The genomic evolution of H1 influenza A viruses from swine detected in the United States between 2009 and 2016

Abstract

Transmission of influenza A virus (IAV) from humans to swine occurs with relative frequency and is a critical contributor to swine IAV diversity. Subsequent to the introduction of these human seasonal lineages, there is often reassortment with endemic viruses and antigenic drift. To address whether particular genome constellations contributed to viral persistence following the introduction of the 2009 H1N1 human pandemic virus to swine in the USA, we collated and analysed 616 whole genomes of swine H1 isolates. For each gene, sequences were aligned, the best-known maximum likelihood phylogeny was inferred, and each virus was assigned a clade based upon its evolutionary history. A time-scaled Bayesian approach was implemented for the haemagglutinin (HA) gene to determine the patterns of genetic diversity over time. From these analyses, we observed an increase in genome diversity across all H1 lineages and clades, with the H1-γ and H1-δ1 genetic clades containing the greatest number of unique genome patterns. We documented 74 genome patterns from 2009 to 2016, of which 3 genome patterns were consistently detected at a significantly higher level than others across the entire time period. Eight genome patterns increased significantly, while five genome patterns were shown to decline in detection over time. Viruses with genome patterns identified as persisting in the US swine population may possess a greater capacity to infect and transmit in swine. This study highlights the emerging genetic diversity of US swine IAV from 2009 to 2016, with implications for swine and public health and vaccine control efforts.

Fig. 1.

Phylogenetic relationships of HA genes from 616 swine influenza collected in the US swine during 2009–2016. The maximum clade credibitly time-scaled Bayesian phylogeny trees for H1-classical lineage (a) and H1-delta lineage (b) are presented with the tips coloured by the NA+internal constellation, which represent the NA+internal patterns following the colour scheme of Table 1. Only genome patterns with an abundance greater than 5 are shown.

Fig. 1.

Phylogenetic relationships of HA genes from 616 swine influenza collected in the US swine during 2009–2016. The maximum clade credibitly time-scaled Bayesian phylogeny trees for H1-classical lineage (a) and H1-delta lineage (b) are presented with the tips coloured by the NA+internal constellation, which represent the NA+internal patterns following the colour scheme of Table 1. Only genome patterns with an abundance greater than 5 are shown.

Fig. 2.

Annual patterns of NA+internal gene patterns within each H1 clade for US H1 viruses, 2009 to 2016. H1 clades are represented in rows, divided by year of detection in columns. The bars represent NA+internal patterns with colours indicated in Table 1. Asterisks above bars indicate genome patterns that were significantly more abundant than other detected patterns from that particular year.