Surveying Patterns in the Cost of Resistance in Plants

Despite the general belief that traits conferring resistance in plants to pests also confer costs, disagreement persists about the frequency of costs and the conditions under which they are most likely to be evident. In this article, we analyze 88 published comparisons to explore when trade-offs between resistance and fitness traits can be detected. Among the patterns revealed are that costs were most often associated with resistance to herbicides, followed by resistance to pathogens, and least often associated with resistance to herbivores; costs were more often found in crops versus wild species; greater control of the genetic background increased the probability of detecting costs of resistance; there was large variation in the cost associated with the same resistance trait in different genetic backgrounds; and many examples of costs of resistance appeared to be due to linkage rather than pleiotropic effects. We discuss these and other results and emphasize that dependencies among the data invalidate statistical verification of these patterns. We hope that our results stimulate experiments that test the observed patterns critically.

[1]  K. Tolstrup,et al.  The Limiting Effect of Disease Resistance on Yield , 1985 .

[2]  B. D. Smith.  Effect of the Plant Alkaloid Sparteine on the Distribution of the Aphid Acyrthosiphon spartii (Koch.) , 1966, Nature.

[3]  Lisa Munk,et al.  Near-Isogenic Barley Lines with Genes for Resistance to Powdery Mildew 1 , 1986 .

[4]  J. S. Holt,et al.  Triazine Resistance in Senecio vulgaris Parental and Nearly Isonuclear Backcrossed Biotypes Is Correlated with Reduced Productivity. , 1990, Plant physiology.

[5]  R. Denno,et al.  CHAPTER 14 – Individual, Population, and Geographic Patterns in Plant Defense , 1983 .

[6]  K. Frey,et al.  Association between Genetic Factors for Crown Rust Resistance and Yield in Oats 1 , 1971 .

[7]  W. Russell,et al.  Recurrent Selection for Resistance to European Corn Borer in a Corn Synthetic and Correlated Effects on Agronomic Traits 1 , 1986 .

[8]  R. Cook,et al.  Resistance and tolerance , 1987 .

[9]  M. Rausher,et al.  THE EVOLUTION OF RESISTANCE TO HERBIVORY IN IPOMOEA PURPUREA. II. NATURAL SELECTION BY INSECTS AND COSTS OF RESISTANCE , 1989, Evolution; international journal of organic evolution.

[10]  A. Waranyuwat,et al.  Effect of Three Genes ( Pd, Rps a 1 , and ln ) on Plant Height, Lodging, and Seed Yield in Indeterminate and Determinate Near‐Isogenic Lines of Soybeans 1 , 1985 .

[11]  V. G. Dethier.  Evolution of Receptor Sensitivity to Secondary Plant Substances with Special Reference to Deterrents , 1980, The American Naturalist.

[12]  H. Darmency,et al.  Agronomic performance of a triazine resistant foxtail millet (Setaria italica (L.) Beauv.) , 1989 .

[13]  N. Chiariello,et al.  Allocating Resources to Reproduction and DefenseNew assessments of the costs and benefits of allocation patterns in plants are relating ecological roles to resource use , 1987 .

[14]  Directed Mass Selection for Developing Multiple Pest Resistance and Conserving Germplasm in Alfalfa , 1972 .

[15]  J. Bergelson.  Changes in Fecundity Do Not Predict Invasiveness: A Model Study of Transgenic Plants , 1994 .

[16]  J. Burdon.  Fungal pathogens as selective forces in plant populations and communities. , 1991 .

[17]  J. P. Ross.  Effect of Aphid-Transmitted Soybean Mosaic Virus on Yields of Closely Related Resistant and Susceptible Soybean Lines 1 , 1977 .

[18]  D. Hume,et al.  Agronomic Performance of Trianzine‐Resistant and Susceptible Reciprocal Spring Canola Hybrids , 1988 .

[19]  M. D. Simons.  Influence of Genes for Resistance toPuccinia coronatafromAvena sterilison Yield and Rust Reaction of Cultivated Oats , 1979 .

[20]  P. Teng,et al.  Effect of leaf rust (Puccinia recondita tritici) on yield of four isogenic wheat lines , 1988 .

[21]  D. Schemske,et al.  The Cost of Defense Against Herbivores: An Experimental Study of Trichome Production in Brassica rapa , 1993, The American Naturalist.

[22]  G. Collins,et al.  Effects of Nicotiana longiflora Cav. Resistance to Race 0 Phytophthora parasitica var. nicotianae on Agronomic and Chemical Traits in Burley Tobacco 1 , 1982 .

[23]  N. Simmonds.  HOW FREQUENT ARE SUPERIOR GENOTYPES IN PLANT BREEDING POPULATIONS? , 1989 .

[24]  M. Berenbaum,et al.  CONSTRAINTS ON CHEMICAL COEVOLUTION: WILD PARSNIPS AND THE PARSNIP WEBWORM , 1986, Evolution; international journal of organic evolution.

[25]  W. W. Weeks,et al.  Restricted index selection for total alkaloids and yield in tobacco , 1989 .

[26]  M. Parker.  LOCAL POPULATION DIFFERENTIATION FOR COMPATIBILITY IN AN ANNUAL LEGUME AND ITS HOST‐SPECIFIC FUNGAL PATHOGEN , 1985, Evolution; international journal of organic evolution.

