Intrahost speciations and host switches played an important role in the evolution of herpesviruses.

Abstract

In times when herpesvirus genomic data were scarce, the cospeciation between these viruses and their hosts was considered to be common knowledge. However, as more herpesviral sequences were made available, tree reconciliation analyses started to reveal topological incongruences between host and viral phylogenies, indicating that other cophylogenetic events, such as intrahost speciation and host switching, likely played important roles along more than 200 million years of evolutionary history of these viruses. Tree reconciliations performed with undated phylogenies can identify topological differences, but offer insufficient information to reveal temporal incongruences between the divergence timing of host and viral species. In this study, we performed cophylogenetic analyses using time-resolved trees of herpesviruses and their hosts, based on careful molecular clock modelling. This approach enabled us to infer cophylogenetic events over time and also integrate information on host biogeography to better understand host–virus evolutionary history. Given the increasing amount of sequence data now available, mismatches between host and viral phylogenies have become more evident, and to account for such phylogenetic differences, host switches, intrahost speciations and losses were frequently found in all tree reconciliations. For all subfamilies in Herpesviridae, under all scenarios we explored, intrahost speciation and host switching were more frequent than cospeciation, which was shown to be a rare event, restricted to contexts where topological and temporal patterns of viral and host evolution were in strict agreement.