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Impact of density and disease on frequency-dependent selection and genetic polymorphism: experiments with stripe rust and wheat

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Abstract

Frequency-dependent disease impacts may contribute to the maintenance of genetic diversity and sexual reproduction in plant populations. In earlier work with experimental wheat (Triticum aestivum) populations at a single density, we found that stripe rust (caused by Puccinia striiformis) created frequency-dependent selection on its host but competitive interactions between host genotypes reduced the potential for disease to maintain genetic polymorphisms in this highly self-pollinated species; the weaker competitor actually exhibited positive disease-mediated frequency-dependent selection. Based on these results we predicted that at low density, where the overall level of competition is lower, disease would have a stronger impact relative to competition and thus be more likely to maintain genetic polymorphisms; at low densities the greatest effect of disease for negative frequency-dependent selection should be seen in the weak competitor. Here we report on results with wheat stripe rust in which we altered both the frequency and density of host genotypes in factorial combinations of two-way mixtures where each host genotype was attacked by its own specialized race of rust. Within each density disease levels increased with genotype frequencies, creating frequency-dependent disease attack at all densities. Similarly, disease created negative frequency-dependent selection on its host at all densities, as a genotype’s fitness was often greater at low than high frequency when disease was present. Disease levels increased with plant density in 1997 but decreased in 1998. While increasing plant density reduced absolute fitness, presumably as a result of increased competition, a genetic polymorphism was not more likely to be maintained at low than high density as we had predicted. Within each density, the impact of disease was insufficient to reverse the slope of the relationship between absolute fitness and planted frequency from positive to negative for the less competitive host genotype, thus preventing the maintenance of a genetic polymorphism.

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References

  • Allard RW, Adams J (1969) Population studies in predominantly self-pollinating species. XIII. Intergenotypic competition and population structure in barley and wheat. Am Nat 103:621–645

    Article  Google Scholar 

  • Akanda SI, Mundt CC (1996) Effects of two-component wheat cultivar mixtures on stripe rust severity. Phytopathology 86:347–353

    Article  Google Scholar 

  • Alexander HM, JJ Burdon (1984) The effect of disease induced by Albugo candida (white rust) and Peronospora parsitica (Downy mildew) on the survival and reproduction of Capsella bursa-pastoris (shepherd’s purse). Oecologia 64:314–318

    Article  Google Scholar 

  • Alexander HM, Roelfs AP, Cobbs G (1986) Effects of disease and plant competition on yield in monocultures and mixtures of two wheat cultivars. Plant Pathol 35:457–465

    Article  Google Scholar 

  • Alexander HM (1991) Plant population heterogeneity and pathogen and herbivore levels: a field experiment. Oecologia 86:125–131

    Article  Google Scholar 

  • Alexander HM (1992) Evolution of disease resistance in natural plant populations. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. The University of Chicago Press, Chicago, pp 326–344

    Google Scholar 

  • Alexander HM, Antonovics J, Kelly AW (1993) Genotypic variation in plant disease resistance: physiological resistance in relation to field disease transmission. J Ecol 81:325–333

    Article  Google Scholar 

  • Antonovics J, Ellstrand NC (1984) Experimental studies of the evolutionary significance of sexual reproduction. I. A test of the frequency-dependent selection hypothesis. Evolution 38: 103–115

    Article  Google Scholar 

  • Antonovics J, Kareiva P (1988) Frequency-dependent selection and competition: empirical approaches. Phil Trans R Soc Lond B 319: 601–613

    Article  CAS  Google Scholar 

  • Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings. Experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61: 211–217

    Article  Google Scholar 

  • Bergelson J (1990) Life after death: site pre-emption by the remains of Poa annua. Ecology 71: 2157–2165

    Article  Google Scholar 

  • Boudreau MA, Mundt CC (1997) Ecological approaches to disease control. In: Rechcigl J, Rechcigl N (eds) Environmentally safe approaches to crop disease control. CRC/Lewis Press, Boca Raton, FL

    Google Scholar 

  • Brophy LS, Mundt CC (1991) Influence of plant spatial patterns on disease dynamics, plant competition and grain-yield in genetically diverse wheat populations. Agric Ecosyst Environ 35: 1–12

    Article  Google Scholar 

  • Brunet J, Mundt CC (2000a) Disease, frequency-dependent selection, and genetic polymorphisms: experiments with stripe rust and wheat. Evolution 54: 406–414

    PubMed  CAS  Google Scholar 

  • Brunet J, Mundt CC (2000b) Effects of competition on resistance gene polymorphism in a plant/pathogen system. Heredity 85:393–400

    Article  PubMed  CAS  Google Scholar 

  • Brunet J, Mundt CC (2000c) Combined effects of disease and competition on plant fitness. Can J Bot 78:646–654

    Article  Google Scholar 

  • Burdon JJ (1994) The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale. Evolution 48:1564–1575

