Frequent cross-species transmissions of foamy virus between domestic and wild felids

Abstract

Emerging viral outbreaks resulting from host switching is an area of continued scientific interest. Such events can result in disease epidemics or in some cases, clinically silent outcomes. These occurrences are likely relatively common and can serve as tools to better understand disease dynamics, and may result in changes in behavior, fecundity, and, ultimately survival of the host. Feline foamy virus (FFV) is a common retrovirus infecting domestic cats globally, which has also been documented in the North American puma (Puma concolor). The prevalent nature of FFV in domestic cats and its ability to infect wild felids, including puma, provides an ideal system to study cross-species transmission across trophic levels (positions in the food chain), and evolution of pathogens transmitted between individuals following direct contact. Here we present findings from an extensive molecular analysis of FFV in pumas, focused on two locations in Colorado, and in relation to FFV recovered from domestic cats in this and previous studies. Prevalence of FFV in puma was high across the two regions, ∼77 per cent (urban interface site) and ∼48 per cent (rural site). Comparison of FFV from pumas living across three states; Colorado, Florida, and California, indicates FFV is widely distributed across North America. FFV isolated from domestic cats and pumas was not distinguishable at the host level, with FFV sequences sharing >93 per cent nucleotide similarity. Phylogenetic, Bayesian, and recombination analyses of FFV across the two species supports frequent cross-species spillover from domestic cat to puma during the last century, as well as frequent puma-to-puma intraspecific transmission in Colorado, USA. Two FFV variants, distinguished by significant difference in the surface unit of the envelope protein, were commonly found in both hosts. This trait is also shared by simian foamy virus and may represent variation in cell tropism or a unique immune evasion mechanism. This study elucidates evolutionary and cross-species transmission dynamics of a highly prevalent multi-host adapted virus, a system which can further be applied to model spillover and transmission of pathogenic viruses resulting in widespread infection in the new host.

Bioaccumulation of Pathogen Exposure in Top Predators

“…Spillover may result in catastrophic consequences to the new host, resulting in significant economic [4,5] or conservation [6][7][8][9] impacts and major threats to wildlife survival and biodiversity; for example, distemper in African lions (Panthera leo) [10], and plague and distemper in blackfooted ferrets (Mustela nigripes) [11,12]. Recent studies have indicated, however, that crossspecies transmission frequently occurs without substantial population-level impacts to the recipient host [13,14]. While drivers and mechanisms of spillover transmission have been broadly reviewed [15][16][17], predation has not been directly implicated as a risk factor.…”

“…Protocols permitting detection of pathogens in excreta have been perfected, allowing noninvasive sampling techniques that augment sample collection protocols that would otherwise be invasive, expensive, and potentially harmful to either animals or field personnel [27][28][29]. Furthermore, significant advances in bioinformatics approaches have accelerated pathogen genomic characterization that estimates time and place of transmission events based on phylodynamic and phylogeographic analyses [13,14,23,[30][31][32][33]. Because of these recent refinements in field and diagnostic methods, inferring source of infection and tracking of pathogen host switching have become substantially more feasible and accurate.…”

Transmission of one predicts another: Apathogenic proxies for transmission dynamics of a fatal virus

“…This finding is further supported by the tendency for FIV phylogenies to show distinct geographic clustering (66,67), but is in contrast to other infectious agents of puma. An additional feline retrovirus, feline foamy virus (FFV), does not show distinct geographic clustering but is commonly transmitted between domestic cats and puma (68). A prior study of several pathogens in puma across the United States rarely identified spatial autocorrelation in pathogen exposures, but notably found that FIV infection status approached statistical significance specifically in Florida panthers (69).…”

“…Rather, targeted investigation of spillover dynamics could draw on studies of other apathogenic viral candidates that are frequently transmitted from domestic cats to puma, such as FFV (68).…”

When are pathogen dynamics likely to reflect host population genetic structure?

“…Patterns of viral co‐infection and pathogen–pathogen interactions may also produce variable IHPC relationships. Similarly, host species ecological factors could include: increased extent of interspecific interactions reducing detectability of IHPC (e.g., Olival et al's finding of NiV clades that extend beyond the distribution of P. medius ); and co‐occurrence of taxonomically related species impacting whether IHPC can be detected in a focal species in some areas, relative to others (Kraberger et al, ). Of course, an array of mechanisms not identified here may also exist.…”