Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation

Ecology Letters

Volumn 15, Issue 5, 2012, Pages 425-435

  Thrall, Peter H ^a   Laine, Anna Liisa ^a,b   Ravensdale, Michael ^a,c   Nemri, Adnane ^a   Dodds, Peter N ^a   Barrett, Luke G ^a   Burdon, Jeremy J ^a  

^a CSIRO   (Australia)

^b UNIVERSITY OF HELSINKI   (Finland)

^c OTTAWA RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

Avirulence; Disease; Epidemiology; Gene for gene; Infectivity; Negative frequency dependence; Pathogen effectors; Red Queen; Resistance; Selective sweeps

Indexed keywords

ALLELE; ANTAGONISM; ARMS RACE; COEVOLUTION; DICOTYLEDON; DISEASE PREVALENCE; EPIDEMIOLOGY; FITNESS; FREQUENCY DEPENDENCE; FUNGUS; GENETIC VARIATION; HOST-PATHOGEN INTERACTION; INFECTIVITY; LOCAL ADAPTATION; METAPOPULATION; NATURAL SELECTION; PATHOGEN; PHENOTYPE; POLYMORPHISM; RED QUEEN HYPOTHESIS;

ARTICLE; BASIDIOMYCETES; DISEASE RESISTANCE; EVOLUTION; FLAX; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOST PARASITE INTERACTION; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY;

BASIDIOMYCOTA; BIOLOGICAL EVOLUTION; DISEASE RESISTANCE; FLAX; GENETIC VARIATION; GENOTYPE; HOST-PARASITE INTERACTIONS;

LINUM; MELAMPSORA;

EID: 84859423134     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2012.01749.x     Document Type: Article

References (50)

