Abstract

Virus host range, i.e., the number and diversity of host species of viruses, is an important determinant of disease emergence and of the efficiency of disease control strategies. However, for plant viruses, little is known about the genetic or ecological factors involved in the evolution of host range. Using available genome sequences and host range data, we performed a phylogenetic analysis of host range evolution in the genus Potyvirus, a large group of plant RNA viruses that has undergone a radiative evolution circa 7000 years ago, contemporaneously with agriculture intensification in mid Holocene. Maximum likelihood inference based on a set of 59 potyviruses and 38 plant species showed frequent host range changes during potyvirus evolution, with 4.6 changes per plant species on average, including 3.1 host gains and 1.5 host loss. These changes were quite recent, 74% of them being inferred on the terminal branches of the potyvirus tree. The most striking result was the high frequency of correlated host gains occurring repeatedly in different branches of the potyvirus tree, which raises the question of the dependence of the molecular and/or ecological mechanisms involved in adaptation to different plant species.

Highlights

  • Host range of a parasite is defined as the set of organisms where the parasite can perform, at least partly, its infection cycle

  • Relatively few studies are available on host range genetic determinants or on host range changes that have occurred during virus evolutionary history [6,7,8,9,10,11,12,13,14,15,16]

  • To identify host range changes during the evolution of potyviruses, we first established the phylogenetic relationships between 62 virus species for which genome and host range data were available: 59 Potyvirus species and three Rymovirus species used as outgroups

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Summary

Introduction

Host range of a parasite is defined as the set of organisms where the parasite can perform, at least partly, its infection cycle. The number and diversity of host species are frequently used to measure a parasites’ host range. Host range is an important notion in parasitology, since it is linked to risks of disease emergence [1] and has important consequences on the implementation and efficiency of disease control strategies including epidemiological surveillance, quarantine measures, vaccination, and deployment of parasite-resistant crop varieties in agricultural landscapes [2,3,4]. Parasites’ host range has been used for decades for taxonomic purposes, both at parasite inter- and intraspecies levels. There is little knowledge on determinants of the host species range of plant parasites by contrast with determinants of infection at the plant intraspecific level that have been the subject of numerous studies, about the ability of a parasite to infect plant genotypes with specific resistance genes [5]. Relatively few studies are available on host range genetic determinants or on host range changes that have occurred during virus evolutionary history [6,7,8,9,10,11,12,13,14,15,16]

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