Emergence and molecular characterization of pigeon Paramyxovirus-1 in non-native Eurasian collared doves (Streptopelia decaocto) in California, USA

Eurasian collared doves (Streptopelia decaocto) were introduced into Florida in the 1980s and have since established populations throughout the continental United States. Pigeon paramyxovirus-1 (PPMV-1), a species-adapted genotype VI Avian orthoavulavirus 1, has caused periodic outbreaks among collared doves in the U.S. since 2001 with outbreaks occasionally involving native doves. In California, PPMV-1 mortality events were first documented in Riverside County in 2014 with subsequent outbreaks in 23 additional counties from southern to northern California between 2015 and 2019. Affected collared doves exhibited torticollis and partial paralysis. Pale kidneys were frequently visible on gross necropsy (65.4%; 51/78) while lymphoplasmacytic interstitial nephritis often with acute tubular necrosis (96.0%; 24/25) and pancreatic necrosis (80.0%; 20/25) were common findings on histopathology. In total, PPMV-1 was confirmed by rRT-PCR and sequence analysis from oropharyngeal and/or cloacal swabs in 93.0% (40/43) of the collared doves tested from 16 California counties. In 2017, Avian orthoavulavirus 1 was confirmed in a native mourning dove (Zenaida macroura) found dead during a PPMV-1 outbreak in collared doves by rRT-PCR from formalin-fixed paraffin-embedded (FFPE) tissues, after the initial rRT-PCR from swabs failed to detect the virus. Molecular sequencing of the fusion protein of isolates collected from collared doves during outbreaks in 2014, 2016, and 2017 identified two distinct subgenotypes, VIa and VIn. Subgenotype VIn has been primarily isolated from collared doves in the southern U.S., while VIa has been isolated from mixed avian species in the northeastern U.S., indicating two independent introductions into California. While populations of collared doves are not expected to be substantially impacted by this disease, PPMV-1 may pose a threat to already declining populations of native columbids. This threat could be assessed by monitoring native and non-native columbids for PPMV-1. Based on our study, swab samples may not be sufficient to detect infection in native columbids and may require the use of non-traditional diagnostic approaches, such as FFPE tissues, to ensure virus detection.