Phylodynamic and Recombination Analyses of Avian Infectious Bronchitis GI-23 Reveal a Widespread Recombinant Cluster and New Among-Countries Linkages

SIMPLE SUMMARY: Infectious bronchitis virus (IBV) is one of the main infectious agents affecting the avian industry. The remarkable evolutionary rate of this virus represents an often unsurmountable challenge to its control, leading to the emergence of different lineages featured by different biological properties and limited cross-protection. In the present study, the origin, spreading and evolution of GI-23, one of the most important IBV emerging lineages, has been reconstructed using a phylodynamic approach. To this purpose, the broadest available collection of complete and partial S1 sequences was downloaded from GenBank and merged with specifically sequenced European strains. After a likely ancient origin, GI-23 circulated undetected in the Middle East for a considerable time, thereafter emerging as a threat in parallel with the intensification of the poultry industry and its introduction in other countries. An intensive viral circulation affecting mainly neighbouring countries or those with strong economic and political relationships was demonstrated, even though some nations appear to play a major role as a “bridge” among less related locations. Of note, a big recombinant cluster, likely originating in the Middle East but spreading thereafter, especially to Europe through Turkey, demonstrated a much-marked increase in viral population size, and potentially fitness, compared to previously circulating variants. ABSTRACT: Infectious bronchitis virus GI-23 lineage, although described approximately two decades ago in the Middle East, has recently drawn remarkable attention and is considered an “emerging” lineage due to its current spread to several other regions, including Europe. Despite the relevance, no comprehensive studies are available investigating its epidemiologic and evolutionary pattern. The present phylodynamic study was designed to fill this gap, benefitting from a collection of freely available GI-23 sequences and ad-hoc generated European ones. After a relatively ancient origin in the Middle East, likely in the first half of the previous century, GI-23 circulated largely undetected or underdiagnosed for a long time in this region, likely causing little damage, potentially because of low virulence coupled with limited development of avian industry in the considered years and regions and insufficient diagnostic activity. The following development of the poultry industry and spread to other countries led to a progressive but slow increase of viral population size between the late ‘90s and 2010. An increase in viral virulence could also be hypothesized. Of note, a big recombinant cluster, likely originating in the Middle East but spreading thereafter, especially to Europe through Turkey, demonstrated a much-marked increase in viral population size compared to previously circulating variants. The extensive available GI-23 sequence datasets allowed to demonstrate several potential epidemiological links among African, Asian, and European countries, not described for other IBV lineages. However, differently from previously investigated IBV lineages, its spread appears to primarily involve neighbouring countries and those with strong economic and political relationships. It could thus be speculated that frequent effective contacts among locations are necessary for efficient strain transmission. Some countries appear to play a major role as a “bridge” among less related locations, being Turkey the most relevant example. The role of vaccination in controlling the viral population was also tentatively evaluated. However, despite some evidence suggesting such an effect, the bias in sequence and data availability and the variability in the applied vaccination protocols prevent robust conclusions and warrant further investigations.