Biodiversity loss is one major outcome of human-mediated ecosystem disturbance. One way that humans have triggered wildlife declines is by transporting disease-causing agents to remote areas of the world. Amphibians have been hit particularly hard by disease due in part to a globally distributed pathogenic chytrid fungus (Batrachochytrium dendrobatidis [Bd]). Prior research has revealed important insights into the biology and distribution of Bd; however, there are still many outstanding questions in this system. Although we know that there are multiple divergent lineages of Bd that differ in pathogenicity, we know little about how these lineages are distributed around the world and where lineages may be coming into contact. Here, we implement a custom genotyping method for a global set of Bd samples. This method is optimized to amplify and sequence degraded DNA from noninvasive skin swab samples. We describe a divergent lineage of Bd, which we call BdASIA3, that appears to be widespread in Southeast Asia. This lineage co-occurs with the global panzootic lineage (BdGPL) in multiple localities. Additionally, we shed light on the global distribution of BdGPL and highlight the expanded range of another lineage, BdCAPE. Finally, we argue that more monitoring needs to take place where Bd lineages are coming into contact and where we know little about Bd lineage diversity. Monitoring need not use expensive or difficult field techniques but can use archived swab samples to further explore the history-and predict the future impacts-of this devastating pathogen.

College of Forestry Southwest Forestry University Kunming 650224 Yunnan China

Department of Biodiversity Conservation El Colegio de la Frontera Sur San Cristobal de las Casas Chiapas 29290 México

Department of Biological Sciences Florida International University Miami FL 33199

Department of Biological Sciences University of Pittsburgh Pittsburgh PA 15260

Department of Biology San Francisco State University San Francisco CA 94132

Department of Biology University of Massachusetts Boston Boston MA 02125

Department of Biology University of Nevada Reno NV 89557

Department of Ecology and Evolution University of Arizona Tucson AZ 85721

Department of Ecology and Evolution University of Kansas Lawrence KS 66045

Department of Ecology Evolution and Marine Biology University of California Santa Barbara CA 93106

Department of Environmental Science Policy and Management University of California Berkeley CA 94720

Department of Environmental Science Policy and Management University of California Berkeley CA 94720;

Department of Evolution and Ecology University of California Davis CA 95616

Department of Herpetology California Academy of Sciences San Francisco CA 94118

Department of Oceanography University of Hawai'i at Manoa Honolulu HI 96822

Department of Pathology Bacteriology and Avian Diseases Ghent University 9820 Merelbeke Belgium

Department of Vertebrate Zoology National Museum of Natural History Smithsonian Institution Washington DC 20560

Environmental Sciences Graduate Program Oregon State University Corvallis OR 97331

Florida Museum of Natural History University of Florida Gainesville FL 32601

Institute of Parasitology Czech Academy of Sciences 370 05 Ceske Budejovice Czech Republic

Museo Nacional de Ciencias Naturales Consejo Superior de Investigaciones Cientificas 28006 Madrid Spain

Museum of Vertebrate Zoology University of California Berkeley CA 94720

One Health Research Group The University of Melbourne Werribee VIC 3030 Australia

Reptile Amphibian and Fish Conservation 6525 ED Nijmegen The Netherlands

Research Unit of Biodiversity CSIC Universidad de Oviedo Gobierno del Principado de Asturias E 33600 Mieres Spain

School of Environment and Sciences Griffith University Gold Coast QLD 4215 Australia

School of Life Sciences University of Nevada Las Vegas NV 89154

Sierra Nevada Aquatic Research Laboratory University of California Mammoth Lakes CA 93546

Unidad de Genómica Avanzada Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional Irapuato Guanajuato CP36824 México

University of Kansas Biodiversity Institute University of Kansas Lawrence KS 66045

Vietnam National Museum of Nature Vietnam Academy of Science and Technology Hanoi Vietnam

Zobrazit více v PubMed

Jones K. E., et al. , Global trends in emerging infectious diseases. Nature 451, 990–993 (2008). PubMed PMC

Daszak P., Cunningham A. A., Hyatt A. D., Emerging infectious diseases of wildlife–Threats to biodiversity and human health. Science 287, 443–449 (2000). PubMed

Fisher M. C., Garner T. W. J., The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biol. Rev. 21, 2–9 (2007).

Foley J., Clifford D., Castle K., Cryan P., Ostfeld R. S., Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats. Conserv. Biol. 25, 223–231 (2011). PubMed

Skerratt L. F., et al. , Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134 (2007).

