Plant traits that predict resistance to herbivores

Summary 1. Although secondary metabolites are recognized as fundamental to the defence of plants against insect and mammalian herbivores, their relative importance compared to other potential defensive plant traits (e.g. physical resistance, gross morphology, life-history, primary chemistry and physiology) are not well understood. 2. We conducted a meta-analysis to answer the question: What types of genetically variable plant traits most strongly predict resistance against herbivores? We performed a comprehensive literature search and obtained 499 separate measurements of the strength of covariation (measured as genetic correlations) between plant traits and herbivore susceptibility – these were extracted from 72 studies involving 19 plant families. 3. Surprisingly, we found no overall association between the concentrations of secondary metabolites and herbivore susceptibility – plant traits other than secondary metabolites most strongly predicted herbivore susceptibility. Specifically, genetic variation in life-history traits (e.g. flowering time, growth rate) consistently exhibited the strongest genetic correlations with susceptibility. Genetic variation in gross morphological traits (e.g. no. branches, plant size) and physical resistance traits (e.g. latex, trichomes) were also frequently correlated with variation in herbivore susceptibility, but these relationships depended on attributes of the herbivores (e.g. feeding guild) and plants (e.g. longevity). 4. These results call into question the conventional wisdom that secondary metabolites are the most important anti-herbivore defence of plants. We propose the hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution. Meanwhile, secondary metabolites could have evolved to be important defensive mechanisms not because they have the largest effect on herbivores, but because the constraints on their evolution are the weakest.

[1]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[2]  J. X. Becerra Insects on plants: macroevolutionary chemical trends in host use. , 1997, Science.

[3]  Xiao-Hua Zhou,et al.  Statistical Methods for Meta‐Analysis , 2008 .

[4]  M. Rausher THE MEASUREMENT OF SELECTION ON QUANTITATIVE TRAITS: BIASES DUE TO ENVIRONMENTAL COVARIANCES BETWEEN TRAITS AND FITNESS , 1992, Evolution; international journal of organic evolution.

[5]  W. J. Mattson,et al.  Herbivory in relation to plant nitrogen content , 1980 .

[6]  I. Baldwin,et al.  Silencing 7 herbivory-regulated proteins in Nicotiana , 2008 .

[7]  G. Cooper-Driver Book reviewHerbivores: Their Interaction with Secondary Metabolites : Edited by G. A. Rosenthal and D. H. Janzen. Academic Press, New York, 1979. 718 pp. £34.60. , 1981 .

[8]  P. Raven,et al.  BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION , 1964 .

[9]  M. Wink,et al.  Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): Role of an amino acid substitution in the ouabain binding site of Na+,K+-ATPase , 1996, Journal of Chemical Ecology.

[10]  M. Rausher,et al.  EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE , 1997, Evolution; international journal of organic evolution.

[11]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

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

[13]  T. Whitham,et al.  Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism , 2001 .

[14]  M. Lerdau,et al.  The Evolution of Function in Plant Secondary Metabolites , 2003, International Journal of Plant Sciences.

[15]  M. Berenbaum,et al.  Facing the Future of Plant-Insect Interaction Research: Le Retour à la “Raison d'Être”1 , 2008, Plant Physiology.

[16]  J. W. Wallace,et al.  Biochemical Interaction Between Plants and Insects , 1976, Recent Advances in Phytochemistry.

[17]  R. Bennett,et al.  Secondary metabolites in plant defence mechanisms. , 1994, The New phytologist.

[18]  J. Fordyce,et al.  Specialist Weevil, Rhyssomatus lineaticollis, Does Not Spatially Avoid Cardenolide Defenses of Common Milkweed by Ovipositing into Pith Tissue , 2000, Journal of Chemical Ecology.

[19]  J. Thompson,et al.  Thyme is of the essence: Biochemical polymorphism and multi-species deterrence , 1999 .

