1932

Abstract

Coevolution is among the most important evolutionary processes that generate biological diversity. Plant–pollinator interactions play a prominent role in the evolution of reproductive traits in flowering plants. Likewise, plant–herbivore interactions select for myriad defenses that protect plants from damage. These mutualistic and antagonistic interactions, respectively, have traditionally been considered in isolation from one another. Here, we consider whether reproductive traits and antiherbivore defenses are interdependent as a result of pollinator- and herbivore-mediated selection. The evolution of floral traits, self-fertilization, and separate sexes frequently affects the expression and evolution of plant defenses. In turn, the evolution of defense can affect allocation to reproductive traits, and herbivores often impose strong selection directly on floral traits. Theory and empirical evidence suggest that herbivores can influence the evolution of selfing from outcrossing and potentially the evolution of separate sexes from combined sexes. We identify several areas in which future research is needed to increase our understanding of the evolutionary interplay between reproduction and defense in plants.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-112414-054215
2015-12-04
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/46/1/annurev-ecolsys-112414-054215.html?itemId=/content/journals/10.1146/annurev-ecolsys-112414-054215&mimeType=html&fmt=ahah

Literature Cited

  1. Adler LS, Bronstein JL. 2004. Attracting antagonists: Does floral nectar increase leaf herbivory?. Ecology 85:1519–26 [Google Scholar]
  2. Adler LS, Seifert MG, Wink M, Morse GE. 2012. Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol. Lett. 15:1140–48 [Google Scholar]
  3. Adler LS, Wink M, Distl M, Lentz AJ. 2006. Leaf herbivory and nutrients increase nectar alkaloids. Ecol. Lett. 9:960–67 [Google Scholar]
  4. Agrawal AA, Fishbein M. 2008. Phylogenetic escalation and decline of plant defense strategies. PNAS 105:10057–60 [Google Scholar]
  5. Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen J-P. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–16 [Google Scholar]
  6. Ågren J, Danell K, Elmqvist T, Ericson L, Hjältén J. 1999. Sexual dimorphism and biotic interactions. Gender and Sexual Dimorphism in Flowering Plants MA Geber, TE Dawson, LF Delph 217–46 Berlin: Springer-Verlag [Google Scholar]
  7. Ågren J, Hellstrom F, Torang P, Ehrlén J. 2013. Mutualists and antagonists drive among-population variation in selection and evolution of floral display in a perennial herb. PNAS 110:18202–7 [Google Scholar]
  8. Armbruster WS. 1997. Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78:1661–72 [Google Scholar]
  9. Armbruster WS, Lee J, Baldwin BG. 2009. Macroevolutionary patterns of defense and pollination in Dalechampia vines: adaptation, exaptation, and evolutionary novelty. PNAS 106:18085–90 [Google Scholar]
  10. Ashman T-L. 2002. The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83:1175–84 [Google Scholar]
  11. Ashman T-L. 2006. The evolution of separate sexes: a focus on the ecological context. Ecology and Evolution of Flowers LD Harder, SCH Barrett 204–22 Oxford, UK: Oxford Univ. Press [Google Scholar]
  12. Ashman T-L, Cole DH, Bradburn M. 2004. Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry. Ecology 85:2550–59 [Google Scholar]
  13. Ashman T-L, Penet L. 2007. Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender-dimorphic plant. Am. Nat. 169:595–608 [Google Scholar]
  14. Avila-Sakar G, Romanow CA. 2012. Divergence in defence against herbivores between males and females of dioecious plant species. Int. J. Evol. Biol. 2012:e897157 [Google Scholar]
  15. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ. et al. 2005. Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol. 167:63–72 [Google Scholar]
  16. Barrett SCH. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3:274–84 [Google Scholar]
  17. Barrett SCH, Charlesworth D. 1991. Effect of a change in the level of inbreeding on the genetic load. Nature 352:522–24 [Google Scholar]
  18. Barrett SCH, Hough J. 2012. Sexual dimorphism in flowering plants. J. Exp. Bot. 64:67–82 [Google Scholar]
