, Volume 187, Issue 2, pp 427–445 | Cite as

Heritable plant phenotypes track light and herbivory levels at fine spatial scales

  • P. T. Humphrey
  • A. D. Gloss
  • J. Frazier
  • A. C. Nelson–Dittrich
  • S. Faries
  • N. K. Whiteman
Special Topic: From Plants to Herbivores


Organismal phenotypes often co-vary with environmental variables across broad geographic ranges. Less is known about the extent to which phenotypes match local conditions when multiple biotic and abiotic stressors vary at fine spatial scales. Bittercress (Brassicaceae: Cardamine cordifolia), a perennial forb, grows across a microgeographic mosaic of two contrasting herbivory regimes: high herbivory in meadows (sun habitats) and low herbivory in deeply shaded forest understories (shade habitats). We tested for local phenotypic differentiation in plant size, leaf morphology, and anti-herbivore defense (realized resistance and defensive chemicals, i.e., glucosinolates) across this habitat mosaic through reciprocal transplant–common garden experiments with clonally propagated rhizomes. We found habitat-specific divergence in morphological and defensive phenotypes that manifested as contrasting responses to growth in shade common gardens: weak petiole elongation and attenuated defenses in populations from shade habitats, and strong petiole elongation and elevated defenses in populations from sun habitats. These divergent phenotypes are generally consistent with reciprocal local adaptation: plants from shade habitats that naturally experience low herbivory show reduced investment in defense and an attenuated shade avoidance response, owing to its ineffectiveness within forest understories. By contrast, plants from sun habitats with high herbivory show shade-induced elongation, but no evidence of attenuated defenses canonically associated with elongation in shade-intolerant plant species. Finally, we observed differences in flowering phenology between habitat types that could potentially contribute to inter-habitat divergence by reducing gene flow. This study illuminates how clonally heritable plant phenotypes track a fine-grained mosaic of herbivore pressure and light availability in a native plant.


Common garden Microgeographic divergence Phenotypic plasticity Shade avoidance syndrome Brassicaceae 



We acknowledge Ian Billick (RMBL), Jennifer Reithel (RMBL), Kailen Mooney (UC-Irvine), and Carol Boggs (University of South Carolina) for advice during the design and data collection phases of this project. We also thank Timothy Morton (University of Chicago) for assistance with glucosinolate profiling. Financial support was provided through the Research Experience for Undergraduate Site Program at the National Science Foundation Division of Environmental Biology (0753774) at the RMBL, to N.K.W. by the RMBL (Research Fellowships 2010–2013), NSF DEB (1256758), the John Templeton Foundation (41855) and the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R35GM119816; to P.T.H. by RMBL Graduate Fellowships (2011–2013), the University of Arizona Center for Insect Science, and NSF DEB (1309493); to A.D.G. by NSF DEB (1405966), an NSF Graduate Research Fellowship, and an RMBL Graduate Fellowship (2011); and to J.F. and S.F. by RMBL undergraduate research awards.

Author contribution statement

ADG, ACND, SF, and NKW designed the experiments. ADG, JF, ACND, SF, and NKW carried out the work. PTH and ADG conducted the analyses. PTH, ADG, and NKW wrote the paper.

Supplementary material

442_2018_4116_MOESM1_ESM.pdf (9.2 mb)
Supplementary material 1 (PDF 9428 kb)


