Inter- and intracontinental migrations and local differentiation have shaped the contemporary epidemiological landscape of canine parvovirus in South America

Abstract

Canine parvovirus (CPV) is a fast-evolving single-stranded DNA virus that causes one of the most significant infectious diseasesof dogs. Although the virus dispersed over long distances in the past, current populations are considered to be spatiallyconfined and with only a few instances of migration between specific localities. It is unclear whether these dynamicsoccur in South America where global studies have not been performed. The aim of this study is to analyze the patterns ofgenetic variability in South American CPV populations and explore their evolutionary relationships with global strains.Genomic sequences of sixty-three strains from South America and Europe were generated and analyzed using a phylodynamicapproach. All the obtained strains belong to the CPV-2a lineage and associate with global strains in four monophyleticgroups or clades. European and South American strains from all the countries here analyzed are representative of awidely distributed clade (Eur-I) that emerged in Southern Europe during 1990?98 to later spread to South America in theearly 2000s. The emergence and spread of the Eur-I clade were correlated with a significant rise in the CPV effective populationsize in Europe and South America. The Asia-I clade includes strains from Asia and Uruguay. This clade originated in Asia during the late 1980s and evolved locally before spreading to South America during 2009?10. The third clade (Eur-II)comprises strains from Italy, Brazil, and Ecuador. This clade appears in South America as a consequence of an early introductionfrom Italy to Ecuador in the middle 1980s and has experienced extensive local genetic differentiation. Some strainsfrom Argentina, Uruguay, and Brazil constitute an exclusive South American clade (SA-I) that emerged in Argentina in the1990s. These results indicate that the current epidemiological scenario is a consequence of inter- and intracontinentalmigrations of strains with different geographic and temporal origins that set the conditions for competition and local differentiationof CPV populations. The coexistence and interaction of highly divergent strains are the main responsible for thedrastic epidemiological changes observed in South America in the last two decades. This highlights the threat of invasionfrom external sources and the importance of whole-genome resolution to robustly infer the origin and spread of new CPVvariants. From a taxonomic standpoint, the findings herein show that the classification system that uses a single aminoacid to identify variants (2a, 2b, and 2c) within the CPV-2a lineage does not reflect phylogenetic relationships and is not suitableto analyze CPV evolution. In this regard, the identification of clades or sublineages within circulating CPV strains is thefirst step towards a genetic and evolutionary classification of the virus.