Avian influenza virus exhibits distinct evolutionary dynamics in wild birds and poultry.

Mathieu Fourment,Edward C Holmes

doi:10.1186/s12862-015-0410-5

Abstract

BackgroundWild birds are the major reservoir hosts for influenza A viruses, occasionally transmitting to other species such as domesticated poultry. Despite an abundance of genomic data from avian influenza virus (AIV), little is known about whether AIV evolves differently in wild birds and poultry, although this is critical to revealing the dynamics and time-scale of viral evolution. In particular, because environmental (water-borne) transmission is more common in wild birds, which may reduce the number of replications per unit time, it is possible that evolutionary rates are systematically lower in wild birds than in poultry.ResultsWe estimated rates of nucleotide substitution in two AIV subtypes that are strongly associated with infections in wild birds – H4 and H6 – and compared these to rates in the H5N1 subtype that has circulated in poultry for almost two decades. Our analyses of three internal genes confirm that H4 and H6 viruses are evolving significantly more slowly than H5N1 viruses, suggesting that evolutionary rates of AIV are reduced in wild birds. This result was verified by the analysis of a poultry-associated H6 lineage that exhibited a markedly higher substitution rate than those H6 viruses circulating in wild birds. Interestingly, we also observed a significant difference in evolutionary rate between H4 and H6, despite frequent reassortment rate among them.ConclusionsAIV experiences markedly different evolutionary dynamics between wild birds and poultry. These results suggest that rate heterogeneity among viral subtypes and ecological groupings should be taken into account when estimating evolutionary rates and divergence times.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0410-5) contains supplementary material, which is available to authorized users.

Highlights

Wild birds are the major reservoir hosts for influenza A viruses, occasionally transmitting to other species such as domesticated poultry
The Markov chain Monte Carlo (MCMC)-based (BEAST) analysis shows that the mean nucleotide substitution rate of avian influenza virus (AIV) varies between 1.87 × 10−3 and 4.2 × 10−3 subs/site/year depending on the model used
Estimates of substitution rates in these poultry H6 viruses are similar to those in H5N1 from poultry and significantly higher than those of H6 from wild birds (Fig. 1), confirming that AIV evolutionary rates are elevated in poultry

Summary

Introduction

Wild birds are the major reservoir hosts for influenza A viruses, occasionally transmitting to other species such as domesticated poultry. With the exception of a small number of viruses recently described in bats [1,2], wild (water) birds are the natural reservoir for all haemaggluttinin (H) and neuraminidase (N) subtypes, harbouring 16 of the former and 9 of the latter [3,4,5]. It is noteworthy that AIV outbreaks in poultry have only been associated with a relatively small number of H and N subtypes, suggesting that there are important species barriers within birds. There are a number of factors that could create important evolutionary differences between AIV in wild birds and poultry, notably reflecting differences in the mode of transmission and population A question that has been less frequently addressed is whether evolutionary patterns and processes differ between wild birds and poultry? there are a number of factors that could create important evolutionary differences between AIV in wild birds and poultry, notably reflecting differences in the mode of transmission and population

Methods

Results

Conclusion