  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42. Google Scholar
  2. Agerbirk N, De Vos M, Kim JH, Jander G (2009) Indole glucosinolate breakdown and its biological effects. Phytochem Rev 8:101–120. Google Scholar
  3. Agerbirk N, Olsen CE, Chew FS, Ørgaard M (2010) Variable glucosinolate profiles of Cardamine pratensis (Brassicaceae) with equal chromosome numbers. J Agric Food Chem 58(8):4693–4700. PubMedGoogle Scholar
  4. Agrawal AA (2001) Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? Am Nat 157:555–569. PubMedGoogle Scholar
  5. Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. In: Bell MA, Eanes WF, Futuyma DJ, Levinton JS (eds) Evolution after darwin: the first 150 years. Sinauer Associates, SunderlandGoogle Scholar
  6. Agrawal AA, Hastings AP, Johnson MT, Maron JL, Salminen J (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116. PubMedGoogle Scholar
  7. Alexandre NM, Humphrey PT, Frazier J, Gloss AD, Lee J, Affeldt HA, Whiteman NK (2018) Habitat preference of an herbivore shapes the habitat distribution of its host plant. bioRxiv. Google Scholar
  8. Antonovics J (2006) Evolution in closely adjacent plant populations X: long-term persistence of prereproductive isolation at a mine boundary. Heredity 97:33. PubMedGoogle Scholar
  9. Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363. PubMedGoogle Scholar
  10. Ballaré CL, Pierik R (2017) The shadeavoidance syndrome: multiple signals and ecological consequences. Plant, Cell Environ 40:2530–2543. Google Scholar
  11. Bartoń K (2017) MuMIn: multi-model inference. R package version 1.40.0Google Scholar
  12. Barton KE, Boege K (2017) Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences. Ecol Lett 20:403–411. PubMedGoogle Scholar
  13. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package v1.7:1–23Google Scholar
  14. Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605. PubMedGoogle Scholar
  15. Bell DL, Galloway LF (2008) Population differentiation for plasticity to light in an annual herb: adaptation and cost. Am J Bot 95:59–65. PubMedGoogle Scholar
  16. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448. PubMedGoogle Scholar
  17. Brachi B, Meyer CG, Villoutreix R, Platt A, Morton TC, Roux F, Bergelson J (2015) Co-selected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana. Proc Natl Acad Sci USA 112:4032–4037. PubMedPubMedCentralGoogle Scholar
  18. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM, Froehlich JE, Johnson BF, Kramer DM, Jander G, Sharkey TD, Howe GA (2016) Rewiring of jasmonate and phytochrome B signaling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. PubMedPubMedCentralGoogle Scholar
  19. Cerrudo I, Caliri-Ortiz ME, Keller MM, Degano ME, Demkura PV, Ballaré CL (2017) Exploring growth-defence tradeoffs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shadeavoidance responses. Plant, Cell Environ 40:635–644. Google Scholar
  20. Chico JM, Fernández-Barbero G, Chini A, Fernández-Calvo P, Díez-Díaz M, Solano R (2014) Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 26:1967–1980. PubMedPubMedCentralGoogle Scholar
  21. Cipollini D (2005) Interactive effects of lateral shading and jasmonic acid on morphology, phenology, seed production, and defense traits in Arabidopsis thaliana. Int J Plant Sci 166:955–959. Google Scholar
  22. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899. PubMedGoogle Scholar
  23. Colicchio J (2017) Transgenerational effects alter plant defence and resistance in nature. J Evol Biol 30:664–680. PubMedPubMedCentralGoogle Scholar
  24. Collinge SK, Louda SM (1988a) Patterns of resource use by a drosophilid (Diptera) leaf miner on a native crucifer. Ann Entomol Soc Am 81:733–741. Google Scholar
  25. Collinge SK, Louda SM (1988b) Herbivory by leaf miners in response to experimental shading of a native crucifer. Oecologia 75:559–566. PubMedGoogle Scholar
  26. Collinge SK, Louda SM (1989a) Scaptomyza nigrita Wheeler (Diptera: Drosophilidae), a leaf miner of the native crucifer, Cardamine cordifolia A. gray (bittercress). J Kans Entomol Soc 62:1–10Google Scholar
  27. Collinge SK, Louda SM (1989b) Influence of plant phenology on the insect herbivore/bittercress interaction. Oecologia 79:111–116. PubMedGoogle Scholar
  28. Darwin C (1859) On the origin of species by means of natural selection, or, the preservation of favoured races in the struggle for life. J. Murray, LondonGoogle Scholar