1. Altermatt, F. & Ebert, D. (2008). Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol. Lett., 11, 918-928.
2. Anderson, M.J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
3. Barrett, L.G., Thrall, P.H., Burdon, J.J., Nicotra, A.B. & Linde, C.C. (2008). Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Mol. Ecol., 17, 3401-3415.
4. Barrett, L.G., Thrall, P.H., Dodds, P.N., van der Merwe, M., Linde, C.C., Lawrence, G.J. et al. (2009). Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Mol. Biol. Evol., 26, 2499-2513.
5. Bergelson, J., Kreitman, M., Stahl, E.A. & Tian, D. (2001). Evolutionary dynamics of plant R-genes. Science, 292, 2281-2285.
6. Brockhurst, M.A., Morgan, A.D., Rainey, P.B. & Buckling, A. (2003). Population mixing accelerates coevolution. Ecol. Lett., 6, 975-979.
7. Brockhurst, M.A., Morgan, A.D., Fenton, A. & Buckling, A. (2007). Experimental coevolution with bacteria and phage: the Pseudomonas fluorescens-φ{symbol}2 model system. Infect. Genet. Evol., 7, 547-552.
8. Brown, J.K.M. & Tellier, A. (2011). Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol., 49, 1-23.
9. Burdon, J.J. (1994). The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale. Evolution, 48, 1564-1575.
10. Burdon, J.J. & Thompson, J.N. (1995). Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. J. Ecol., 83, 199-206.
11. Burdon, J.J., Thrall, P.H. & Brown, A.H.D. (1999). Resistance and virulence structure in two Linum marginale-Melampsora lini host-pathogen metapopulations with different mating systems. Evolution, 53, 704-716.
12. Catanzariti, A.-M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. & Ellis, J.G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 18, 243-256.
13. Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., Stoks, R., Van Kerckhoven, L., Ebert, D. et al. (2007). Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature, 450, 870-873.
14. Dodds, P.N. & Rathjen, J.R. (2010). Plant Immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Gen., 11, 539-548.
15. Dodds, P. & Thrall, P.H. (2009). Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust. Funct. Plant Biol., 36, 395-408.
16. Dybdahl, M.F. & Lively, C.M. (1998). Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution, 52, 1057-1066.
17. Ebert, D. (2008). Host-parasite coevolution: insights from the Daphnia-parasite model system. Curr. Opin. Microbiol., 11, 290-301.
18. Gaba, S. & Ebert, D. (2009). Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol. Evol., 24, 226-232.
19. Gandon, S., Buckling, A., Decaestecker, E. & Day, T. (2008). Host-parasite coevolution and patterns of adaptation across time and space. J. Evol. Biol., 21, 1861-1866.
20. Gomez, P. & Buckling, A. (2011). Bacteria-phage antagonistic coevolution in soil. Science, 332, 106-109.
21. Gomulkiewicz, R., Thompson, J.N., Holt, R.D., Nuismer, S.L. & Hochberg, M.E. (2000). Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am. Nat., 156, 156-174.
22. Hall, A.R., Scanlan, P.D., Morgan, A.D. & Buckling, A. (2011). Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett., 14, 635-642.
23. Jones, J.D. & Dangl, J.L. (2006). The plant immune system. Nature, 444, 323-329.
24. Koskella, B. & Lively, C.M. (2009). Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution, 63, 2213-2221.
25. Laine, A.-L. (2006). Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc. R. Soc. Lond. B, 273, 267-273.
26. Laine, A.-L. & Tellier, A. (2008). Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos, 117, 1281-1288.
27. Lawrence, G.J. & Burdon, J.J. (1989). Flax rust from Linum marginale- variation in a natural host pathogen interaction. Can. J. Bot., 67, 3192-3198.
28. Leonard, K.J. & Czochor, R.J. (1970). Theory of genetic interactions among populations of plants and their pathogens. Annu. Rev. Phytopathol., 18, 237-258.
29. Lively, C.M. (2010). The effect of host genetic diversity on disease spread. Am. Nat., 175, E149-E152.
30. Lively, C.M., Dybdahl, M.F., Jokela, J., Osnas, E.E. & Delph, L.F. (2004). Host sex and local adaptation by parasites in a snail-trematode interaction. Am. Nat., 164, S6-S18.
31. Lockett, S.F., Robertson, J.R., Brettle, R.P., Yap, P.L., Middleton, D. & Leigh Brown, A.J. (2001). Mismatched human leukocyte antigen alleles protect against heterosexual HIV transmission. J. Acq. Immun. Def. Synd., 27, 277-280.
32. Obbard, D.J., Jiggins, F.M., Bradshaw, N.J. & Little, T.J. (2011). Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol. Biol. Evol., 28, 1043-1056.
33. Paterson, S., Wilson, K. & Pemberton, J.M. (1998). Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). P. Natl. Acad Sci. USA, 95, 3714-3719.
34. Paterson, S., Vogwill, T., Buckling, A., Benmayor, R., Spiers, A.J., Thomson, N.R. et al. (2010). Antagonistic coevolution accelerates molecular evolution. Nature, 464, 275-278.
35. Poullain, V., Gandon, S., Brockhurst, M.A., Buckling, A. & Hochberg, M.E. (2008). The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution, 62, 1-11.
36. Salathé, M., Scherer, A. & Bonhoeffer, S. (2005). Neutral drift and polymorphism in gene-for-gene systems. Ecol. Lett., 8, 925-932.
37. SAS Institute (1999). SAS/STAT Software User's Guide. Release 8.00. SAS Institute Inc., Cary, NC.
38. Sasaki, A. (2000). Host-parasite coevolution in a multilocus gene-for-gene system. Proc. Roy. Soc. Lond. B, 267, 2183-2188.
39. Smith, D.L., Ericson, L. & Burdon, J.J. (2003). Epidemiological patterns at multiple spatial scales: an 11-year study of a Triphragmium ulmariae-Filipendula ulmaria metapopulation. J. Ecol., 91, 890-903.
40. Soubeyrand, S., Laine, A.-L., Hanski, I. & Penttinen, A. (2009). Spatio-temporal structure of host-pathogen interactions in a metapopulation. Am. Nat., 174, 308-320.
41. Stahl, E.A., Dwyer, G., Mauricio, R., Kreitman, M. & Bergelson, J. (1999). Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature, 400, 667-671.
42. Stukenbrock, E.H. & McDonald, B.A. (2009). Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol. Plant Microbe Interact., 22, 371-380.
43. Thompson, J.N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.
44. Thrall, P.H. & Burdon, J.J. (2000). Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant. Pathol., 49, 767-773.
45. Thrall, P.H. & Burdon, J.J. (2002). Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant. Pathol., 51, 169-184.
46. Thrall, P.H. & Burdon, J.J. (2003). Evolution of virulence in a plant host-pathogen metapopulation. Science, 299, 1735-1737.
47. Thrall, P., Burdon, J. & Young, A. (2001). Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. J. Ecol., 89, 736-748.
48. Thrall, P.H., Burdon, J.J. & Bever, J.D. (2002). Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution, 56, 1340-1351.
49. Tian, D., Traw, M.B., Chen, J.Q., Kreitman, M. & Bergelson, J. (2003). Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature, 423, 74-77.
50. van Valen, L. (1973). A new evolutionary law. Evol. Theor., 1, 1-30.