  19. Bawa KS. 1980. Evolution of dioecy in flowering plants. Annu. Rev. Ecol. Syst. 11:15–39 [Google Scholar]
  20. Bello-Bedoy R, Núñez-Farfán J. 2010. Cost of inbreeding in resistance to herbivores in Datura stramonium. Ann. Bot. 105:747–53 [Google Scholar]
  21. Berger N, Dubreucq B. 2011. Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27. Plant Cell 23:4065–78 [Google Scholar]
  22. Brody AK, Mitchell RJ. 1997. Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110:86–93 [Google Scholar]
  23. Bruinsma M, Lucas-Barbosa D, ten Broeke CJ, van Dam NM, van Beek TA. et al. 2014. Folivory affects composition of nectar, floral odor and modifies pollinator behavior. J. Chem. Ecol. 40:39–49 [Google Scholar]
  24. Campbell SA. 2014. Ecological mechanisms for the coevolution of plant mating and defence strategies. New Phytol. 205:1047–53 [Google Scholar]
  25. Campbell SA, Halitschke R, Thaler JS, Kessler A. 2014. Plant mating systems affect adaptive plasticity in response to herbivory. Plant J. 78:481–90 [Google Scholar]
  26. Campbell SA, Kessler A. 2013. Plant mating system transitions drive the macroevolution of defense strategies. PNAS 110:3973–78 [Google Scholar]
  27. Campbell SA, Thaler JS, Kessler A. 2013. Plant chemistry underlies herbivore-mediated inbreeding depression in nature. Ecol. Lett. 16:252–60 [Google Scholar]
  28. Carr DE, Eubanks MD. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution 56:22–30 [Google Scholar]
  29. Carr DE, Eubanks MD. 2014. Interactions between insect herbivores and plant mating systems. Annu. Rev. Entomol. 59:185–203 [Google Scholar]
  30. Charlesworth B, Charlesworth D. 1999. The genetic basis of inbreeding depression. Genet. Res. 74:329–40 [Google Scholar]
  31. Charlesworth D. 1999. Theories of the evolution of dioecy. Gender and Sexual Dimorphism in Flowering Plants MA Geber, TE Dawson, LF Delph 33–60 Berlin: Springer-Verlag [Google Scholar]
  32. Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237–68 [Google Scholar]
  33. Charnov EL, Maynard Smith J, Bull JJ. 1976. Why be an hermaphrodite?. Nature 263:125–26 [Google Scholar]
  34. Cheptou PO, Donohue K. 2011. Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol. 189:395–407 [Google Scholar]
  35. Cleland RE. 1972. Oenothera: Cytogenetics and Evolution New York: Academic [Google Scholar]
  36. Coley PD, Bryant JP, Chapin FS. 1985. Resource availability and plant antiherbivore defense. Science 230:895–99 [Google Scholar]
  37. Cook JM, Rasplus J-Y. 2003. Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol. Evol. 18:241–48 [Google Scholar]
  38. Cornelissen T, Stiling P. 2005. Sex-biased herbivory: a meta-analysis of the effects of gender on plant-herbivore interactions. Oikos 111:488–500 [Google Scholar]
  39. Cox PA. 1982. Vertebrate pollination and the maintenance of dioecism in Freycinetia. Am. Nat. 120:65–80 [Google Scholar]
  40. Darwin CR. 1876. The Effects of Cross and Self-Fertilisation in the Vegetable Kingdom London: John Murray [Google Scholar]
  41. Darwin CR. 1877. The Different Forms of Flowers on Plants of the Same Species London: John Murray [Google Scholar]
  42. DeAngelis DL, Koslow JM, Jiang J, Ruan SG. 2008. Host mating system and the spread of a disease-resistant allele in a population. Theor. Popul. Biol. 74:191–98 [Google Scholar]
  43. Des Marais DL, Rausher MD. 2008. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454:762–65 [Google Scholar]
  44. Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ. 1988. Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. PNAS 85:6738–42 [Google Scholar]
  45. Dufaÿ M, Anstett MC. 2003. Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14 [Google Scholar]
  46. Ehrlén J, Borg-Karlson A-K, Kolb A. 2012. Selection on plant optical traits and floral scent: effects via seed development and antagonistic interactions. Basic Appl. Ecol. 13:509–15 [Google Scholar]
  47. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586–608 [Google Scholar]
  48. Elle E, Hare JD. 2002. Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Funct. Ecol. 16:79–88 [Google Scholar]
