Topic 1 : How do pathogen/pest populations respond to deployment of host resistance?

1. Topic 1: How do pathogen/pest populations respond to deployment of host resistance? • Natural vs. human-managed systems • Selective effects of qualitative resistance (R genes) • How does evolution to virulence affect pathogens – is there a cost to virulence? • Can durability of R genes be predicted? • Selective effects of quantitative (partial) resistance • Evolution of pathogen populations with host-selective toxins (HSTs) • What affects evolutionary potential of pathogen populations

2. Terminology • Using Vanderplank’s definitions: • Virulence: specific disease-causing ability • Aggressiveness: non-specific disease-causing ability

3. virulent avirulent less aggressive more aggressive

4. Terminology • Using Vanderplank’s definitions: • Virulence: specific disease-causing ability • Aggressiveness: non-specific disease-causing ability • Other definitions are used, especially in host-pathogen co-evolution (natural systems, human infectious diseases) • Virulence: damage a pathogen strain causes to a host

5. Natural, co-evolving systems (vs. artificial, agricultural/horticultural systems) • In co-evolving systems • “Arms race” model (discussed in Holub, 2001, “The arms race is ancient history in Arabidopsis, the wildflower,” Nat. Rev. Genet. 2:516-527.) • Transient polymorphism: continual selective turnover of alleles; • “Selective sweeps” where R genes driven to extinction

6. Arms race model • Evolution of R genes in local populations: transient polymorphism model of co-evolving host-pathogen system (Holub et al) • Resistance alleles would be relatively young, nearly identical in sequence to susceptible alleles

7. In contrast: the “trench warfare” model of natural (co-evolutionary) systems: • Balanced or “dynamical” polymorphism rather than selective sweeps • Epidemics alternate with periods of high host resistance and low pathogen population • Resistance and susceptibility alleles would be old, differ greatly in DNA sequence

8. Trench warfare or “balanced polymorphism” model – natural Arabidopsis system • Around Rpm1 deletion site, divergence between R and S alleles indicates Rpm1 polymorphism arose 9.8 million years ago – old!

9. Natural system 1: Puccinia coronata on Avena sterilis (wild oat) in Israel, a stable coevolving pathosystem in the center of origin • Virulence/resistance polymorphisms are highly diverse – • extreme genetic diversity in the host (many resistance types) • matched by broad range of virulence patterns in pathogen • accumulation of many R and Vir genes • Balancing selection -- natural selection prevented from going to fixation of R genes and Vir genes • Durability of resistance -- prevalence of low-reaction resistance types over 17 years; Pc genes effective in the 1960s and 1970s are still effective against a large proportion of isolates 20-30 years later • “…An example of stability of wild pathosystems that consist of natural mixtures of resistance and virulence.” Leonard et al, 2004, Phytopathology 94:505-514

10. Natural system 2: Melampsora lini on Linum marginale (wild flax) in southeastern Australia Jeremy Burdon, Peter Thrall & colleagues – CSIRO 15 yrs of studies on Kiandra Plain, Kosciuszko National Park

11. L. marginale frequently composed of many different host resistance phenotypes distributed unevenly through the deme • Sympatric M. lini populations also typically diverse, although sometimes dominated by just a few pathotypes • Year-to-year fluctuations in incidence and frequency of pathotypes suggest population bottlenecks and subsequent genetic drift • “The tight frequency-dependent cycling predicted by early gene-for-gene models is not evident at the individual population level.” http://www.anbg.gov.au/cpbr/program/sc/evol_host.htm

12. Thrall & Burdon, 2003, Science 299:1735-1737

13. Why don’t virulent M. lini strains dominate and wipe out susceptible host populations? • More resistant host populations select for more virulent pathogen populations • Virulence (complexity) is favored (over aggressiveness) in resistant host populations • Aggressiveness is favored (over virulence) in susceptible host populations • Suggests a cost of virulence – no benefit to carrying virulence genes in the absence of corresponding R genes

15. Natural system 3: powdery mildew (Podosphaera plantaginis) on Plantago lanceolata (ribwort)on a Finnish island Laine, A. 2004. J. Ecology, 92:990-1000 • Multi-year studies of natural populations of weed host and obligate biotroph pathogen • High extinction and colonization rates • Only 5% of host populations infected at a given time