    Article  Google Scholar 

  • Burdon JJ, Chilvers GA (1982) Host density as a factor in plant disease ecology. Annu Rev Phytopathol 20:143–166

    Article  Google Scholar 

  • Burdon JJ, Jarosz AM (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: I. Patterns of resistance and racial variation in a large host population. Evolution 45:205–217

    Article  Google Scholar 

  • Burdon JJ, Thompson JN (1995) Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. J Ecol 83:199–206

    Article  Google Scholar 

  • Burdon JJ, Thrall PH (1999) Spatial and temporal patterns in coevolving plant and pathogen associations. Am Nat 153:S15–S33

    Article  Google Scholar 

  • Campbell CL, Madden LV (1990) Introduction to plant disease epidemiology. Wiley, New York

    Google Scholar 

  • Clarke DD (1997) The genetic structure of natural pathosystems. In: Crute IR, Holub EB, Burdon JJ (eds) The gene-for-gene relationship in plant-parasite interactions. Bios Scientific, Lancaster, pp 231–243

    Google Scholar 

  • Clay K, Kover PX (1996) The red queen hypothesis and plant/pathogen interactions. Annu Rev Phytopathol 34:29–50

    Article  PubMed  CAS  Google Scholar 

  • Darwinkel A (1978) Patterns of tillering and grain production of winter wheat at a wide range of plant densities. Neth J Agric Sci 26:383–398

    Google Scholar 

  • Dybdahl MF, Lively CM (1998) Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52:1057–1066

    Article  Google Scholar 

  • Finckh MR, Mundt CC (1992a) Plant competition and disease in genetically diverse wheat populations. Oecologia 91:81–92

    Google Scholar 

  • Finckh MR, Mundt CC (1992b) Stripe rust yield and plant competition on yield of wheat cultivar mixtures. Phytopathology 82:905–913

    Article  Google Scholar 

  • Finckh MR, Mundt CC (1993) Effects of stripe rust on the evolution of genetically diverse wheat populations. Theor Appl Genet 85:809–821

    Article  Google Scholar 

  • Finckh MR, Gacek ES, Wolfe MS (1999) Host frequency and density effects on powdery mildew and yield in mixtures of barley cultivars. Plant Pathol 48:807–816

    Article  Google Scholar 

  • Firbank LG, Watkinson AR (1985) On the analysis of competition within two-species mixtures of plants. J Appl Ecol 22:503–517

    Article  Google Scholar 

  • Firbank LG, Watkinson AR (1990) On the effects of competition: from monocultures to mixtures. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, New York

    Google Scholar 

  • Flor HH (1956) The complementary genic systems in flax and flax rust. Adv. Genet. 8:29–54

    Article  Google Scholar 

  • Frederick JR, Marshall HG (1985) Grain yield and yield components of soft red winter wheat as affected by management practices. Agron J 77:495–499

    Article  Google Scholar 

  • Goldberg DE, Barton AM (1992) Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. Am Nat 139:771–801

    Article  Google Scholar 

  • Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A meta-analysis of competition in field experiments. Am Nat 140:539–572

    Article  Google Scholar 

  • Harper JL (1977) Population biology of plants. Academic Press, New York

    Google Scholar 

  • Jarosz AM, Levy M (1988) Effects of habitat and population structure on powdery mildew epidemics in experimental phlox populations. Phytopathology 78:358–362

    Article  Google Scholar 

  • Jarosz AM, Burdon JJ (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: II. Local and regional variation in patterns of resistance and racial structure. Evolution 45: 1618–1627

    Article  Google Scholar 

  • Jarosz AM, Burdon JJ (1992) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini: III. Influence of pathogen epidemics on host survivorship and flower production. Oecologia 89:53–61

    Article  Google Scholar 

  • Joliffe PA, Minjas AN, Runeckles VC (1984) A reinterpretation of yield relationships in replacement series experiments. J Appl Ecol 21:227–243

    Article  Google Scholar 

  • Kira T, Ogawa H, Shinozaki K (1953) Intraspecific competition among higher plants. I. Competition-density-yield inter-relationships in regularly dispersed populations. J Inst Polytech Osaka Cy Univ Series D 4:1–16

    Google Scholar 

  • Lively CM (1996) Host-parasite coevolution and sex. Bioscience 46:107–114

    Article  Google Scholar 

  • Lively CM, Johnson SG, Delph LF, Clay K (1995) Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology 76:1859–1862

    Article  Google Scholar 

  • Little TJ (2002) The evolutionary significance of parasitism: do parasite-driven genetic dynamics occur ex silico? J Evol Biol 15:1–9

    Article  Google Scholar 

  • Monzeglio U, Stoll P (2005) Spatial patterns and species performances in experimental plant communities. Oecologia 145:619–628

    Article  PubMed  Google Scholar 

  • Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 40:381–410

    Article  PubMed  CAS  Google Scholar 

  • Mundt CC, Brophy LS, Schmitt ME (1995) Disease severity and yield of pure-line wheat cultivars and mixtures in the presence of eyespot, yellow rust, and their combination. Plant Pathol 43:173–182

