The evolutionary dynamics of influenza A virus adaptation to mammalian hosts

Abstract

Few questions on infectious disease are more important than understanding how and why avian influenza A viruses successfully emerge in mammalian populations, yet little is known about the rate and nature of the virus’ genetic adaptation in new hosts. Here, we measure, for the first time, the genomic rate of adaptive evolution of swine influenza viruses (SwIV) that originated in birds. By using a curated dataset of more than 24 000 human and swine influenza gene sequences, including 41 newly characterized genomes, we reconstructed the adaptive dynamics of three major SwIV lineages (Eurasian, EA; classical swine, CS; triple reassortant, TR). We found that, following the transfer of the EA lineage from birds to swine in the late 1970s, EA virus genes have undergone substantially faster adaptive evolution than those of the CS lineage, which had circulated among swine for decades. Further, the adaptation rates of the EA lineage antigenic haemagglutinin and neuraminidase genes were unexpectedly high and similar to those observed in human influenza A. We show that the successful establishment of avian influenza viruses in swine is associated with raised adaptive evolution across the entire genome for many years after zoonosis, reflecting the contribution of multiple mutations to the coordinated optimization of viral fitness in a new environment. This dynamics is replicated independently in the polymerase genes of the TR lineage, which established in swine following separate transmission from non-swine hosts.

Extensive Positive Selection Drives the Evolution of Nonstructural Proteins in Lineage C Betacoronaviruses

“…Recently, an extended analysis indicated that the adaptation of avian influenza virus to swine was accompanied by substitutions in al-most all viral genes. Mutation accrual continued for a long time after the host shift, suggesting that multiple mutations progressively optimize viral fitness in the new host (70); many of these mutations were suggested to represent compensatory or epistatic changes (70). Interestingly, we also found evidence of coevolution between site pairs, possibly suggesting epistatic interactions.…”

Prisoners of war — host adaptation and its constraints on virus evolution

“…Host jumps are associated with periods of accelerated sequence change as the virus remodels and regains fitness in an altered environment, very much as conceptualized in bacterial evolution 71 . Host adaptation after cross-species transmission is associated with rapid amino acid sequence changes of viral genes, typically those associated with receptor interactions and the evasion of innate immunity [72][73][74][75][76] but often pervasive throughout the entire virus genome 77 . Larger-scale gene modifications, such as the repurposing of the HIV-1 accessory protein Vpu to antagonize the cellular antiviral protein tetherin was a key adaptive change that enhanced the replication ability of HIV-1 in humans following its zoonotic transfer from chimpanzees 22 .…”

Recent host-shifts in ranaviruses: signatures of positive selection in the viral genome

“…Computational tools that can detect episodes of rapid adaptation of specific genes, in conjunction with the increased availability of genomic data, have provided new avenues for identifying candidate genes potentially involved in dynamic processes such as host switching (Sawyer & Elde, 2012). In many cases, genes that are involved in host-pathogen interactions exhibit episodes of intense positive selection during the process of establishing a new host species (Shackelton et al, 2005;Hoelzer et al, 2008;Meyerson & Sawyer, 2011;Bhatt et al, 2013). Genes identified via these methods are often involved in immune evasion, replication, reproduction, gene expression, host-pathogen co-evolution and host defences (Endo et al, 1996;Yang et al, 2000;McLysaght et al, 2003;Harrison & Bonning, 2004;Shackelton et al, 2005;Sabeti et al, 2006;Kosiol et al, 2008;Elde et al, 2012).…”