The population genetics of the causative agent of snake fungal disease indicate recent introductions to the USA

Abstract

Snake fungal disease (SFD; ophidiomycosis), caused by the pathogen Ophidiomyces ophiodiicola (Oo), has been documented in wild snakes in North America and Eurasia, and is considered an emerging disease in the eastern United States of America. However, a lack of historical disease data has made it challenging to determine whether Oo is a recent arrival to the USA or whether SFD emergence is due to other factors. Here, we examined the genomes of 82 Oo strains to determine the pathogen’s history in the eastern USA. Oo strains from the USA formed a clade (Clade II) distinct from European strains (Clade I), and molecular dating indicated that these clades diverged too recently (approximately 2,000 years ago) for transcontinental dispersal of Oo to have occurred via natural snake movements across Beringia. A lack of nonrecombinant intermediates between clonal lineages in Clade II indicates that Oo has actually been introduced multiple times to North America from an unsampled source population, and molecular dating indicates that several of these introductions occurred within the last few hundred years. Molecular dating also indicated that the most common Clade II clonal lineages have expanded recently in the USA, with time of most recent common ancestor mean estimates ranging from 1985 to 2007 CE. The presence of Clade II in captive snakes worldwide demonstrates a potential mechanism of introduction and highlights that additional incursions are likely unless action is taken to reduce the risk of pathogen translocation and spillover into wild snake populations.

Ophiodimyces ophiodiicola, Etiologic Agent of Snake Fungal Disease, in Europe since Late 1950s

“…The significance of both clades existing in Europe will require further investigations. In spite of the absence in the United States of any strain proven to belong to the clade from Europe, introduction cannot be completely ruled out (14). In an alternative scenario, the clade from North America might have been introduced into Europe before the 1950s.…”

Ophidiomyces ophidiicola detection and infection: a global review on a potential threat to the world’s snake populations

“…Therefore, to better understand the distribution, evolution, and origins of Oo, it is advisable to continue with the molecular phylogenetic analysis of new isolates, especially from those areas where data are still lacking. This may be carried out following phylogenetics methods such as those performed by Franklinos et al (2017) and Sun et al (2021), and the methods used by Ladner et al (2022).…”

“…Considering that Oo might be spread by animate and inanimate vectors, it is recommended that the authorities monitor compliance in terms of unauthorized manipulation or collection of wild snakes, as well as the release of captive snakes in the wild. This is needed to limit transmission of the pathogen in new habitats and snake populations (see Ladner et al 2022), especially those small in size and/or occurring in a restricted area. At the same time, captive snake holders and recovery centers should always consider disease risk prevention and assessment and should perform a quarantine of at least 90 days and a microbiological screening for Oo when a new individual enters the collection (Rivera 2019;Rossi 2019).…”

“…Whether or not Oo is now ubiquitous in terms of distribution, this fungus has probably been present for an indefinitely long time outside its native range. Indeed, a very recent molecular-based study suggests that the fungus has been introduced to North America on multiple occasions since the 18 th century (see Ladner et al 2022).…”

“…A recent characterization of some isolates highlighted that all strains from wild USA snakes belong to Clade 2, that seems to originate itself from the older European Clade 1 (Ladner et al 2022). Moreover, Oo strains from Taiwan, as well as, from captive snakes from Australia, Europe and North America were grouped within the outgroup Clade 3 or within different lineages of Clade 2 also found in Eastern USA wild snakes, suggesting a spillover via pet trade (Ladner et al 2022).…”