    Article  Google Scholar 

  • Norris RF, Elmore CL, Rejmanek M, Akey WC (2001) Spatial arrangement, density, and competition between barnyard grass and tomato. Weed Sci 49:61–68

    Article  CAS  Google Scholar 

  • Nunney L (1983) Sex differences in larval competition in Drosophila melanogaster the testing of a competition model and its relevance to frequency-dependent selection. Am Nat 121:67–93

    Article  Google Scholar 

  • Pacala SW (1997) Dynamics of plant competition. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford

    Google Scholar 

  • Parker MA (1985) Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39:713–723

    Article  Google Scholar 

  • Parker MA (1988) Polymorphism for disease resistance in the annual legume Amphicarpaea bracteata. Heredity 60:27–31

    Article  Google Scholar 

  • Parker MA (1989) Disease impact and local genetic diversity in the clonal plant Podophyllum peltatum. Evolution 43:540–547

    Article  Google Scholar 

  • Parker MA (1992) Disease and plant population genetic structure. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. University of Chicago Press, Chicago, pp 345–362

    Google Scholar 

  • Parker MA (1994) Pathogens and sex in plants. Evol Ecol 8:560–584

    Article  Google Scholar 

  • Radosevich SR, Rousch ML (1990) The role of competition in agriculture. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, New York

    Google Scholar 

  • Roy BA (1993) Patterns of rust infection as a function of host genetic diversity and host density in natural populations of the apomictic crucifer, Arabis holboellii. Evolution 47:111–124

    Article  Google Scholar 

  • Roy BA (1998) Differentiating the effects of origin and frequency in reciprocal transplant experiments used to test negative frequency-dependent selection hypotheses. Oecologia 115:73–83

    Article  Google Scholar 

  • SAS Institute, Inc. (1988) SAS/STAT user’s guide, 6.03. SAS Institute, Cary, North Carolina

    Google Scholar 

  • Schmitt J, Antonovics J (1986) Experimental studies of the evolutionary significance of sexual reproduction. IV. Effect of neighbor relatedness and aphid infestation on seedling performance. Evolution 40: 830–836

    Article  Google Scholar 

  • Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285

    Article  Google Scholar 

  • Segal A. Manisterski J, Gischbeck G, Wahl I (1980) How plant populations defend themselves in natural ecosystems. Plant Dis Advanced Treatise 5:75–102

    Google Scholar 

  • Siemens DH, Roy BA (2005) Tests for parasite-mediated frequency-dependent selection in natural populations of an asexual plant species. Evol Ecol 19:321–338

    Article  Google Scholar 

  • Spitters CJT (1983) An alternative approach to the analysis of mixed cropping experiments. 1. Estimation of competition effects. Neth J Agric 31:1–11

    Google Scholar 

  • Stauber LG, Smith RJ, Talbert RE (1991) Density and spatial interference of barnyardgrass (Echinochloa crus-galli) with rice (Oryza sativa). Weed Sci 39:163–168

    Google Scholar 

  • Stoll P, Prati D (2001) Intraspecific aggregation alters competitive interactions in experimental plant communities. Ecology 82:319–327

    Article  Google Scholar 

  • Summers K, McKeon S, Sellars J, Keusenkothen M, Morris J, Gloeckner D, Pressley C, Price B, Snow H (2003) Parasitic exploitation as an engine of diversity. Biol Rev 78:639–675

    Article  PubMed  Google Scholar 

  • Thrall PH, Burdon JJ (2000) Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathol 49:767–773

    Article  Google Scholar 

  • Thrall PH, Burdon JJ (2003) Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735–1737

    Article  PubMed  CAS  Google Scholar 

  • Thrall PH, Burdon JJ, Young A (2001) Variation in resistance and virulence among demes of a plant host-pathogen metapopulation, J Ecol 89:736–748

    Google Scholar 

  • Tomerlin JR, Howell TA (1988) DISTRAIN: A computer program for training people to estimate disease severity on cereal leaves. Plant Dis 72:455–459

    Google Scholar 

  • Vanderplank JE (1963) Plant diseases: epidemics and control. Academic press, New York

    Google Scholar 

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Acknowledgements

We thank Brian Anacker, Lee Cohnstaedt, Dan Coyle, Sarah DeMay, Karen Garrett, Molly Hoffer, Kris Kovar, Susan Lambrecht, Pat Martinez, and Karl Rhinhart for technical assistance.

This work was supported by USDA NRI grant # 96-35303-3206 to CCM and JB

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Correspondence to Christopher C. Mundt.

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Mundt, C.C., Brunet, J. & Sackett, K.E. Impact of density and disease on frequency-dependent selection and genetic polymorphism: experiments with stripe rust and wheat. Evol Ecol 22, 637–657 (2008). https://doi.org/10.1007/s10682-007-9187-3

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