Long‐term endemism of two highly divergent lineages of the amphibian‐killing fungus in the Atlantic Forest of Brazil

Abstract

The recent global spread of the amphibian-killing fungus [Batrachochytrium dendrobatidis (Bd)] has been closely tied to anthropogenic activities; however, regional patterns of spread are not completely understood. Using historical samples, we can test whether Bd was a spreading or endemic pathogen in a region within a particular time frame, because those two disease states provide different predictions for the regional demographic dynamics and population genetics of Bd. Testing historical patterns of pathogen prevalence and population genetics under these predictions is key to understanding the evolution and origin of Bd. Focusing on the Atlantic Forest (AF) of Brazil, we used qPCR assays to determine the presence or absence of Bd on 2799 preserved postmetamorphic anurans collected between 1894 and 2010 and used semi-nested PCRs to determine the frequency of rRNA ITS1 haplotypes from 52 samples. Our earliest date of detection was 1894. A mean prevalence of 23.9% over time and spatiotemporal patterns of Bd clusters indicate that Bd has been enzootic in the Brazilian AF with no evidence of regional spread within the last 116 years. ITS1 haplotypes confirm the long-term presence of two divergent strains of Bd (BdGPL and Bd-Brazil) and three spatiotemporally broad genetic demes within BdGPL, indicating that Bd was not introduced into southeast Brazil by the bullfrog trade. Our data show that the evolutionary history and pathogen dynamics of Bd in Brazil is better explained by the endemic pathogen hypothesis.

Overview of chytrid emergence and impacts on amphibians

“…Importantly, the long history of Bd-GPL in Brazil suggests additional vectors of pathogen introduction beyond the trade in amphibians. The lack of clear evidence of population declines, the long occurrence of Bd in Brazil and the low but steady prevalence of infection in Brazil suggests that these amphibians have evolved ways of coexisting with chytrid [83] and may produce insights for long-term planning in other regions of the world.…”

Jumping into a trap: high prevalence of chytrid fungus in the preferred microhabitats of a bromeliad-specialist frog

“…Likewise, Bd in the AF has a high genetic diversity (Schloegel et al 2012, Rosenblum et al 2013, Jenkinson et al 2016) and has been detected in more than 130 amphibian species (James et al 2015, Valencia-Aguilar et al 2015. Despite an association between Bd and amphibians of the AF dating back at least 100 yr (Rodriguez et al 2014), the role of the chytrid in amphibian population declines in this region is uncertain (Eterovick et al 2005, Lips et al 2005. Climatic variation, Bd strain, amphibian species/population susceptibility, microbiota assemblages on amphibian skin, and presence/density of non-amphibian carriers could all shape how the disease interacts with amphibians at any given site (Fisher et al 2009, Voyles et al 2011, Schmeller et al 2014.…”

Amphibian Alliance for Zero Extinction Sites in Chiapas and Oaxaca

“…However, the geographic origins of Bd are unclear. Authors have suggested that Bd could have spread from Africa (Weldon et al 2004), Asia (Goka et al 2009), North America (James et al 2009), or South America (Rodriguez et al 2014). This is particularly hard to determine given that there has been relatively sparse sampling for Bd in Africa and Asia, and most sampling that has occurred around the globe has been targeted in areas affected by disease (Fisher et al 2009a;Rosenblum et al 2010a,b).…”

“…38 Although chytridiomycosis has not yet reached South America via Panama, the disease has been reported from numerous locations across the continent. Bd is thought to have been introduced to multiple countries starting in 1970s , although Bd has been present in the Atlantic Forest of Brazil for at least a century and could possibly have originated there (Rodriguez et al 2014). …”