When virulence originates from nonagricultural hosts: evolutionary and epidemiological consequences of introgressions following secondary contacts inVenturia inaequalis

Abstract

SummaryIn pathogens, introgressions through secondary contacts between divergent populations from agricultural and nonagricultural disease reservoirs are expected to have crucial evolutionary and epidemiological implications. Despite the importance of this question for disease management, experimental demonstrations of these implications remain scarce.Recently, we identified a virulent population of the apple scab pathogen Venturia inaequalis that migrated from nonagricultural hosts to European domestic apple orchards. Here, we investigated the occurrence of gene flow between agricultural and nonagricultural populations sampled in two orchards, and thereafter its consequences on the pathogenicity of hybrids.Population genetic structure and demographic inferences based on the genotypes of 104 strains revealed a high amount of gene flow between the two populations in one orchard. In this site, mating between populations was made possible by the presence of a common host. Our results revealed an invasion of the virulent trait in the agricultural population; a main direction of introgression in hybrids from the agricultural to nonagricultural genetic backgrounds; and a population of hybrids with transgressive traits.We demonstrate a secondary contact with gene flow between divergent populations of pathogens. Our findings highlight evolutionary and epidemiological changes in pathogens and have concrete implications for sustainable disease management.

Extensive recent secondary contacts between four European white oak species

“…Methods assessing the maintenance of gene flow have been little used to date (but see Wang et al, 2014, andChriste et al, 2016, for examples in Populus), and divergence scenarios involving secondary contact have, thus, been largely neglected. Pathogenic species provide an emblematic example, in which ecological hypotheses of divergence with gene flow continue to predominate (Leroy et al, 2014), despite clear evidence for secondary contact from studies explicitly testing different demographic scenarios (Gladieux et al, 2011;Lemaire et al, 2016;Leroy et al, 2016). Deciphering the evolutionary history of species is of utmost importance and studies of this kind should be carried out before attempting to evaluate the genomic imprint of natural selection.…”

Population genome sequencing of the scab fungal speciesVenturia inaequalis,Venturia pirina,Venturia aucupariaeandVenturia asperata

“…V. aucupariae has diverged more recently from V. inaequalis than V. pirina. Phylogenetic relationships among V. inaequalis strains from different populations cannot be accurately resolved, probably because of the existence of incomplete lineage sorting and gene flow between populations (Gladieux et al, 2010b;Lemaire et al, 2016;Leroy et al 2016).…”

“…In some cases, host specificity occurs; for instance strains from Pyracantha are not able to infect Malus and vice-versa, which is referred to as formae specialis f. sp pyracantha and f.sp pomi, respectively (Le Cam et al, 2002). Worldwide sampling of V. inaequalis strains has identified divergent populations, mostly reflecting their hosts: wild apple (Malus sieversii, M. orientalis, M sylvestris, M. floribunda) and domesticated apple (Malus x domestica) trees (Gladieux et al, 2008;Gladieux et al, 2010a;Gladieux et al, 2010b;Leroy et al, 2013;Ebrahimi et al, 2016;Leroy et al, 2016). Certain populations have experienced a secondary contact with subsequent gene flow, resulting in the introduction from a wild population into the agricultural compartment of strains that are virulent on resistant cultivars carrying the Rvi6 resistance gene (Guérin et al, 2007;Lemaire et al, 2016).…”

Asian wild apples threatened by gene flow from domesticated apples and by their pestified pathogen

“…Such gene flow between differentiated pathogen populations or species parasitizing wild and domesticated hosts can promote the emergence of new diseases or the breakdown of resistance, through the generation of pathogens with an expanded host range (Depotter, Seidl, Wood & Thomma, 2016), higher resistance to antibiotics (Hanage, Fraser, Tang, Connor & Corander, 2009) or enhanced virulence (i.e. degree of damage caused by the pathogen to its host) (Stukenbrock, Christiansen, Hansen, Dutheil & Schierup, 2012), thus potentially representing a major threat to both crop health and wild host persistence (Lemaire et al, 2016; Leroy, Lemaire, Dunemann & Le Cam, 2013; Leroy et al, 2016). Pathogen spillover ( i .…”