Contact-number-driven virus evolution: A multi-level modeling framework for the evolution of acute or persistent RNA virus infection

摘要

Viruses evolve in infected host populations, and host population dynamics affect viral evolution. RNA viruses with a short duration of infection and a high peak viral load, such as SARS-CoV-2, are maintained in human populations. By contrast, RNA viruses characterized by a long infection duration and a low peak viral load (e.g., borna disease virus) can be maintained in nonhuman populations, and the process of the evolution of persistent viruses has rarely been explored. Here, using a multi-level modeling approach including both individual-level virus infection dynamics and population-scale transmission, we consider virus evolution based on the host environment, specifically, the effect of the contact history of infected hosts. We found that, with a highly dense contact history, viruses with a high virus production rate but low accuracy are likely to be optimal, resulting in a short infectious period with a high peak viral load. In contrast, with a low-density contact history, viral evolution is toward low virus production but high accuracy, resulting in long infection durations with low peak viral load. Our study sheds light on the origin of persistent viruses and why acute viral infections but not persistent virus infection tends to prevail in human society. Author summaryAs exemplified by the SARS-CoV-2 variants of concern and influenza A virus variants, we need to predict the future evolution of viral properties to counter an oncoming pandemic. While some RNA viruses such as influenza A viruses adopt an acute infection strategy, others, such as Borna disease virus, adopt a persistent infection strategy. In what kind of environment did these viruses evolve? This study presents a modeling framework to investigate the evolution of proliferative ability and accuracy throughout the viral life cycle. Specifically, we calculated eco-evolutionary dynamics from virus infection in the host to transmission between hosts and capture the transmission potential of the virus. The acute infection phenotype evolves under a contact history involving frequent contacts between hosts. By contrast, the persistent infection phenotype evolves under an environment with a small mean and a large variance in the host contact history. These findings have direct implications for the fight against the continuous evolution of various viruses, which have easily prevailed in the setting of dense human contacts. We believe it is essential to readdress the evolution of viruses from an evolutionary and ecological perspective.