Evidence for emergence of an amphibian iridoviral disease because of human‐enhanced spread

Abstract

Our understanding of origins and spread of emerging infectious diseases has increased dramatically because of recent applications of phylogenetic theory. Iridoviruses are emerging pathogens that cause global amphibian epizootics, including tiger salamander (Ambystoma tigrinum) die-offs throughout western North America. To explain phylogeographical relationships and potential causes for emergence of western North American salamander iridovirus strains, we sequenced major capsid protein and DNA methyltransferase genes, as well as two noncoding regions from 18 geographically widespread isolates. Phylogenetic analyses of sequence data from the capsid protein gene showed shallow genetic divergence (< 1%) among salamander iridovirus strains and monophyly relative to available fish, reptile, and other amphibian iridovirus strains from the genus Ranavirus, suggesting a single introduction and radiation. Analysis of capsid protein sequences also provided support for a closer relationship of tiger salamander virus strains to those isolated from sport fish (e.g. rainbow trout) than other amphibian isolates. Despite monophyly based on capsid protein sequences, there was low genetic divergence among all strains (< 1.1%) based on a supergene analysis of the capsid protein and the two noncoding regions. These analyses also showed polyphyly of strains from Arizona and Colorado, suggesting recent spread. Nested clade analyses indicated both range expansion and long-distance colonization in clades containing virus strains isolated from bait salamanders and the Indiana University axolotl (Ambystoma mexicanum) colony. Human enhancement of viral movement is a mechanism consistent with these results. These findings suggest North American salamander ranaviruses cause emerging disease, as evidenced by apparent recent spread over a broad geographical area.

Recent host-shifts in ranaviruses: signatures of positive selection in the viral genome

“…There is significant evidence for host switching of ranaviruses between vertebrate classes (Jancovich et al, 2005(Jancovich et al, , 2010 documented instances of simultaneous infections of sympatric fish and frogs with the same viral isolate (Mao et al, 1999;Bayley et al, 2013). In viral host switching, the virus of one species evolves such that it can replicate and spread in a new species.…”

“…Direct contact and ingestion of contaminated water are known transmission modes, and infection leads to necrosis of the liver, spleen, skin and haematopoietic tissue (Lesbarrères et al, 2012). The bait, pet and food industries are major factors in the spread of these pathogens geographically to naïve localities and species (Jancovich et al, 2005;Picco & Collins, 2008). Although both pathogens pose a lethal threat to amphibians, ranaviruses tend to cause recurrent population dieoffs that target larval-stage amphibians (Chinchar, 2002).…”

Combined Effects of Atrazine and Chlorpyrifos on Susceptibility of the Tiger Salamander to Ambystoma tigrinum Virus

“…A major cause for these die-offs has been the emergence of a single host ranaviral pathogen, Ambystoma tigrinum virus (ATV) (Jancovich et al, 1997(Jancovich et al, , 2005Storfer et al, 2007). It is hypothesized that environmental cofactors might have triggered some of these recent outbreaks (Jancovich et al, 2005;Forson and Storfer, 2006a, b).…”

“…Tiger salamanders (Ambystoma tigrinum), like many other amphibian species, have undergone widespread epizootics throughout the western United States (Jancovich et al, 1997(Jancovich et al, , 2005. A major cause for these die-offs has been the emergence of a single host ranaviral pathogen, Ambystoma tigrinum virus (ATV) (Jancovich et al, 1997(Jancovich et al, , 2005Storfer et al, 2007).…”

Ecophysiology meets conservation: understanding the role of disease in amphibian population declines

“…Currently, three amphibian ranaviruses have been identified: frog virus 3 (FV3), Bohle iridovirus (BIV) and Ambystoma tigrinum virus (ATV) [57]. Mortality events and/or infections involving viruses have been detected in amphibian population across the globe [58][59][60][61][62][63][64][65][66][67][68]. While ranavirus infections have been detected in both adult and larval amphibians, the virus appears to be most lethal in larvae [69].…”