  29. Doheny-Adams T, Redeker K, Kittipol V, Bancroft I, Hartley SE (2017) Development of an efficient glucosinolate extraction method. Plant Methods 13:17. PubMedPubMedCentralGoogle Scholar
  30. Donohue K, Messiqua D, Pyle EH, Heschel MS, Schmitt J (2000) Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54:1956–1968. PubMedGoogle Scholar
  31. Dostálek T, Rokaya MB, Maršík P, Rezek J, Skuhrovec J, Pavela R, Münzbergová Z (2016) Trade-off among different anti-herbivore defence strategies along an altitudinal gradient. AoB Plants. PubMedPubMedCentralGoogle Scholar
  32. Dudley S, Schmitt J (1995) Genetic differentiation in morphological responses to simulated foliage shade between populations of Impatiens capensis from open and woodland sites. Funct Ecol 9:655–666. Google Scholar
  33. Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465. Google Scholar
  34. Ehrlich PR, Raven PH (1969) Differentiation of populations. Science 165:1228–1232. PubMedGoogle Scholar
  35. Epling C, Dobzhansky T (1942) Genetics of natural populations. VI. Microgeographic races in Linanthus parryae. Genetics 27:317–332PubMedPubMedCentralGoogle Scholar
  36. Fine PV, Mesones I, Coley PD (2004) Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–665. PubMedGoogle Scholar
  37. Freckleton RP (2002) On the misuse of residuals in ecology: regression of residuals vs. multiple regression. J Anim Ecol 71:542–545. Google Scholar
  38. Galen C, Shore JS, Deyoe H (1991) Ecotypic divergence in alpine Polemonium viscosum: genetic structure, quantitative variation, and local adaptation. Evolution 45:1218–1228. PubMedGoogle Scholar
  39. Galloway LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytol 166:93–100. PubMedGoogle Scholar
  40. Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136. PubMedGoogle Scholar
  41. Gloss AD, Vassao DG, Hailey AL, Nelson Dittrich AC, Schramm K, Reichelt M, Rast TJ, Weichsel A, Cravens MG, Gershenzon J, Montfort WR, Whiteman NK (2014) Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the Drosophilidae. Mol Biol Evol 31:2441–2456. PubMedPubMedCentralGoogle Scholar
  42. Gommers CM, Visser EJ, St Onge KR, Voesenek LA, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71. PubMedGoogle Scholar
  43. Gommers CM, Keuskamp DH, Buti S, Van Veen H, Koevoets IT, Reinen E, Voesenek LA, Pierik R (2017) Molecular profiles of contrasting shade response strategies in wild plants: differential control of immunity and shoot elongation. Plant Cell 29:331–344. PubMedPubMedCentralGoogle Scholar
  44. Graham HM (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815. Google Scholar
  45. Greig-Smith P (1952) The use of random and contiguous quadrats in the study of the structure of plant communities. Ann Bot 16:293–316. Google Scholar
  46. Haldane JBS (1930) A mathematical theory of natural and artificial selection (Part VI, isolation). Proc Camb Philos Soc 26:220–230. Google Scholar
  47. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333. PubMedGoogle Scholar
  48. Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 37:67–93. Google Scholar
  49. Hendrick MF, Finseth FR, Mathiasson ME, Palmer KA, Broder EM, Breigenzer P, Fishman L (2016) The genetics of extreme microgeographic adaptation: an integrated approach identifies a major gene underlying leaf trichome divergence in Yellowstone Mimulus guttatus. Mol Ecol 25:5647–5662. PubMedGoogle Scholar
  50. Hopkins RJ, van Dam NM, van Loon JJ (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83. PubMedGoogle Scholar
  51. Humphrey PT, Nguyen TT, Villalobos MM, Whiteman NK (2014) Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Mol Ecol 23:1497–1515. PubMedGoogle Scholar
  52. Humphrey PT, Gloss AD, Alexandre NM, Villalobos MM, Fremgen MR, Groen SC, Meihls LN, Jander G, Whiteman NK (2016) Aversion and attraction to harmful plant secondary compounds jointly shape the foraging ecology of a specialist herbivore. Ecol Evol 6:3256–3268. PubMedPubMedCentralGoogle Scholar
  53. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. Google Scholar
  54. Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997. PubMedGoogle Scholar
  55. Keuskamp DH, Sasidharan R, Pierik R (2010) Physiological regulation and functional significance of shade avoidance responses to neighbors. Plant Signal Behav 5:655–662. PubMedPubMedCentralGoogle Scholar
  56. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw. Google Scholar
