Different Evolutionary Trajectories of European Avian-Like and Classical Swine H1N1 Influenza A Viruses

Abstract

In 1979, a lineage of avian-like H1N1 influenza A viruses emerged in European swine populations independently from the classical swine H1N1 virus lineage that had circulated in pigs since the Spanish influenza pandemic of 1918. To determine whether these two distinct lineages of swine-adapted A/H1N1 viruses evolved from avian-like A/H1N1 ancestors in similar ways, as might be expected given their common host species and origin, we compared patterns of nucleotide and amino acid change in whole genome sequences of both groups. An analysis of nucleotide compositional bias across all eight genomic segments for the two swine lineages showed a clear lineage-specific bias, although a segment-specific effect was also apparent. As such, there appears to be only a relatively weak host-specific selection pressure. Strikingly, despite each lineage evolving in the same species of host for decades, amino acid analysis revealed little evidence of either parallel or convergent changes. These findings suggest that although adaptation due to evolutionary lineages can be distinguished, there are functional and structural constraints on all gene segments and that the evolutionary trajectory of each lineage of swine A/H1N1 virus has a strong historical contingency. Thus, in the context of emergence of an influenza A virus strain via a host switch event, it is difficult to predict what specific polygenic changes are needed for mammalian adaptation.

The evolutionary dynamics of influenza A virus adaptation to mammalian hosts

“…150 days) lowers the chance of re-infection. However, several studies have concluded that the EA lineage HA gene undergoes more antigenic drift than the CS lineage HA gene [8,24,35], and it has been hypothesized that this provided EA viruses with a selective advantage, contributing to it replacing CS and TR strains in Asia [8]. Antibodies arising from CS and TR infection cross-react with many (but not all) EA viruses, which could explain some adaptation observed in the EA lineage HA and NA genes.…”

“…Genes of the EA, CS and TR swine influenza lineages provide a unique system in which these questions can be studied as they originated in birds but have been established in pigs for different durations. In perhaps the only direct comparison of the molecular evolution of the CS and EA lineages, Dunham et al [24] found that the nucleotide base composition of both changed through time since their respective cross-species transmissions, although with no apparent difference in nucleotide substitution rate. However, this study was constrained by a small sample size.…”

First Isolation of the H1N2 Swine Influenza Virus in Polish Pig Farm

“…In Asia, the situation is even more complex as, in addition to the above viruses, Eurasian avian-like H1N1 SIVs are present (1,6,7,10).…”

Epidemiological update on swine influenza (H1N1) in pigs

“…Independently, a novel lineage of avian-like H1N1 swine IAV emerged in Europe in 1979 that essentially replaced classical swine IAV [27,29,30]. This second lineage of swine IAV is enzootic throughout swine-producing regions of Western Europe, where it cocirculates with swine IAVs of the H3N2 and H1N2 subtypes [31,32]. All eight gene segments of the prototype H1N1 viruses of this lineage are thought to be derived from closely related Eurasian avian IAVs by a stable host switch without re-assortment, and this lineage is phylogenetically and antigenically distinct from the classical swine H1N1 lineage [29,[33][34][35].…”