The escalatory Red Queen: Population extinction and replacement following arms race dynamics in poplar rust

Abstract

Host-parasite systems provide convincing examples of Red Queen co-evolutionary dynamics. Yet, a key process underscored in Van Valen's theory - that arms race dynamics can result in extinction - has never been documented. One reason for this may be that most sampling designs lack the breadth needed to illuminate the rapid pace of adaptation by pathogen populations. In this study, we used a 25-year temporal sampling to decipher the demographic history of a plant pathogen: the poplar rust fungus, Melampsora larici-populina. A major adaptive event occurred in 1994 with the breakdown of R7 resistance carried by several poplar cultivars widely planted in Western Europe since 1982. The corresponding virulence rapidly spread in M. larici-populina populations and nearly reached fixation in northern France, even on susceptible hosts. Using both temporal records of virulence profiles and temporal population genetic data, our analyses revealed that (i) R7 resistance breakdown resulted in the emergence of a unique and homogeneous genetic group, the so-called cultivated population, which predominated in northern France for about 20 years, (ii) selection for Vir7 individuals brought with it multiple other virulence types via hitchhiking, resulting in an overall increase in the population-wide number of virulence types and (iii) - above all - the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown. Our temporal analysis illustrates how antagonistic co-evolution can lead to population extinction and replacement, hence providing direct evidence for the escalation process which is at the core of Red Queen dynamics.

Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution

“…An analysis of 25‐year temporal sampling of the poplar rust fungus, Melampsora larici‐populina , nicely illustrated how antagonistic co‐evolution can lead to population extinction and replacement, hence providing direct evidence for the escalation process which is at the core of Red Queen dynamics (Persoons et al . ).…”

Editorial 2018

“…Kraemer and Boynton () reviewed that literature and found that “local adaptation has been most frequently studied, and most frequently found, in host–pathogen systems” (Giraud et al., ). This review was accompanied in the issue by a number of new investigations into local adaptation in nature (e.g., Delmas et al., ; Kroner, Mabon, Corbiere, Montarry, & Andrivon, ; Parratt, Barres, Penczykowski, & Laine, ; Persoons et al., ; Petit et al., ; Pokalyuk et al., ; Robin, Andanson, Saint‐Jean, Fabreguettes, & Dutech, ; Vanhove et al., ; Walker et al., ). A final set of papers took a genomic approach to investigate the genomic basis of local adaptation and to detect the molecular signatures of local adaptation (e.g., Alayon et al., ; Almeida, Barbosa, Bensasson, Goncalves, & Sampaio, ; Badouin et al., ; Branco et al., ; Coi et al., ; De Fine Licht, Jensen, & Eilenberg, ; Nikolin et al., ; Richard et al., ).…”

Pathogenomic Analysis of Wheat Yellow Rust Lineages Detects Seasonal Variation and Host Specificity

“…For P. striiformis , the ability to accurately genotype both the pathogen and host directly in the field using this technique enabled us to study the coexistence of P. striiformis genetic groups and their hosts. The coexistence of distinct genetic groups of a plant pathogen on the same host is widespread (e.g., Melampsora larici-populina , Persoons et al 2016 ; Botrytis cinerea , Fournier and Giraud 2007 ; Puccinia striiformis f. sp. tritici , Hubbard et al 2015 ).…”