Natural disease and evolution of an Amdoparvovirus endemic in striped skunks (Mephitis mephitis).

Abstract

Striped skunks (Mephitis mephitis) densely populate the human-animal interface of suburbia throughout North America. Skunks share that habitat with numerous related mesocarnivores, where increased contact, competition for shared food and water sources and other stressors contribute to increased exposure and susceptibility to viral infection. The recently identified skunk amdoparvovirus (SKAV) has been detected at high prevalence in skunks and occasionally in mink, but its distribution in North America is unknown. To understand the impact of SKAV in striped skunks and the risk posed to related species, we investigated the geographic distribution of SKAV, analysed its genetic diversity and evolutionary dynamics and evaluated viral distribution in tissues of infected animals to identify possible mechanisms of transmission. SKAV was detected in 72.5% (37/51) skunks and was present at high rates at all locations tested across North America. Analysis of the complete genomic sequence of 29 strains showed a clear geographic segregation, frequent recombination and marked differences in the evolutionary dynamics of the major structural (VP2) and non-structural (NS1) proteins. NS1 was characterized by a higher variability and a higher percentage of positively selected codons. This could indicate that antibody-mediated enhancement of infection occurs in SKAV, an infection strategy that may be conserved across amdoparvoviruses. Finally, in situ hybridization revealed virus in epithelium of the gastrointestinal tract, urinary tract and skin, indicating that viral transmission could occur via oronasal, faecal and/or urinary secretions, as well as from skin and hair. The endemicity of SKAV over large geographic distances and its high genetic diversity suggest a long-term virus-host association. Persistent shedding and high environmental stability likely contribute to efficient viral spread, simultaneously offering opportunities for cross-species transmission with consequent risk to sympatric species, including domestic animals and wildlife.