  49. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G. 2007. Time after time: flowering phenology and biotic interactions. Trends Ecol. Evol. 22:432–39 [Google Scholar]
  50. Endara M-J, Coley PD. 2011. The resource availability hypothesis revisited: a meta-analysis. Funct. Ecol. 25:389–98 [Google Scholar]
  51. Ferrari MJ, Stephenson AG, Mescher MC, De Moraes CM. 2006. Inbreeding effects on blossom volatiles in Cucurbita pepo subsp. texana (Cucurbitaceae). Am. J. Bot. 93:1768–74 [Google Scholar]
  52. Fineblum WL, Rausher MD. 1997. Do floral pigmentation genes also influence resistance to enemies? The W locus in Ipomoea purpurea. Ecology 78:1646–54 [Google Scholar]
  53. Geber MA, Dawson TE, Delph LF. 1999. Gender and Sexual Dimorphism in Flowering Plants Berlin: Springer-Verlag [Google Scholar]
  54. Geber MA, Griffen LR. 2003. Inheritance and natural selection on functional traits. Int. J. Plant Sci. 164:S21–42 [Google Scholar]
  55. Golenberg EM, West NW. 2013. Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants. Am. J. Bot. 100:1022–37 [Google Scholar]
  56. Gómez JM. 2003. Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am. Nat. 162:242–56 [Google Scholar]
  57. Goodwillie C, Kalisz S, Eckert CG. 2005. The evolutionary enigma of mixed mating in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36:47–79 [Google Scholar]
  58. Greef JM, Compton SG. 2002. Can seed protection lead to dioecy in Ficus?. Oikos 96:386–88 [Google Scholar]
  59. Hanley ME, Lamont BB, Armbruster WS. 2009. Pollination and plant defence traits co-vary in Western Australian Hakeas. New Phytol. 182:251–60 [Google Scholar]
  60. Harborne JB, Williams CA. 2000. Advances in flavonoid research since 1992. Phytochemistry 55:481–504 [Google Scholar]
  61. Harder LD, Johnston SD. 2009. Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol. 183:530–45 [Google Scholar]
  62. Hawkes CV, Sullivan JJ. 2001. The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–58 [Google Scholar]
  63. Herms DA, Mattson WJ. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283–335 [Google Scholar]
  64. Hersch-Green EI, Myburg H, Johnson MTJ. 2012. Adaptive molecular evolution of a defence gene in sexual but not functionally asexual evening primroses. J. Evol. Biol. 25:1576–86 [Google Scholar]
  65. Hollister JD, Greiner S, Wang W, Wang J, Zhang Y. et al. 2015. Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera. Mol. Biol. Evol. 32:896–905 [Google Scholar]
  66. Hull-Sanders HM, Eubanks MD. 2005. Plant defense theory provides insight into interactions involving inbred plants and insect herbivores. Ecology 86:897–904 [Google Scholar]
  67. Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70 [Google Scholar]
  68. Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G. 2003. The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–43 [Google Scholar]
  69. Ivey CT, Carr DE. 2005. Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). Am. J. Bot. 92:1641–49 [Google Scholar]
  70. Ivey CT, Carr DE. 2012. Tests for the joint evolution of mating system and drought escape in Mimulus. Ann. Bot. 109:583–98 [Google Scholar]
  71. Ivey CT, Carr DE, Eubanks MD. 2004. Effects of inbreeding in Mimulus guttatus on tolerance to herbivory in natural environments. Ecology 85:567–74 [Google Scholar]
  72. Janzen DH. 1971. Seed predation by animals. Annu. Rev. Ecol. Syst. 2:465–92 [Google Scholar]
  73. Jing SW, Coley PD. 1990. Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo. Oikos 58:369–77 [Google Scholar]
  74. Johnson MTJ, Ives AR, Ahern J, Salminen J-P. 2014. Macroevolution of plant defenses against herbivores in the evening primroses. New Phytol. 203:267–79 [Google Scholar]
  75. Johnson MTJ, Smith SD, Rausher MD. 2009. Plant sex and the evolution of plant defenses against herbivores. PNAS 106:18079–84 [Google Scholar]
  76. Kariyat RR, Mauck KE, De Moraes CM, Stephenson AG, Mescher MC. 2012. Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.). Ecol. Lett. 15:301–9 [Google Scholar]
  77. Kariyat RR, Scanlon SR, Mescher MC, De Moraes CM, Stephenson AG. 2011. Inbreeding depression in Solanum carolinense (Solanaceae) under field conditions and implications for mating system evolution. PLOS ONE 6:e28459 [Google Scholar]
