Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade

Abstract

Global amphibian declines are linked with the presence of specific, highly virulent genotypes of the emerging fungal disease chytridiomycosis caused by Batrachochytrium dendrobatidis (Bd) known as the global panzootic lineage (Bd-GPL). The global trade in amphibians for human consumption is suspected to have facilitated emergence of the disease, but evidence to support this is largely lacking. Here, we investigated the role the Lithobates catesbeianus (North American bullfrog) trade in spreading Bd genotypes by comparing strains associated with L. catesbeianus to a global panel using 36 sequenced loci from multiple chromosomal regions. Most bullfrogs were infected with Bd-GPL genotypes, but we also detected novel, highly divergent Bd genotypes (Bd-Brazil) from a live bullfrog in a US market and from native Brazilian anurans in the Atlantic Forest where bullfrogs are widely farmed. Sexual reproduction was also detected for the first time in Bd in the form of a hybrid genotype between the Bd-GPL and Bd-Brazil lineages in the Atlantic Forest. Despite the demonstration that ribosomal RNA types in Bd fail to undergo concerted evolution (over 20 sequence types may be found in a single strain), the Bd-GPL and Bd-Brazil lineages form largely separate clusters of related internal transcribed spacer (ITS) RNA sequences. Using ITS sequences, we then demonstrate the presence of Bd-Brazil in Japan, primarily on invasive L. catesbeianus. The finding that Bd is capable of sexual reproduction between panzootic and endemic genotypes emphasizes the risk of international wildlife trade as a source of additional Bd epizootics owing to hybridization.

Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic

“…[45]. This previous research prompted several researchers to propose that the trade of bullfrogs was a primary driver of the spread of Bd [43,44]. However, recent evidence suggests that crayfish are also hosts of Bd [46].…”

Pathogenic fungus in feral populations of the invasive North American bullfrog in Argentina

“…The chytrid fungus Batrachochytrium dendrobatidis (Bd) (Chytridiomycetes: Ryzophydiales) (2) has been recognized as responsible for mass mortalities or population extinctions of numerous anuran species in different continents (e.g., 3,4,5 and citations therein). There is evidence that legal and illegal trade in amphibians as pets, food and for bio-control is one of the reasons for the spread of Bd (6,7,8,9).…”

First detection of the amphibian chytrid fungus (Batrachochytridium dendrobatidis) in free- living anuran populations in Greece

“…The role of anthropogenic transmission, through trade of bullfrogs, of the chytrid fungus has been discussed (Schloegel et al 2012, Rodriguez et al 2013. American bullfrogs are not considered a delicacy in ΠΕΚΕ 2016, 67(4) of the public authorities, naturalist associations, and local communities in order to prevent the further spread of the fungus in other wetlands.…”

“…Forthcoming field research should include a larger number of wetlands with variable habitats, a larger number of samples and amphibian anuran species-especially endemic species. The role of the alien American bullfrog (L. catesbeianus), a known carrier of the amphibian chytrid fungus (Daszak et al 2004, Schloegel et al 2010, Schloegel et al 2012, should be evaluated in the local decrease of the population of the endemic Cretan water frog (P. cretensis) (Mantziou et al 1999). …”