Absence of adaptive evolution is the main barrier against influenza emergence in horses in Asia despite frequent virus interspecies transmission from wild birds.

Henan Zhu,Batchuluun Damdinjav,Livia Victoria Patrono,Humberto Ramirez-Mendoza,John F Marshall,Julien A R Amat,Joanna Crispell,Martin Gilbert,Gaelle Gonzalez,Toni-Ann Hammond,Joseph Hughes,Malik Peiris,Pablo R Murcia,Yasmin Amy Parr,Enkhtuvshin Shiilegdamba,Y H Connie Leung

doi:10.1371/journal.ppat.1007531

Abstract

Virus ecology and evolution play a central role in disease emergence. However, their relative roles will vary depending on the viruses and ecosystems involved. We combined field studies, phylogenetics and experimental infections to document with unprecedented detail the stages that precede initial outbreaks during viral emergence in nature. Using serological surveys we showed that in the absence of large-scale outbreaks, horses in Mongolia are routinely exposed to and infected by avian influenza viruses (AIVs) circulating among wild birds. Some of those AIVs are genetically related to an avian-origin virus that caused an epizootic in horses in 1989. Experimental infections showed that most AIVs replicate in the equine respiratory tract without causing lesions, explaining the absence of outbreaks of disease. Our results show that AIVs infect horses but do not spread, or they infect and spread but do not cause disease. Thus, the failure of AIVs to evolve greater transmissibility and to cause disease in horses is in this case the main barrier preventing disease emergence.

Highlights

IntroductionViral emergence causing an epidemic of disease in a new host is a rare event, despite the wide diversity of viruses that are known to exist [1] and the constant exposure of hosts to viruses that circulate in other species that share the same habitat
Emerging viral infections pose a constant threat to humans and animals
Influenza A viruses (IAVs) constitute the archetypical example of emerging viruses: their main natural reservoir is in wild birds but they have established in humans, pigs and horses

Summary

Introduction

Viral emergence causing an epidemic of disease in a new host is a rare event, despite the wide diversity of viruses that are known to exist [1] and the constant exposure of hosts to viruses that circulate in other species that share the same habitat. Viral emergence could be impaired in the presence of ample ecological opportunities if mutations required to adapt to a new host are difficult to acquire or have a high fitness cost in the donor or recipient host [10]. Even in the presence of the “right” ecological and evolutionary factors, influenza virus emergence could be impaired by hemagglutinin imprinting, a biological process by which the first IAV infection of an individual confers lifelong cross-protection against severe infection by viruses carrying an HA of the same phylogenetic group [11, 12]

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