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What is pathogen aggressiveness?
          Does it matter?

    If it does what should we do
               about it?


          Chair: Chris Gilligan University of Cambridge
What is aggressiveness?
• Panellists
   – Gene Milus, University of Arkansas
   – Mogens Hovmøller, Aarhus University
   – Robert Park, University of Sydney
Organisation of discussion

• Definitions              • Case studies


• Big questions           • Scientific challenges
   • Epidemiological         • Surveillance
   • Evolutionary            • Measurement
   • Genetical & Breeding    • Management
   • Crop loss

• (Relations with human epidemiology)

 • Actions
Aggressiveness: definition
 • Virulence
     – Pathotype either infects or does not
     – Remarkably important, relatively easy to work with
“This compatibility relationship has so far largely monopolized the attention
of plant pathologists and shaped the discipline.” Periaud et al. (2009)

 • Aggressiveness
     – Quantitative measure of pathogenicity & spread
     – Manifest by spread of new strains
        – Population level:    rate of spread
        – Host plant level:     yield loss & infectiousness
Aggressiveness: case studies

• Puccinia striiformis
• Puccinia graminis
• Puccinia triticina

• Many others:
   – Phytophthora infestans
   – Gaeumannomyces graminis
   – Ophiostoma novo-ulmi
   – Melampsora lini Invasion?
   –…                  Persistence?
                       Co-existence?
Components of aggressiveness

• Latent period              • Speeds up infection cycle

• Infection efficiency
• Spore production rate      • Increases rate of transmission
• Lesion size
• Infectious period
                              • Increases host damage
• Production of toxins
• Reduction of photosynthetic activity
• Necrosis
What are the big questions?
• Epidemic perspective:
   – How do changes in aggressiveness affect epidemic dynamics?
      » Invasion, rate of spread, persistence
• Evolutionary perspective:
   – What causes evolutionary change in aggressiveness?
      » How aggressive can a pathogen go?
      » Are evolutionary changes affected by crop management?
• Genetical and breeding perspective
   – Is aggressiveness heritable and predictable?
   – How should it affect breeding strategies?
• Yield perspective:
   – How does increased aggressiveness affect crop loss?
      » Trade-off: crop loss vs spread
Epidemiological perspective
  Adjusting the components of aggressiveness can lead to all
                   or nothing responses

• Infection efficiency             R0 > 1 for epidemic invasion
                                   R0 < 1 no epidemic invasion
• Spore production rate
• Lesion size                        Phase transition from no
• Infectious period               invasion to sudden invasion by
                                     adjusting components of
                                          aggressiveness
                                     Ieq


                                    Ieq
       R0
   “Reproductive                          0
                                              0   1   2    3   4
     number”                                          R0
                                                      R0
Epidemiological perspective
  Adjusting the components of aggressiveness can lead to all
                   or nothing responses

• Infection efficiency                    R0 just greater than 1:
                                           variability matters
• Spore production rate
• Lesion size
• Infectious period                                 Infecteds




       R0
   “Reproductive
     number”

                                  Gilligan, C.A. & van den Bosch, F. (2008) Ann rev. Phytopathol 46: 385-418
Evolutionary perspectives
                            Trade-offs matter: accounting for
                                 absence of excessively aggressive pathotypes
                                 selection of generalists and specialists

Consider trade-off in
 transmission rates
Infectivity to host 2
Infectivity to host 2




                        Infectivity to host 1        Gudelj, I., van den Bosch, F. and Gilligan, C. A. (2004). Proc.Roy. Soc. Ser. B 271: 2187-2194.
                                                van den Berg, F. Gilligan C.A. Bailey D.J. and van den Bosch, F. (2010). Phytopathology 100: 1169-1175
Organisation of discussion

• Definitions              • Case studies


• Big questions           • Scientific challenges
   • Epidemiological         • Surveillance
   • Evolutionary            • Measurement
   • Genetical & Breeding    • Management
   • Crop loss

