts on disease-relevant loci are less well-studied. We examined the effects of habitat fragmentation in Brazil’s Atlantic Forest on amphibian genetic diversity at an immune locus related to antigen presentation and detection (MHC IIB Exon 2). We used a custom high-throughput assay to sequence a fragment of MHC IIB and quantified Batrachochytrium dendrobatidis (Bd) infections in six frog species in two Atlantic Forest regions. Habitat fragmentation was associated with genetic erosion at MHC IIB Exon 2. This erosion was most severe in forest specialists. Significant Bd infections were detected only in one Atlantic Forest region, potentially due to relatively higher elevation. In this region, forest specialists showed an increase in both Bd prevalence and infection loads in fragmented habitats. Reduced population-level MHC IIB diversity was associated with increased Bd infection risk. On the individual level, MHC IIB heterozygotes exhibited a trend toward reduced Bd infection risk, although this was marginally non-significant. Our results suggest that habitat fragmentation increases Bd infection susceptibility in amphibians, mediated at least in part through erosion of immunogenetic diversity. Our findings have implications for management of fragmented populations in the face of emerging infectious diseases.
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Data availability
The data that support the findings of this study are openly available in the supplementary material and GenBank (ddRAD data: SRA accessions SAMN25158801, SAMN25182090; MHC sequences: GenBank accessions OM362104 - OM362229).
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Acknowledgments
The authors acknowledge a number of Indigenous Lands on which this work was performed. Fieldwork was performed on pre-colonization territories of Indigenous Peoples including the Tupi-Guarani and Pataxó Peoples; analyses and writing by AMB and TYJ were performed on traditional territories of Indigenous Peoples including the Ojibwe, Odawa, and Bodéwadmi Peoples, and additional work by AMB was performed on Haudenosaunee Land. We thank Katherine Crocker for generous education that inspired and informed this Indigenous Land Acknowledgment. The authors would like to acknowledge Meghan Duffy, the Zamudio Lab, and the Cornell EEID Journal Club for feedback on an earlier version of the manuscript; Renato Martins, Vinicius Hansser, Rafael Benetti, Joice Ruggeri, João Roberto, Leildo Carilo, Cesar Alexandre, Diego Alejandro, Felipe Andrade, Isa Haga, Lucas Forti, Anna Barbara Bella Sanches Forti, Adolfo Delgado, Carlos Henrique Luz Nunes de Almeida, and Sandra Goutte for assistance in the field; Mirco Solé, Victor Dill, Tadeu Medeiros, Euvaldo Junior, and Caio Vinícius for assistance with field logistics; Kevin Flesher and the Michelin Reserve staff; and the generous Brazilian farmers who accommodated our teams and permitted access to land.
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This work was supported by the National Science Foundation (NSF OISE-1159513 to TYJ), the Brazilian National Council for Scientific and Technological Development (CNPq 300980/2014-0 to LFT), the University of Michigan Department of Ecology and Evolutionary Biology Block Grant (to AMB), and the University of Michigan Rackham International Research Award (to AMB).
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AMB and TYJ conceived of the project; AMB, CGB, LFT, and TYJ performed the fieldwork; AMB and RAC performed the lab work; AMB and KRA analyzed the data; AMB, KRA, and CGB produced the figures; AMB wrote the paper; all authors contributed to reviewing and revising the paper.
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Belasen, A.M., Amses, K.R., Clemons, R.A. et al. Habitat fragmentation in the Brazilian Atlantic Forest is associated with erosion of frog immunogenetic diversity and increased fungal infections. Immunogenetics 74, 431–441 (2022). https://doi.org/10.1007/s00251-022-01252-x
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DOI: https://doi.org/10.1007/s00251-022-01252-x