[20]  J. M. Scriber,et al.  Growth of Herbivorous Caterpillars in Relation to Feeding Specialization and to the Growth Form of Their Food Plants , 1979 .

[21]  R. Mithen,et al.  Divergent selection for secondary metabolites between wild populations of Brassica oleracea and its implications for plant-herbivore interactions , 1995, Heredity.

[22]  Gwenn W. Gröndal,et al.  Meta-analytic procedures for social research , 1993 .

[23]  J. X. Becerra Synchronous coadaptation in an ancient case of herbivory , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Brian D. Farrell,et al.  The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? , 1998 .

[25]  Yi Zhang,et al.  Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection , 2009, BMC Plant Biology.

[26]  C. F. Wilkinson,et al.  Detoxication Enzymes in the Guts of Caterpillars: An Evolutionary Answer to Plant Defenses? , 1971, Science.

[27]  A. Agrawal,et al.  HERBIVORE OFFENSE , 2002 .

[28]  Brian D. Farrell,et al.  The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? , 1998 .

[29]  P. Feeny,et al.  Plant apparency and chemical defense , 1976 .

[30]  G. Fraenkel The raison d'ĕtre of secondary plant substances; these odd chemicals arose as a means of protecting plants from insects and now guide insects to food. , 1959, Science.

[31]  F. Kondrashov,et al.  The evolution of gene duplications: classifying and distinguishing between models , 2010, Nature Reviews Genetics.

[32]  A. Agrawal,et al.  Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment , 2009, Journal of evolutionary biology.

[33]  R. Firn,et al.  On the evolution of plant secondary chemical diversity , 1991 .

[34]  P. Coley,et al.  Convergence in Defense Syndromes of Young Leaves in Tropical Rainforests , 2003 .

[35]  J. Keurentjes,et al.  Metabolomics: the chemistry between ecology and genetics , 2010, Molecular ecology resources.

[36]  V. G. Dethier,et al.  Chemical Factors Determining the Choice of Food Plants by Papilio Larvae , 1941, The American Naturalist.

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

[38]  Mark Fishbein,et al.  Plant defense syndromes. , 2006, Ecology.

[39]  M. Berenbaum Evolution of Specialization in Insect-Umbellifer Associations , 1990 .

[40]  D. Kliebenstein,et al.  Differential Levels of Insect Herbivory in the Field Associated with Genotypic Variation in Glucosinolates in Arabidopsis thaliana , 2008, Journal of Chemical Ecology.

[41]  F. James Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[42]  Campbell O. Webb,et al.  Phylomatic: tree assembly for applied phylogenetics , 2005 .

[43]  G. Arnqvist,et al.  MetaWin: Statistical Software for Meta-Analysis with Resampling Tests. Version 1.Michael S. Rosenberg , Dean C. Adams , Jessica Gurevitch , 1998 .

[44]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[45]  Steff Lewis,et al.  Forest plots: trying to see the wood and the trees , 2001, BMJ : British Medical Journal.

[46]  M. Wink Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. , 2003, Phytochemistry.

[47]  I. Baldwin,et al.  Silencing the Jasmonate Cascade: Induced Plant Defenses and Insect Populations , 2004, Science.

[48]  A. Agrawal Plant Defense and Density Dependence in the Population Growth of Herbivores , 2004, The American Naturalist.

[49]  E. Simms,et al.  Botanical Defenses. (Book Reviews: Plant Resistance to Herbivores and Pathogens. Ecology, Evolution, and Genetics.) , 1992 .

[50]  A. Palmer,et al.  Detecting Publication Bias in Meta‐analyses: A Case Study of Fluctuating Asymmetry and Sexual Selection , 1999, The American Naturalist.

[51]  D. Wardle,et al.  Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms , 1998 .

[52]  Y. Choi,et al.  Identification of Chlorogenic Acid as a Resistance Factor for Thrips in Chrysanthemum[C][OA] , 2009, Plant Physiology.