16. 1 isolate derived from each of 4 infected populations (red circles) • 8 plants x 8 pops = 64 plants challenged with each of 4 isolates • Responses: 0 or 1 • Results: • Highly diverse host resistance phenotypes using just 4 isolates • Overall susceptibility high: 55% of plants susc. to at least 3 strains • But differences in mean resistance level of local populations appear to retard spread of pathogen

17. 1 isolate derived from each of 4 infected populations (red circles) • 8 plants from each of 8 pops were challenged with each of 4 isolates • Responses: 0 or 1 • Results: • Highly diverse host resistance phenotypes using just 4 isolates • Overall susceptibility high: 55% of plants susc. to at least 3 strains • But differences in mean resistance level of local populations appear to retard spread of pathogen

18. Mean percentages of resistant plants higher in non-infected populations than in infected populations Only 5% of host populations infected at a given time; high extinction & colonization rates

19. Natural system 4: long-mouthed weevil and Japanese camellia in Japan (obligate parasite – trying to lay eggs in seeds) Bore holes Drilling with rostrum Geographic variation in rostrum length (9-19 mm) Matching variation in pericarp thickness (6-20 mm) Toju, H. 2009. Natural selection drives the fine-scale divergence of a coevolutionary arms race involving a long-mouthed weevil and its obligate host plant. BMC Evolutionary Biology 9:273

20. Pericarp thickness is a heritable quantitative trait • Camellia fitness is proportion or number of intact seeds (= resistance)

21. Fitness is positively correlated with pericarp thickness • Gene flow of both spp. restricted  fine-scale differentiation of pops. • The evolutionary interaction varies at a fine spatial scale • Not all interacting Yakushima weevil/camellia populations have evolved to have long rostra and thick pericarps • Strength of selection for thicker pericarps varies geographically; pericarp thickness at which weevil excavations are 50% successful varies geographically • Evolution of thicker pericarps (and presumably long rostra) restricted by the cost of the trait

22. Geographic mosaic theory of co-evolution (John Thompson, UC Santa Cruz) • Forms and strength of natural selection on interacting species vary among populations (“geographic selection mosaic”) • Co-evolutionary “coldspots” and “hotspots” of reciprocal selection

23. Geographic mosaic theory of co-evolution • Gene flow, genetic drift, extinction of local populations promote geographic structuring (patchiness) • Perturb/promote local adaptation of interacting spp. (“trait remixing”) • May swamp local selection

24. Predictions of geographic mosaic theory of co-evolution • Co-evolving traits vary among populations • Traits are well-matched in some local communities and not in others • There may routinely be local transient mixtures of apparently mal-adaptive traits • Few co-evolving traits or underlying alleles will be widespread across geographic ranges or fixed within interacting spp. Toju, Yakushima island

25. More on evolution of resistance and virulence in natural systems: • Tellier and Brown, 2007, Polymorphism in multilocus host–parasite coevolutionary interactions, Genetics,177: 1777–1790. • Thrall and Burdon, 1997, Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial, Journal of Ecology 85:743-753 • Thompson and Burdon, 1992, Gene-for-gene coevolution between plants and parasites, Nature 360:121-597

26. Some conclusions from natural systems • There is substantial polymorphism at R and Avr loci both within populations and across spatially separated subpopulations • Some of these polymorphisms are ancient, indicating that selective forces are preserving them • Spatial dynamics are key: • The stability of host-parasite interactions is strongly affected by spatial substructuring • Patchiness promotes persistence of resistance/ virulence polymorphisms • Damaging regional epidemics are rare in natural systems

27. Characteristic Human-managed plant systems Natural plant systems • Reciprocal selection (co-evolution • No • Not influenced by host dispersal capabilities • Host mobility • Influenced by host dispersal capabilities • Yes • Diversity of vir-avir polymorphisms • Often highly diverse • Often very limited • Presented over large contiguous areas • Spatial extent of particular resistance genes • Confined to relatively small areas; patchy • Host fitness (e.g., seed production) • Outcome of co-evolutionary processes • Ensured with pesticides • R genes often obsolete within a few years • Durability of resistance alleles • Resistance genes expected to be ancient and durable • Battle model • Trench warfare? Epidemics alternate with period of low pathogen population • Arms race?