skip to main content

Title: Cryptic diversity of a widespread global pathogen reveals expanded threats to amphibian conservation
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 Bd ASIA3, that appears to be widespread in Southeast Asia. This lineage co-occurs with the global panzootic lineage ( Bd GPL) in multiple localities. Additionally, we shed light on the global distribution of Bd GPL and highlight the expanded range of another lineage, Bd CAPE. 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.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; ; ; ; ; « less
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Chytridiomycosis, caused by the fungusBatrachochytrium dendrobatidis(Bd), is the emerging infectious disease implicated in recent population declines and extinctions of amphibian species worldwide.Bdstrains from regions of disease‐associated amphibian decline to date have all belonged to a single, hypervirulent clonal genotype (BdGPL). However, earlier studies in the Atlantic Forest of southeastern Brazil detected a novel, putatively enzootic lineage (Bd‐Brazil), and indicated hybridization betweenBdGPLandBd‐Brazil. Here, we characterize the spatial distribution and population history of these sympatric lineages in the Brazilian Atlantic Forest. To investigate the genetic structure ofBdin this region, we collected and genotypedBdstrains along a 2400‐km transect of the Atlantic Forest.Bd‐Brazil genotypes were restricted to a narrow geographic range in the southern Atlantic Forest, whileBdGPLstrains were widespread and largely geographically unstructured.Bdpopulation genetics in this region support the hypothesis that the recently discovered Brazilian lineage is enzootic in the Atlantic Forest of Brazil and thatBdGPLis a more recently expanded invasive. We collected additional hybrid isolates that demonstrate the recurrence of hybridization between panzootic and enzootic lineages, thereby confirming the existence of a hybrid zone in the Serra da Graciosa mountain range of Paraná State. Our field observations suggest thatBdGPLmay be more infective towards native Brazilian amphibians, and potentially more effective at dispersing across a fragmented landscape. We also provide further evidence of pathogen translocations mediated by the Brazilian ranaculture industry with implications for regulations and policies on global amphibian trade.

    more » « less
  2. Abstract

    Phenotypes are the target of selection and affect the ability of organisms to persist in variable environments. Phenotypes can be influenced directly by genes and/or by phenotypic plasticity. The amphibian‐killing fungusBatrachochytrium dendrobatidis(Bd) has a global distribution, unusually broad host range, and high genetic diversity. Phenotypic plasticity may be an important process that allows this pathogen to infect hundreds of species in diverse environments. We quantified phenotypic variation of nine Bd genotypes from two Bd lineages (Global Pandemic Lineage [GPL] and Brazil) and a hybrid (GPL‐Brazil) grown at three temperatures (12, 18 and 24°C). We measured five functional traits including two morphological traits (zoospore and zoosporangium sizes) and three life history traits (carrying capacity, time to fastest growth and exponential growth rate) in a phylogenetic framework. Temperature caused highly plastic responses within each genotype, with all Bd genotypes showing phenotypic plasticity in at least three traits. Among genotypes, Bd generally showed the same direction of plastic response to temperature: larger zoosporangia, higher carrying capacity, longer time to fastest growth and slower exponential growth at lower temperatures. The exception was zoospore size, which was highly variable. Our findings indicate that Bd genotypes have evolved novel phenotypes through plastic responses to temperature over very short timescales. High phenotypic variability likely extends to other traits and may facilitate the large host range and rapid spread of Bd.

    more » « less
  3. Abstract

    Determining how genetic diversity is structured between populations that span the divergence continuum from populations to biological species is key to understanding the generation and maintenance of biodiversity. We investigated genetic divergence and gene flow in eight lineages of birds with a trans‐Beringian distribution, where Asian and North American populations have likely been split and reunited through multiple Pleistocene glacial cycles. Our study transects the speciation process, including eight pairwise comparisons in three orders (ducks, shorebirds and passerines) at population, subspecies and species levels. Using ultraconserved elements (UCEs), we found that these lineages represent conditions from slightly differentiated populations to full biological species. Although allopatric speciation is considered the predominant mode of divergence in birds, all of our best divergence models included gene flow, supporting speciation with gene flow as the predominant mode in Beringia. In our eight lineages, three were best described by a split‐migration model (divergence with gene flow), three best fit a secondary contact scenario (isolation followed by gene flow), and two showed support for both models. The lineages were not evenly distributed across a divergence space defined by gene flow (M) and differentiation (FST), instead forming two discontinuous groups: one with relatively shallow divergence, no fixed single nucleotide polymorphisms (SNPs), and high rates of gene flow between populations; and the second with relatively deeply divergent lineages, multiple fixed SNPs, and low gene flow. Our results highlight the important role that gene flow plays in avian divergence in Beringia.

    more » « less
  4. null (Ed.)
    Chytridiomycosis, an infectious disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), poses an imminent conservation threat. The global spread of Bd has led to mass mortality events in many amphibian species, resulting in at least 90 species' extinctions to date. Exposure to Bd metabolites (i.e. non-infectious antigenic chemicals released by Bd) partially protects frogs during subsequent challenges with live Bd, suggesting its use as a prophylactic treatment and potential vaccine. However, we do not know whether Bd metabolite exposure protects against strains beyond the one used for treatment. To address this knowledge gap, we conducted a 3 × 2 experiment where we exposed adult Cuban treefrogs, Osteopilus septentrionalis , to one of three treatments (Bd metabolites from California-isolated strain JEL-270, Panamá-isolated strain JEL-419, or an artificial spring water control) and then challenged individuals with live Bd from either strain. We found that exposure to Bd metabolites from the California-isolated strain significantly reduced Bd loads of frogs challenged with the live Panamá-isolated strain, but no other treatments were found to confer protective effects. These findings demonstrate asymmetric cross-protection of a Bd metabolite prophylaxis and suggest that work investigating multiple, diverse strains is urgently needed. 
    more » « less
  5. Abstract

    Nitric oxide (NO) is a ubiquitous gaseous messenger, but we know little about its early evolution. Here, we analyzed NO synthases (NOS) in four different species of placozoans—one of the early-branching animal lineages. In contrast to other invertebrates studied,TrichoplaxandHoilungiahave three distinct NOS genes, including PDZ domain-containing NOS. Using ultra-sensitive capillary electrophoresis assays, we quantified nitrites (products of NO oxidation) andl-citrulline (co-product of NO synthesis froml-arginine), which were affected by NOS inhibitors confirming the presence of functional enzymes inTrichoplax. Using fluorescent single-molecule in situ hybridization, we showed that distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions ofTrichoplax. These data suggest both the compartmentalized release of NO and a greater diversity of cell types in placozoans than anticipated. NO receptor machinery includes both canonical and novel NIT-domain containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors. Thus, althoughTrichoplaxandHoilungiaexemplify the morphologically simplest free-living animals, the complexity of NO-cGMP-mediated signaling in Placozoa is greater to those in vertebrates. This situation illuminates multiple lineage-specific diversifications of NOSs and NO/nitrite/nitrate sensors from the common ancestor of Metazoa and the preservation of conservative NOS architecture from prokaryotic ancestors.

    more » « less