[53]  A. Agrawal Macroevolution of plant defense strategies. , 2007, Trends in ecology & evolution.

[54]  M. Rausher,et al.  Plant sex and the evolution of plant defenses against herbivores , 2009, Proceedings of the National Academy of Sciences.

[55]  Dean C. Adams,et al.  RESAMPLING TESTS FOR META‐ANALYSIS OF ECOLOGICAL DATA , 1997 .

[56]  M. Berenbaum,et al.  Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? , 1981, Science.

[57]  T. White,et al.  The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants , 1984, Oecologia.

[58]  Anurag A. Agrawal,et al.  Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores , 2005 .

[59]  Brian D. Farrell,et al.  Escalation of Plant Defense: Do Latex and Resin Canals Spur Plant Diversification? , 1991, The American Naturalist.

[60]  D. Tallamy,et al.  Polymorphism in Plant Defense Against Herbivory: Constitutive and Induced Resistance in Cucumis sativus , 1999, Journal of Chemical Ecology.

[61]  P. Coley,et al.  Effects of leaf age and plant life history patterns on herbivory , 1980, Nature.

[62]  Marc T. J. Johnson Bottom-up effects of plant genotype on aphids, ants, and predators. , 2008, Ecology.

[63]  John E. Hunter,et al.  Methods of Meta-Analysis , 1989 .

[64]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  M. Rausher The Evolution of Flavonoids and Their Genes , 2006 .

[66]  R. Julkunen‐Tiitto,et al.  Ecological role of reindeer summer browsing in the mountain birch (Betula pubescens ssp. czerepanovii) forests: effects on plant defense, litter decomposition, and soil nutrient cycling , 2007, Oecologia.

[67]  R. Mauricio Costs of Resistance to Natural Enemies in Field Populations of the Annual Plant Arabidopsis thaliana , 1998, The American Naturalist.

[68]  M. Lajeunesse,et al.  Meta‐Analysis and the Comparative Phylogenetic Method , 2009, The American Naturalist.

[69]  Richard A. Lankau Specialist and generalist herbivores exert opposing selection on a chemical defense. , 2007, The New phytologist.

[70]  Jessica Gurevitch,et al.  STATISTICAL ISSUES IN ECOLOGICAL META‐ANALYSES , 1999 .

[71]  Mark D. Rausher,et al.  Escape from adaptive conflict after duplication in an anthocyanin pathway gene , 2008, Nature.

[72]  N. Stamp Out Of The Quagmire Of Plant Defense Hypotheses , 2003, The Quarterly Review of Biology.

[73]  M. Berenbaum,et al.  Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[75]  H. Cyr,et al.  Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems , 1993, Nature.

[76]  H. Niemeyer,et al.  Differences in Effects of Pyrrolizidine Alkaloids on Five Generalist Insect Herbivore Species , 2005, Journal of Chemical Ecology.

[77]  A. Agrawal,et al.  Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. , 2009, The New phytologist.

[78]  Sudhir Kumar,et al.  The timetree of life , 2009 .

[79]  L. Després,et al.  The evolutionary ecology of insect resistance to plant chemicals. , 2007, Trends in ecology & evolution.

[80]  D. Ward,et al.  Evolution of plant defenses in nonindigenous environments. , 2010, Annual review of entomology.

[81]  C. Williams,et al.  Advances in Flavonoid Research Since 1992 , 2001 .

[82]  Julia Koricheva,et al.  A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies , 2006 .

[83]  M. Lajeunesse 13. Recovering Missing or Partial Data from Studies: A Survey of Conversions and Imputations for Meta-analysis , 2013 .

[84]  David C. Tank,et al.  An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: , 2009 .

[85]  A. Agrawal,et al.  Phylogenetic escalation and decline of plant defense strategies , 2008, Proceedings of the National Academy of Sciences.

[86]  D. Pilson Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus , 2000, Oecologia.