  57. Latzel V, Klimešová J (2010) Transgenerational plasticity in clonal plants. Evol Ecol 24:1537–1543. Google Scholar
  58. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189. Google Scholar
  59. Leone M, Keller MM, Cerrudo I, Ballaré CL (2014) To grow or defend? Low red: far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. New Phytol 204:355–367. PubMedGoogle Scholar
  60. Levin DA (2009) Flowering-time plasticity facilitates niche shifts in adjacent populations. New Phytol 183:661–666. PubMedGoogle Scholar
  61. Linhart YB, Baker I (1973) Intra-population differentiation of physiological response to flooding in a population of Veronica peregrina L. Nature 242:275–276. Google Scholar
  62. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277. Google Scholar
  63. Liu T, Zhang X, Yang H, Agerbirk N, Qiu Y, Wang H, Shen D, Song J, Li X (2016a) Aromatic glucosinolate biosynthesis pathway in Barbarea vulgaris and its response to Plutella xylostella infestation. Front Plant Sci 7:83. PubMedPubMedCentralGoogle Scholar
  64. Liu Y, Dawson W, Prati D, Haeuser E, Feng Y, van Kleunen M (2016b) Does greater specific leaf area plasticity help plants to maintain a high performance when shaded? Ann Bot 118:1329–1336. PubMedPubMedCentralGoogle Scholar
  65. Louda SM (1984) Herbivore effect on stature, fruiting, and leaf dynamics of a native crucifer. Ecology 65:1379–1386. Google Scholar
  66. Louda SM, Collinge SK (1992) Plant resistance to insect herbivores: a field test of the environmental stress hypothesis. Ecology 73:153–169. Google Scholar
  67. Louda SM, Rodman JE (1983a) Ecological patterns in the glucosinolate content of a native mustard, Cardamine cordifolia, in the Rocky Mountains. J Chem Ecol 9:397–422. PubMedGoogle Scholar
  68. Louda SM, Rodman JE (1983b) Concentration of glucosinolates in relation to habitat and insect herbivory for the native crucifer Cardamine cordifolia. Biochem Syst Ecol 11:199–207. Google Scholar
  69. Louda SM, Rodman JE (1996) Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, bittercress). J Ecol 84:229–237. Google Scholar
  70. Louda SM, Dixon PM, Huntly NJ (1987) Herbivory in sun versus shade at a natural meadow-woodland ecotone in the Rocky Mountains. Plant Ecol 72:141–149Google Scholar
  71. Luke SG (2017) Evaluating significance in linear mixed-effects models in R. Behav Res Methods 49:1494–1502. PubMedGoogle Scholar
  72. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Lond B 273:2575–2584. Google Scholar
  73. Mooney EH, Phillips JS, Tillberg CV, Sandrow C, Nelson AS, Mooney KA (2016) Abiotic mediation of a mutualism drives herbivore abundance. Ecol Lett 19:37–44. PubMedGoogle Scholar
  74. Moreno JE, Tao Y, Chory J, Ballare CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci USA 106:4935–4940. PubMedPubMedCentralGoogle Scholar
  75. Mosteller F, Tukey JW (1977) Data analysis and regression: a second course in statistics. Addison-Wesley Publishing Co, ReadingGoogle Scholar
  76. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. Google Scholar
  77. Nosil P, Harmon L (2009) Niche dimensionality and ecological speciation. In: Butlin R, Bridle J, Schluter D (eds) Speciation and patterns of diversity (Ecological Reviews). Cambridge University Press, Cambridge, pp 127–154. Google Scholar
  78. Pellissier L, Roger A, Bilat J, Rasmann S (2014) High elevation Plantago lanceolata plants are less resistant to herbivory than their low elevation conspecifics: is it just temperature? Ecography 37:950–959. Google Scholar
  79. Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410. Google Scholar
  80. Prasad KV, Song BH, Olson-Manning C, Anderson JT, Lee CR, Schranz ME, Windsor AJ, Clauss MJ, Manzaneda AJ, Naqvi I, Reichelt M, Gershenzon J, Rupasinghe SG, Schuler MA, Mitchell-Olds T (2012) A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337:1081–1084. PubMedGoogle Scholar
  81. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. v3.3.
  82. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854–863. PubMedGoogle Scholar
  83. Reznick DN, Ricklefs RE (2009) Darwin’s bridge between microevolution and macroevolution. Nature 457:837–842. PubMedGoogle Scholar
  84. Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends Ecol Evol 29:165–176. PubMedGoogle Scholar
  85. Ricklefs R, Miller G (2000) Ecology, 4th edn. W.H. Freeman, New YorkGoogle Scholar
