Impact of ploidy and pathogen life cycle on resistance durability

Abstract

The breeding of resistant hosts based on the gene-for-gene interaction is crucial to address epidemics of plant pathogens in agroecosystems. Resistant host deployment strategies are developed and studied worldwide to decrease the probability of resistance breakdown and increase the resistance durability in various pathosystems. A major component of deployment host strategies is the proportion of resistant hosts in the landscape. However, the impact of this proportion on resistance durability remains unclear for diploid pathogens with complex life cycles. In this study, we modelled pathogen population dynamics and genetic evolution at the virulence locus to assess the impact of the ploidy (haploid or diploid) and the pathogen's life cycle (with or without host alternation) on resistance durability. Ploidy has a strong impact on evolutionary trajectories, with much greater stochasticity and delayed times of resistance breakdown for diploids. This result emphasizes the importance of genetic drift in this system: as the virulent allele is recessive, positive selection on resistant hosts only applies to homozygous (virulent) individuals, which may lead to population collapses at low frequencies of the virulent allele. We also observed differences in the effect of host deployment depending on the pathogen's life cycle. With host alternation, the probability that the pathogen population collapses strongly increases with the proportion of resistant hosts in the landscape. Therefore, resistance breakdown events occurring at high proportions of resistant hosts frequently amount to evolutionary rescue. Last, life cycles correspond to two selection regimes: without host alternation (soft selection) the resistance breakdown is mainly driven by the migration rate. Conversely, host alternation (hard selection) resembles an all-or-nothing game, with stochastic trajectories caused by the recurrent allele redistributions on the alternate host.

Neutral genetic structuring of pathogen populations during rapid adaptation

“…As such, it drives the strength of both population expansion and selection pressure exerted on the pathogen population. With host alternation, this proportion also shapes the population demography in determining the vulnerability of the population to evolutionary rescue (See Figure 4 in Saubin et al, 2021). Pathogen control often leads to high proportions of resistant hosts in agricultural landscapes (Stukenbrock and McDonald, 2008; Zhan et al, 2015).…”

“…invaded compartment one year and cleared compartment the next year). As the virulent allele is recessive, it is more vulnerable to extinction with host alternation (Saubin et al, 2021). Here we show that in addition to the stochasticity in the fate of the virulent allele, this life cycle also increases the stochasticity in the genetic signatures of resistance overcoming.…”

“…This is because of additional mortality that originates once a year from the massive redistribution of individuals after the sexual reproduction, with the death of all avirulent individuals that migrate to resistant hosts. Besides the additional mortality, the massive redistribution also increases the probability that a virulent individual migrates to the resistant host, and hence increases the probability of evolutionary rescue (Saubin et al, 2021). Here we demonstrate that such events can lead to strong and typical genetic signatures at neutral loci, that define a specific cluster with host alternation (Cluster 3) and can thus be uncovered using population genetics indices.…”

“…It couples population dynamics and population genetics to follow through time the evolutionary trajectory of different genotypes at the selected avirulence locus and at neutral genetic markers scattered in the genome. The model is similar to the model described in Saubin et al (2021), with the addition in this study of the evolution of neutral markers through time. We consider a life cycle commonly found in temperate pathogen species, which alternate rounds of clonal reproduction with an annual event of sexual reproduction (Agrios, 2005).…”

“…the invasion of resistant hosts by virulent individuals (Johnson, 1984; Pink and Puddephat, 1999; Brown and Tellier, 2011; Burdon et al, 2016). The resistant variety is usually deployed widely across the landscape, and this intense and unidirectional selection pressure can result in severe epidemics, which impose rapid and drastic demographic changes for the pathogen population (Burdon et al, 2016; Persoons et al, 2017; Saubin et al, 2021). We have limited knowledge of how such events shape the genetic evolution of pathogens and what would be the typical genetic signatures of such strong demographic and selective events on the pathogen population.…”