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The Escalatory Red Queen Antoine Persoons, Katherine Hayden, Bénédicte Fabre, Pascal Frey, Stéphane De Mita, Aurélien Tellier, Fabien Halkett

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The Escalatory Red Queen Antoine Persoons, Katherine Hayden, Bénédicte Fabre, Pascal Frey, Stéphane De Mita, Aurélien Tellier, Fabien Halkett The escalatory Red Queen Antoine Persoons, Katherine Hayden, Bénédicte Fabre, Pascal Frey, Stéphane de Mita, Aurélien Tellier, Fabien Halkett To cite this version: Antoine Persoons, Katherine Hayden, Bénédicte Fabre, Pascal Frey, Stéphane de Mita, et al.. The escalatory Red Queen: Population extinction and replacement following arms race dynamics in poplar rust. Molecular Ecology, Wiley, 2017, 26 (7), pp.1902-1918. 10.1111/mec.13980. hal-01564550 HAL Id: hal-01564550 https://hal.archives-ouvertes.fr/hal-01564550 Submitted on 18 Jul 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Molecular Ecology (2017) 26, 1902–1918 doi: 10.1111/mec.13980 MICROBIAL LOCAL ADAPTATION The escalatory Red Queen: Population extinction and replacement following arms race dynamics in poplar rust 1 2 ANTOINE PERSOONS,* KATHERINE J. HAYDEN,* BENEDICTE FABRE,* PASCAL FREY,* STEPHANE DE MITA,* AURELIEN TELLIER† and FABIEN HALKETT* *UMR IAM, INRA, Universite de Lorraine, 54000 Nancy, France, †Section of Population Genetics, Center of Life and Food Sciences Weihenstephan, Technische Universit€at Munchen,€ 85354 Freising, Germany, 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 fun- gus, Melampsora larici-populina. A major adaptive event occurred in 1994 with the breakdown of R7 resistance carried by several poplar cultivars widely planted in Wes- tern Europe since 1982. The corresponding virulence rapidly spread in M. larici-popu- lina 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 popu- lation, 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. Keywords: gene-for-gene interaction, genetic hitchhiking, parasite, Red Queen hypothesis, temporal sampling Received 29 July 2016; revision accepted 15 December 2016 drivers for the evolution of sexual reproduction Introduction (Lively et al. 1990; Busch et al. 2004; Lively 2010) and Since the publication of the ‘new evolutionary law’ by have illustrated co-evolutionary cycles expected with Van Valen more than 40 years ago (Van Valen 1973), the so-called Red Queen dynamics (e.g. Dybdahl & the metaphor of the Red Queen has fostered numer- Lively 1998; Thrall et al. 2001, 2012; Decaestecker et al. ous developments in evolutionary biology (Brockhurst 2007; Betts et al. 2014). Yet to our knowledge, no et al. 2014). Parasites have been credited as primary study has explicitly tested the core hypothesis of Van Valen (1973): antagonistic co-evolution can lead to Correspondence: Fabien Halkett, Fax: +33 3 83 39 40 69; E-mail: extinction (Dawkins & Krebs 1979). In this article, we [email protected] aim to benefit from a comprehensive and long-lasting 1 Present address: Earlham Institute, Norwich Research Park survey to document population extinction in a plant Innovation Centre, Colney Ln, Norwich NR4 7UH, UK pathogen species facing strong selection exerted by 2Present address: Royal Botanic Garden Edinburgh, 20A Inver- leith Row, Edinburgh EH3 5LR, UK host resistance. © 2016 John Wiley & Sons Ltd GENETIC REVOLUTION AFTER RESISTANCE BREAKDOWN 1903 Plant systems lend themselves to studying the occur- the hosts (Tellier et al. 2014). Recent findings support rence and the mechanisms of extinction events due to the theory with effector genes showing elevated levels host–parasite dynamics, as much is known on the of nonsynonymous polymorphisms (Poppe et al. 2015). molecular basis of the interactions. In plants, major Theory also predicts that extinction of host and/or par- resistance to fungal pathogens relies on the so-called asite populations following co-evolution should occur gene-for-gene interaction (Flor 1971). In the simplest under arms races rather than under trench warfare sce- set-up, the outcome of infection is determined by one narios (Dawkins & Krebs 1979; Brockhurst et al. 2014). locus in the plant (the resistance (R) gene) and in the Therefore, understanding the mechanisms linking allele pathogen (the infectivity gene). One allele of the patho- fixation in host and pathogen populations and the gen infectivity gene, which is termed hereafter as the extinction of a host or parasite species (or population at avirulence (Avr) allele as in the plant pathology litera- the intraspecific level) is of fundamental importance for ture, is recognized by plants harbouring a matching testing the Red Queen predictions. resistance allele at the corresponding R-gene. Once the In this study, we investigate the temporal changes in pathogen is recognized, a defence response is triggered population structure in the poplar rust pathogen, (Jones & Dangl 2006). If plants harbour a susceptibility Melampsora larici-populina, which underwent a severe allele – or if the pathogen has the alternative virulence selection event in poplar-cultivating areas (Xhaard et al. allele – infection occurs. In many cultivated crop spe- 2011). Worldwide, Melampsora spp. (Basidiomycota, Puc- cies, such major resistance genes have been favoured in ciniales) are the most damaging pathogens of poplars selection by plant breeders because they provide com- (Vialle et al. 2011), and M. larici-populina is the largest plete control of the disease. However, despite the problem in European poplar plantations (Frey et al. potential for great efficiency, gene-for-gene resistance 2005). Poplars are particularly susceptible to M. larici- may be quickly broken down, as a single mutation in populina because of their intensive monoclonal the pathogen Avr allele can be sufficient to break or cultivation spanning several decades and the probable change its functionality and impair recognition of the counterselection of nonspecific resistance traits during plant R-gene, thereby restoring virulence (Schulze- breeding (Gerard et al. 2006). Eight resistances (R1 to Lefert et al. 1997). In this case, the so-called resistance R8) have been described in poplar so far (Pinon & Frey breakdown is accompanied by the possible fixation of 2005). Most of them have been deployed in European the virulence allele in the parasite population. Infecti- plantations, and all have been overcome by M. larici- vity loci code for pathogenicity factors, also known as populina (Pinon & Frey 2005). The most economically effectors, which accordingly contribute to the success of damaging resistance breakdown occurred when the pathogen infection. Virulent individuals are often widely planted R7 resistance was overcome and led to shown to exhibit a fitness penalty (the so-called viru- the invasion of France by Vir7 M. larici-populina individ- lence cost) when compared to individuals harbouring uals (Fig. 1). Several poplar cultivars bear the R7 resis- the Avr allele on susceptible plants (Huang et al. 2006; tance, among which Populus 9 interamericana ‘Beaupre’ Bahri et al. 2009a; Montarry et al. 2010). was the most popular, accounting for 57% of the stems Over time, a wide range of dynamics in changes in planted in France in 1996, and as much as 80% in north- allele frequencies in plant and pathogen populations ern France (Pinon & Frey 2005). Conversely, other resis- can be observed. At one end of the spectrum, we find tance types (including R1 to R5) have been planted at a trench-warfare dynamics, in which polymorphism is low and constant frequency since the 1950s (Pinon & maintained in the plant and pathogen populations, as Frey 2005). The first report of R7 resistance breakdown has been shown in several wild species (Thrall et al. occurred in 1994 in Belgium and northern France (Pinon 2001, 2012). At the other end, arms races can occur with & Frey 2005). In fewer than 5 years, Vir7 individuals recurrent fixation of new resistance and virulence alleles spread all over Western Europe and went on to cause in plant and pathogen populations. The ecological con- very destructive epidemics on all cultivated poplar ditions and life history
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