Abstract

The cross-species transmission of viruses from one host species to another is responsible for the majority of emerging infections. However, it is unclear whether some virus families have a greater propensity to jump host species than others. If related viruses have an evolutionary history of co-divergence with their hosts there should be evidence of topological similarities between the virus and host phylogenetic trees, whereas host jumping generates incongruent tree topologies. By analyzing co-phylogenetic processes in 19 virus families and their eukaryotic hosts we provide a quantitative and comparative estimate of the relative frequency of virus-host co-divergence versus cross-species transmission among virus families. Notably, our analysis reveals that cross-species transmission is a near universal feature of the viruses analyzed here, with virus-host co-divergence occurring less frequently and always on a subset of viruses. Despite the overall high topological incongruence among virus and host phylogenies, the Hepadnaviridae, Polyomaviridae, Poxviridae, Papillomaviridae and Adenoviridae, all of which possess double-stranded DNA genomes, exhibited more frequent co-divergence than the other virus families studied here. At the other extreme, the virus and host trees for all the RNA viruses studied here, particularly the Rhabdoviridae and the Picornaviridae, displayed high levels of topological incongruence, indicative of frequent host switching. Overall, we show that cross-species transmission plays a major role in virus evolution, with all the virus families studied here having the potential to jump host species, and that increased sampling will likely reveal more instances of host jumping.

Highlights

  • Emerging pathogens that cross the species barrier to infect new hosts can profoundly affect human and animal health, as well as wildlife and the agricultural industries

  • Given the ecological and genetic barriers a virus must overcome to jump species and adapt to new hosts, it might be reasonable to assume that successful cross-species transmission is a relatively rare occurrence and that viruses are instead more likely to co-diverge with their hosts

  • Cross-species transmission among viral families we have revealed that co-divergence is relatively infrequent among 19 diverse families of RNA and DNA viruses, such that cross-species transmission plays a central role in virus evolution

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Summary

Introduction

Emerging pathogens that cross the species barrier to infect new hosts can profoundly affect human and animal health, as well as wildlife and the agricultural industries. Most emerging diseases seemingly result from such a process of cross-species transmission, it is the case that some viruses seem to rarely jump the species barrier and instead co-diverge with their hosts over long stretches of evolutionary time. It has been proposed that a number of families of DNA viruses have codiverged with their hosts over long evolutionary time-scales [3,4,5], and do so more frequently than RNA viruses, which in contrast display a combination of co-divergence and host switching [6]. While phylogenetic trees for some RNA viruses, such as particular retroviruses, are generally congruent with those from their hosts suggesting long-term codivergence [7], for others, such as flaviviruses, host jumping appears to be relatively frequent [8]. The situation appears to be even more complex in cases such as the hantaviruses where there is evidence of both codivergence and host jumping [6]

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