Quantifying the strength of viral fitness tradeoffs between hosts: A meta-analysis of pleiotropic fitness effects

Abstract

AbstractThe range of hosts a given virus can infect is widely presumed to be limited by tradeoffs in fitness between alternative hosts. These fitness tradeoffs may arise naturally due to antagonistic pleiotropy if mutations that increase fitness in one host tend to decrease fitness in alternate hosts. While antagonistic pleiotropy underlies certain tradeoffs, there is a growing recognition that positive pleiotropy may be more common than previously appreciated. With positive pleiotropy, mutations have concordant fitness effects such that a beneficial mutation can simultaneously increase fitness in different hosts, providing a genetic mechanism by which selection can overcome fitness tradeoffs. How readily evolution can overcome fitness tradeoffs therefore depends on the overall distribution of mutational fitness effects between hosts, including the relative frequency of antagonistic versus positive pleiotropy. We therefore conducted a systematic meta-analysis of the pleiotropic fitness effects of viral mutations reported in different hosts. Our analysis indicates that the relative frequency of antagonistic versus positive pleiotropy may simply reflect the underlying frequency of beneficial and deleterious mutations in individual hosts. Given a mutation is beneficial in one host, the probability that it is deleterious in another host is roughly equal to the probability that any mutation is deleterious, suggesting there is no natural tendency towards antagonistic pleiotropy beyond that expected by chance. While both antagonistic and positive pleiotropy are common, fitness effects are overall positively correlated between hosts and unconditionally beneficial mutations are not uncommon. The widespread prevalence of positive pleiotropy suggests that many fitness tradeoffs may be readily overcome by evolution given the right selection pressures.