Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion

Authors: HICKS, JOSEPH - University Of Texas Health Science Center; DIMITROV, KIRIL - Consultant; Afonso, Claudio; RAMEY, ANDREW - Us Geological Survey (USGS); BAHL, JUSTIN - University Of Texas Health Science Center

Submitted to: BMC Evolutionary Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/3/2019
Publication Date: 5/24/2019
Citation: Hicks, J.T., Dimitrov, K.M., Afonso, C.L., Ramey, A.M., Bahl, J. 2019. Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion. BMC Evolutionary Biology. 19:108. https://doi.org/10.1186/s12862-019-1431-2.
DOI: https://doi.org/10.1186/s12862-019-1431-2

Interpretive Summary: Newcastle disease outbreaks are a global challenge to the poultry industry, as effective management of this disease depend on understanding of the ecology and transmission properties of the virus. Although the susceptibility of wild birds to NDV has been largely accepted, their role in the short-term spread of the virus, as maintenance hosts, remain unclear. In this study, we analyzed how host and geography affect viral movement by dissecting the evolutionary history of 1,602 APMV-1 sequences collected from 1970 to 2016. The viral transmission between avian host types and the diffusion between geographic regions was analyzed. The movement of Newcastle disease viruses among divergent host taxa was statistically supported, specifically the bidirectional transitions between domestic chickens and ducks. Chickens also acted as an important viral source to other host species. The results indicated that Europe was an important node acting as either a source or sink location in half of the supported geographic transitions.

Technical Abstract: Background Avian avulavirus (commonly known as avian paramyxovirus-1 or APMV-1) can cause disease of varying severity in both domestic and wild birds. Understanding how viruses move among hosts and geography would be useful for informing prevention and control efforts. A Bayesian statistical framework was employed to estimate the evolutionary history of 1602 complete fusion gene APMV-1 sequences collected from 1970 to 2016 in order to infer viral transmission between avian host orders and diffusion among geographic regions. Ancestral states were estimated with a non-reversible continuous-time Markov chain model, allowing transition rates between discrete states to be calculated. The evolutionary analyses were stratified by APMV-1 classes I (n'='198) and II (n'='1404), and only those sequences collected between 2006 and 2016 were allowed to contribute host and location information to the viral migration networks. Results While the current data was unable to assess impact of host domestication status on APMV-1 diffusion, these analyses supported the sharing of APMV-1 among divergent host taxa. The highest supported transition rate for both classes existed from domestic chickens to Anseriformes (class I:6.18 transitions/year, 95% highest posterior density (HPD) 0.31–20.02, Bayes factor (BF)'='367.2; class II:2.88 transitions/year, 95%HPD 1.9–4.06, BF'='34,582.9). Further, among class II viruses, domestic chickens also acted as a source for Columbiformes (BF'='34,582.9), other Galliformes (BF'='34,582.9), and Psittaciformes (BF'='34,582.9). Columbiformes was also a highly supported source to Anseriformes (BF'='322.0) and domestic chickens (BF'='402.6). Additionally, our results provide support for the diffusion of viruses among continents and regions, but no interhemispheric viral exchange between 2006 and 2016. Among class II viruses, the highest transition rates were estimated from South Asia to the Middle East (1.21 transitions/year; 95%HPD 0.36–2.45; BF'='67,107.8), from Europe to East Asia (1.17 transitions/year; 95%HPD 0.12–2.61; BF'='436.2) and from Europe to Africa (1.06 transitions/year, 95%HPD 0.07–2.51; BF'='169.3). Conclusions While migration appears to occur infrequently, geographic movement may be important in determining viral diversification and population structure. In contrast, inter-order transmission of APMV-1 may occur readily, but most events are transient with few lineages persisting in novel hosts.