• (Relations with human epidemiology)

 • Actions
What are the big questions?
• Epidemic perspective:
   – How do changes in aggressiveness affect epidemic dynamics?
      » Invasion, rate of spread, persistence
• Evolutionary perspective:
   – What causes evolutionary change in aggressiveness?
      » How aggressive can a pathogen go?
      » Are evolutionary changes affected by crop management?
• Genetical and breeding perspective
   – Is aggressiveness heritable and predictable?
   – How should it affect breeding strategies?
• Yield perspective:
   – How does increased aggressiveness affect crop loss?
      » Trade-off: crop loss vs spread
Relations with human epidemiology
Human pathogens

 Within hosts
   • ‘Virulence’
       • Quantity of damage induced by pathogen on host
       • Driven by within-host pathogen multiplication
 Between hosts
   • Pathogen fitness
       • Host => Host transmission
       • Usually assessed by R0
       • Includes multiplication and survival


                                    Galvani, A.P. (2003) Trends in Ecology & Evolution 18: 132-139
Adaptive potential of aggressiveness components

• Variability within pathogen populations

• Heritability of aggressiveness components

• Differential Cv x Isolate interactions

• Trade-off: virulence vs aggressiveness

• Genetic correlations between quantitative traits

• Adaptation to environmental conditions


                 Periaud, B., Ravigné, V., Halkett,F., Goyeau, H. Carlier, J. Lannou, C. (2009) Plant Pathology 58: 409-424
Evolutionary perspectives
                         2) Quantitatively-resistant crops
                               could result in selection for increased pathogen aggressiveness

                            Trade-off: for P. triticina
Total spore production




                                                                                                      Total number of spores produced
                                                                                                                                        250
                                                                                                                                                                              a
                                                                                                                                        200                                                 Susceptible
                                                                                                                                                                                  c   b
                                                                                                                                        150
                                                                                                                                                                                            Resistant
                                                                                                                                        100

                                                                                                                                         50

                                                                                                                                          0
                                                                                                                                              0.0   0.2      0.4     0.6      0.8     1.0

                                                                                                                                                          Lesion size (mm2)
                               Lesion size




                            van den Berg, F., Lannou, C. Pariaud, B., Gilligan, C. A. and van den Bosch, F. Quantitative resistance can select for increased
                            aggressiveness through pathogen traits not related to resistance breaking in Puccinia triticina (Under review)

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What is Pathogen Aggressiveness?