[27]  J. Dudley,et al.  Improving Corn Population for Grain Yield and Resistance to Leaf Blight and Stalk Rot 1 , 1980 .

[28]  M. Crawley.  Herbivory: the Dynamics of Animal-plant Interactions , 1984 .

[29]  B. Kerry,et al.  Principles and Practice of Nematode Control in Crops , 1987 .

[30]  B. L. Blad,et al.  Growth Analysis of Soybean Isolines Differing in Pubescence Density1 , 1986 .

[31]  F. Stuart Chapin,et al.  Resource Availability and Plant Antiherbivore Defense , 1985, Science.

[32]  B. Everitt,et al.  Statistical methods for rates and proportions , 1973 .

[33]  J. Gressel,et al.  Low intraspecific competitive fitness in a triazine-resistant, nearly nuclear-isogenic line of Brassica napus , 1985 .

[34]  S. Frank,et al.  EVOLUTION OF HOST‐PARASITE DIVERSITY , 1993, Evolution; international journal of organic evolution.

[35]  D. Levin.  Plant Phenolics: An Ecological Perspective , 1971, The American Naturalist.

[36]  and D G Bottrell,et al.  Cotton Insect Pest Management , 1977 .

[37]  J. Gershenzon.  Changes in the Levels of Plant Secondary Metabolites Under Water and Nutrient Stress , 1984 .

[38]  A. Dobson,et al.  Pathogens and the structure of plant communities. , 1994, Trends in ecology & evolution.

[39]  J. S. Holt,et al.  Comparison of Triazine-Resistant and -Susceptible Biotypes of Senecio vulgaris and Their F(1) Hybrids. , 1988, Plant physiology.

[40]  E. Stoller,et al.  Competition, Growth Rate, and CO2 Fixation in Triazine-Susceptible and -Resistant Smooth Pigweed (Amaranthus hybridus) , 1983, Weed Science.

[41]  C. Steelink,et al.  Effects of some environmental stress factors on certain phenolic compounds in tobacco. , 1970 .

[42]  R. H. Painter,et al.  Insect resistance in crop plants. , 1951 .

[43]  J. Bergelson.  The Effects of Genotype and the Environment on Costs of Resistance in Lettuce , 1994, The American Naturalist.

[44]  R. Whittaker,et al.  Allelochemics: chemical interactions between species. , 1971, Science.

[45]  D. McKey.  Adaptive Patterns in Alkaloid Physiology , 1974, The American Naturalist.

[46]  K. Miyamoto,et al.  Effects of Near-Ultraviolet Light on Alkaloid Production in Catharanthus roseus Plants , 1993, Planta medica.

[47]  K. Frey,et al.  Growth Analysis of Isoline‐Recurrent Parent Grain Yield Differences in Oats 1 , 1977 .

[48]  G. Collins,et al.  Effects of the N Mosaic‐Resistance Factor on Agronomic and Chemical Traits in Burley Tobacco 1 , 1979 .

[49]  E. H. Franz,et al.  THE EFFECTS OF INSECT PARASITISM ON PLANT COMPETITION: GREENBUGS AND BARLEY' , 1979 .

[50]  H. F. Robinson,et al.  Genetic variability in flue-cured varieties of Nicotiana tabacutn. I Hicks broadleaf × Coker 139. , 1960 .

[51]  P. Solymosi,et al.  Characterization of a triple (atrazine-pyrazon-pyridate) resistant biotype of common lambsquarters (Chenopodium album L.). , 1989 .

[52]  E. Simms,et al.  Resistance variation in natural and managed systems. , 1992 .

[53]  A. Wiberg.  Mutants of barley with induced resistance to powdery mildew. , 2009, Hereditas.

[54]  T. J. Mann,et al.  Evaluation of tobacco mosaic resistance factor transferred from burley to flue-cured tobacco , 1978 .

[55]  K. Frey,et al.  Yield-component Analysis of Oat Isolines that Produce Different Grain Yields 1 , 1977 .

[56]  D. Patterson,et al.  Growth performance of triazine-resistant and -susceptible biotypes of Solanum nigrum over a range of temperatures , 1988 .

[57]  E. Simms,et al.  Selective impact of herbivores. , 1992 .

[58]  H. P. Jensen,et al.  Effect of "unnecessary" powdery mildew resistance genes on agronomic properties of spring barley. , 1990 .

[59]  D. Herms,et al.  The Dilemma of Plants: To Grow or Defend , 1992, The Quarterly Review of Biology.

[60]  E. Simms,et al.  Theory and pattern in plant defense allocation. , 1992 .

[61]  E. Simms,et al.  Costs of plant resistance to herbivory. , 1992 .

[62]  M. Rausher,et al.  Costs and Benefits of Plant Resistance to Herbivory , 1987, The American Naturalist.

[63]  L. Segel,et al.  The paucity of plants evolving genetic resistance to herbicides: possible reasons and implications. , 1978, Journal of theoretical biology.

[64]  P. Kølster,et al.  Barley Isolines with Genes for Resistance to Erysiphe graminis f. sp. hordei in the Recurrent Parent ‘Siri’ , 1987 .

[65]  Ian T. Baldwin,et al.  The Reproductive Consequences Associated with Inducible Alkaloidal Responses in Wild Tobacco , 1990 .