Wake D. B., Vredenburg V. T., Colloquium paper: Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl. Acad. Sci. U.S.A. 105 (suppl. 1), 11466–11473 (2008). PubMed PMC

Longcore J. E., Pessier A. P., Nichols D. K., Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to Amphibians. Mycologia 91, 219–227 (1999).

Voyles J., et al. , Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326, 582–585 (2009). PubMed

Vredenburg V. T., Knapp R. A., Tunstall T. S., Briggs C. J., Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl. Acad. Sci. U.S.A. 107, 9689–9694 (2010). PubMed PMC

Briggs C. J., Knapp R. A., Vredenburg V. T., Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. U.S.A. 107, 9695–9700 (2010). PubMed PMC

Reeder N. M. M., Pessier A. P., Vredenburg V. T., A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS One 7, e33567 (2012). PubMed PMC

Yap T. A., Koo M. S., Ambrose R. F., Vredenburg V. T., Introduced bullfrog facilitates pathogen invasion in the western United States. PLoS One 13, e0188384 (2018). PubMed PMC

Schloegel L. M., et al. , The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Anim. Conserv. 13, 53–61 (2010).

O’Hanlon S. J., et al. , Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018). PubMed PMC

Rosenblum E. B., et al. , Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc. Natl. Acad. Sci. U.S.A. 110, 9385–9390 (2013). PubMed PMC

Jenkinson T. S., et al. , Amphibian-killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Mol. Ecol. 25, 2978–2996 (2016). PubMed

Farrer R. A., et al. , Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl. Acad. Sci. U.S.A. 108, 18732–18736 (2011). PubMed PMC

Schloegel L. M., et al. , Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol. Ecol. 21, 5162–5177 (2012). PubMed

Greenspan S. E., et al. , Hybrids of amphibian chytrid show high virulence in native hosts. Sci. Rep. 8, 9600 (2018). PubMed PMC

Boyle D. G., Boyle D. B., Olsen V., Morgan J. A., Hyatt A. D., Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Organ. 60, 141–148 (2004). PubMed

Byrne A. Q., et al. , Unlocking the story in the swab: A new genotyping assay for the amphibian chytrid fungus Batrachochytrium dendrobatidis. Mol. Ecol. Resour. 17, 1283–1292 (2017). PubMed

Bletz M. C., et al. , Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar. Sci. Rep. 5, 8633 (2015). PubMed PMC

Grenfell B. T., et al. , Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327–332 (2004). PubMed

Miller C. A., et al. , Distribution modeling and lineage diversity of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in a central African amphibian hotspot. PLoS One 13, e0199288 (2018). PubMed PMC

Soto‐Azat C., Clarke B. T., Poynton J. C., Cunningham A. A., Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Divers. Distrib. 16, 126–131 (2010).

Kolby J. E., Padgett-Flohr G. E., Field R., Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco National Park, Honduras. Dis. Aquat. Organ. 92, 245–251 (2010). PubMed

Voyles J., et al. , Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science 359, 1517–1519 (2018). PubMed

Knapp R. A., et al. , Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proc. Natl. Acad. Sci. U.S.A. 113, 11889–11894 (2016). PubMed PMC

Swei A., et al. , Is chytridiomycosis an emerging infectious disease in Asia? PLoS One 6, e23179 (2011). PubMed PMC

Schloegel L. M., et al. , Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol. Conserv. 142, 1420–1426 (2009).

Mutnale M. C., et al. , Enzootic frog pathogen Batrachochytrium dendrobatidis in Asian tropics reveals high ITS haplotype diversity and low prevalence. Sci. Rep. 8, 10125 (2018). PubMed PMC

Cheng T. L., Rovito S. M., Wake D. B., Vredenburg V. T., Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc. Natl. Acad. Sci. U.S.A. 108, 9502–9507 (2011). PubMed PMC

Rodriguez D., Becker C. G., Pupin N. C., Haddad C. F. B., Zamudio K. R., Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Mol. Ecol. 23, 774–787 (2014). PubMed

Burrowes P. A., De la Riva I., Unraveling the historical prevalence of the invasive chytrid fungus in the Bolivian Andes: Implications in recent amphibian declines. Biol. Invasions 19, 1781–1794 (2017).

Stamatakis A., RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). PubMed PMC

Zhang C., Rabiee M., Sayyari E., Mirarab S., ASTRAL-III: Polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19 (suppl. 6), 153 (2018). PubMed PMC