  • 1. What is pathogen aggressiveness? Does it matter? If it does what should we do about it? Chair: Chris Gilligan University of Cambridge
  • 2. What is aggressiveness? • Panellists – Gene Milus, University of Arkansas – Mogens Hovmøller, Aarhus University – Robert Park, University of Sydney
  • 3. Organisation of discussion • Definitions • Case studies • Big questions • Scientific challenges • Epidemiological • Surveillance • Evolutionary • Measurement • Genetical & Breeding • Management • Crop loss • (Relations with human epidemiology) • Actions
  • 4. Aggressiveness: definition • Virulence – Pathotype either infects or does not – Remarkably important, relatively easy to work with “This compatibility relationship has so far largely monopolized the attention of plant pathologists and shaped the discipline.” Periaud et al. (2009) • Aggressiveness – Quantitative measure of pathogenicity & spread – Manifest by spread of new strains – Population level: rate of spread – Host plant level: yield loss & infectiousness
  • 5. Aggressiveness: case studies • Puccinia striiformis • Puccinia graminis • Puccinia triticina • Many others: – Phytophthora infestans – Gaeumannomyces graminis – Ophiostoma novo-ulmi – Melampsora lini Invasion? –… Persistence? Co-existence?
  • 6. Components of aggressiveness • Latent period • Speeds up infection cycle • Infection efficiency • Spore production rate • Increases rate of transmission • Lesion size • Infectious period • Increases host damage • Production of toxins • Reduction of photosynthetic activity • Necrosis
  • 7. What are the big questions? • Epidemic perspective: – How do changes in aggressiveness affect epidemic dynamics? » Invasion, rate of spread, persistence • Evolutionary perspective: – What causes evolutionary change in aggressiveness? » How aggressive can a pathogen go? » Are evolutionary changes affected by crop management? • Genetical and breeding perspective – Is aggressiveness heritable and predictable? – How should it affect breeding strategies? • Yield perspective: – How does increased aggressiveness affect crop loss? » Trade-off: crop loss vs spread
  • 8. Epidemiological perspective Adjusting the components of aggressiveness can lead to all or nothing responses • Infection efficiency R0 > 1 for epidemic invasion R0 < 1 no epidemic invasion • Spore production rate • Lesion size Phase transition from no • Infectious period invasion to sudden invasion by adjusting components of aggressiveness Ieq Ieq R0 “Reproductive 0 0 1 2 3 4 number” R0 R0
  • 9. Epidemiological perspective Adjusting the components of aggressiveness can lead to all or nothing responses • Infection efficiency R0 just greater than 1: variability matters • Spore production rate • Lesion size • Infectious period Infecteds R0 “Reproductive number” Gilligan, C.A. & van den Bosch, F. (2008) Ann rev. Phytopathol 46: 385-418
  • 10. Evolutionary perspectives Trade-offs matter: accounting for absence of excessively aggressive pathotypes selection of generalists and specialists Consider trade-off in transmission rates Infectivity to host 2 Infectivity to host 2 Infectivity to host 1 Gudelj, I., van den Bosch, F. and Gilligan, C. A. (2004). Proc.Roy. Soc. Ser. B 271: 2187-2194. van den Berg, F. Gilligan C.A. Bailey D.J. and van den Bosch, F. (2010). Phytopathology 100: 1169-1175
  • 11. Organisation of discussion • Definitions • Case studies • Big questions • Scientific challenges • Epidemiological • Surveillance • Evolutionary • Measurement • Genetical & Breeding • Management • Crop loss • (Relations with human epidemiology) • Actions
  • 12. What are the big questions? • Epidemic perspective: – How do changes in aggressiveness affect epidemic dynamics? » Invasion, rate of spread, persistence • Evolutionary perspective: – What causes evolutionary change in aggressiveness? » How aggressive can a pathogen go? » Are evolutionary changes affected by crop management? • Genetical and breeding perspective – Is aggressiveness heritable and predictable? – How should it affect breeding strategies? • Yield perspective: – How does increased aggressiveness affect crop loss? » Trade-off: crop loss vs spread
  • 13.
  • 14. Relations with human epidemiology Human pathogens Within hosts • ‘Virulence’ • Quantity of damage induced by pathogen on host • Driven by within-host pathogen multiplication Between hosts • Pathogen fitness • Host => Host transmission • Usually assessed by R0 • Includes multiplication and survival Galvani, A.P. (2003) Trends in Ecology & Evolution 18: 132-139
  • 15. Adaptive potential of aggressiveness components • Variability within pathogen populations • Heritability of aggressiveness components • Differential Cv x Isolate interactions • Trade-off: virulence vs aggressiveness • Genetic correlations between quantitative traits • Adaptation to environmental conditions Periaud, B., Ravigné, V., Halkett,F., Goyeau, H. Carlier, J. Lannou, C. (2009) Plant Pathology 58: 409-424
  • 16.
  • 17. Evolutionary perspectives 2) Quantitatively-resistant crops could result in selection for increased pathogen aggressiveness Trade-off: for P. triticina Total spore production Total number of spores produced 250 a 200 Susceptible c b 150 Resistant 100 50 0 0.0 0.2 0.4 0.6 0.8 1.0 Lesion size (mm2) Lesion size van den Berg, F., Lannou, C. Pariaud, B., Gilligan, C. A. and van den Bosch, F. Quantitative resistance can select for increased aggressiveness through pathogen traits not related to resistance breaking in Puccinia triticina (Under review)