  86. Rodman JE, Louda SM (1985) Seasonal flux of isothiocyanate-yielding glucosinolates in roots, stems and leaves of Cardamine cordifolia. Biochem Syst Ecol 13:405–412. Google Scholar
  87. Runkle ES, Heins RD (2001) Specific functions of red, far red, and blue light in flowering and stem extension of long-day plants. J Am Soc Hort Sci 126:275–282Google Scholar
  88. Sasidharan R, Chinnappa CC, Voesenek LA, Pierik R (2008) The regulation of cell wall extensibility during shade avoidance: a study using two contrasting ecotypes of Stellaria longipes. Plant Physiol 148:1557–1569. PubMedPubMedCentralGoogle Scholar
  89. Sato Y, Kudoh H (2017) Fine-scale frequency differentiation along a herbivory gradient in the trichome dimorphism of a wild Arabidopsis. Ecol Evol 7:2133–2141. PubMedPubMedCentralGoogle Scholar
  90. Schemske DW, Bierzychudek P (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evolution 61:2528–2543. PubMedGoogle Scholar
  91. Schmitt J, Gamble SE (1990) The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution 44:2022–2030. PubMedGoogle Scholar
  92. Schmitt J, Stinchcombe JR, Heschel MS, Huber H (2003) The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integr Comp Biol 43:459–469. PubMedGoogle Scholar
  93. Schwaegerle KE, McIntyre H, Swingley C (2000) Quantitative genetics and the persistence of environmental effects in clonally propagated organisms. Evolution 54:452–461. PubMedGoogle Scholar
  94. Selander RK, Kaufman DW (1975) Genetic structure of populations of the brown snail (Helix aspersa). I. Microgeographic variation. Evolution 29:385–401. PubMedGoogle Scholar
  95. Sork VL, Stowe KA, Hochwender C (1993) Evidence for local adaptation in closely adjacent subpopulations of northern red oak (Quercus rubra L.) expressed as resistance to leaf herbivores. Am Nat 142:928–936. PubMedGoogle Scholar
  96. Strauss SY, Cacho NI (2013) Nowhere to run, nowhere to hide: the importance of enemies and apparency in adaptation to harsh soil environments. Am Nat 182(1):E1–E14. PubMedGoogle Scholar
  97. Uesugi A, Connallon T, Kessler A, Monro K (2017) Relaxation of herbivore-mediated selection drives the evolution of genetic covariances between plant competitive and defense traits. Evolution 71:1700–1709. PubMedGoogle Scholar
  98. Ullah MI, Aslam DM (2017) mctest: multicollinearity diagnostic measures, 2017. R package version 1.1.1Google Scholar
  99. Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257. Google Scholar
  100. van Hinsberg A, van Tienderen P (1997) Variation in growth form in relation to spectral light quality (red/far-red ratio) in Plantago lanceolata L. in sun and shade populations. Oecologia 111:452–459. PubMedGoogle Scholar
  101. Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43:1097–1109. PubMedGoogle Scholar
  102. Whiteman NK, Groen SC, Chevasco D, Bear A, Beckwith N, Gregory TR, Denoux C, Mammarella N, Ausubel FM, Pierce NE (2011) Mining the plant-herbivore interface with a leafmining Drosophila of Arabidopsis. Mol Ecol 20:995–1014. PubMedGoogle Scholar
  103. Whiteman NK, Gloss AD, Sackton TB, Groen SC, Humphrey PT, Lapoint RT, Sonderby IE, Halkier BA, Kocks C, Ausubel FM, Pierce NE (2012) Genes involved in the evolution of herbivory by a leaf-mining, drosophilid fly. Genome Biol Evol 4:900–916. PubMedPubMedCentralGoogle Scholar
  104. Winde I, Wittstock U (2011) Insect herbivore counter adaptations to the plant glucosinolate-myrosinase system. Phytochemistry 72:1566–1575. PubMedGoogle Scholar
  105. Wit M, Spoel SH, Sanchez-Perez GF, Gommers CM, Pieterse CM, Voesenek LA, Pierik R (2013) Perception of low red: far-red ratio compromises both salicylic acid-and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75:90–103. PubMedGoogle Scholar
  106. Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monogr 82:149–168. Google Scholar
  107. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534. PubMedGoogle Scholar
  108. Züst T, Joseph B, Shimizu KK, Kliebenstein DJ, Turnbull LA (2011) Using knockout mutants to reveal the growth costs of defensive traits. Proc R Soc Lond B 278:2598–2603. Google Scholar
  109. Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119. PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.Department of Ecology and EvolutionUniversity of ChicagoChicagoUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  4. 4.Rocky Mountain Biological LaboratoryGothicUSA
  5. 5.Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA

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