  78. Kariyat RR, Scanlon SR, Moraski RP, Stephenson AG, Mescher MC, De Moraes CM. 2014. Plant inbreeding and prior herbivory influence attraction of caterpillars (Manduca sexta) to odors of the host plant Solanum carolinense (Solanaceae). Am. J. Bot. 101:376–80 [Google Scholar]
  79. Kerdelhué C, Rasplus J-Y. 1996. Non-pollinating Afrotropical fig wasps affect the fig-pollinator mutualism in Ficus within the subgenus Sycomorus. Oikos 75:3–14 [Google Scholar]
  80. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328 [Google Scholar]
  81. Kessler A, Halitschke R. 2009. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct. Ecol. 23:901–12 [Google Scholar]
  82. Kessler A, Halitschke R, Poveda K. 2011. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–80 [Google Scholar]
  83. Kessler D. 2012. Context dependency of nectar reward-guided oviposition. Entomol. Exp. Appl. 144:112–22 [Google Scholar]
  84. Kessler D, Bhattacharya S, Diezel C, Rothe E, Gase K. et al. 2012. Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata. Plant J. 71:529–38 [Google Scholar]
  85. Kessler D, Diezel C, Baldwin IT. 2010. Changing pollinators as a means of escaping herbivores. Curr. Biol. 20:237–42 [Google Scholar]
  86. Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT. 2013. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol. Lett. 16:299–306 [Google Scholar]
  87. Koslow JM, DeAngelis DL. 2006. Host mating system and the prevalence of disease in a plant population. Proc. R. Soc. B 273:1825–31 [Google Scholar]
  88. Krupnick GA, Weis AE. 1998. Floral herbivore effect on the sex expression of an andromonoecious plant, Isomeris arborea (Capparaceae). Plant Ecol. 134:151–62 [Google Scholar]
  89. Krupnick GA, Weis AE, Campbell DR. 1999. The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–34 [Google Scholar]
  90. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40 [Google Scholar]
  91. Lehtilä K, Strauss SY. 1999. Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. Ecology 80:116–24 [Google Scholar]
  92. Leimu R, Kloss L, Fischer M. 2008. Effects of experimental inbreeding on herbivore resistance and plant fitness: the role of history of inbreeding, herbivory and abiotic factors. Ecol. Lett. 11:1101–10 [Google Scholar]
  93. Levin DA. 1975. Pest pressure and recombination systems in plants. Am. Nat. 109:437–51 [Google Scholar]
  94. Liston A, Cronn R, Ashman T-L. 2014. Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights. Am. J. Bot. 101:1686–99 [Google Scholar]
  95. Lively CM. 2010. A review of Red Queen models for the persistence of obligate sexual reproduction. J. Hered. 101:S13–20 [Google Scholar]
  96. Lloyd DG. 1979. Parental strategies in angiosperms. N.Z. J. Bot. 17:595–606 [Google Scholar]
  97. Lloyd DG, Bawa KS. 1984. Modification of the gender of seed plants in varying conditions. Evol. Biol. 17:255–338 [Google Scholar]
  98. Lucas-Barbosa D, van Loon JJ, Dicke M. 2011. The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–54 [Google Scholar]
  99. Marshall M, Ganders FR. 2001. Sex-biased seed predation and the maintenance of females in a gynodioecious plant. Am. J. Bot. 88:1437–43 [Google Scholar]
  100. McCall AC, Irwin RE. 2006. Florivory: the intersection of pollination and herbivory. Ecol. Lett. 9:1351–65 [Google Scholar]
  101. McCall AC, Karban R. 2006. Induced defense in Nicotiana attenuata (Solanceae) fruit and flowers. Oecologia 146:566–71 [Google Scholar]
  102. McCall AC, Murphy SJ, Venner C, Brown M. 2013. Florivores prefer white versus pink petal color morphs in wild radish, Raphanus sativus. Oecologia 172:189–95 [Google Scholar]
  103. Mothershead K, Marquis RJ. 2000. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40 [Google Scholar]
  104. Muenchow G, Delesalle VA. 1992. Patterns of weevil herbivory on male, monoecious and female inflorescences of Sagittaria latifolia. Am. Midl. Nat. 127:355–67 [Google Scholar]
  105. Muola A, Mutikainen P, Laukkanen L, Lilley M, Leimu R. 2011. The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria. Ann. Bot. 108:547–55 [Google Scholar]
  106. Núñez-Farfán J, Cabrales-Vargas RA, Dirzo R. 1996. Mating system consequences on resistance to herbivory and life history traits in Datura stramonium. Am. J. Bot. 83:1041–49 [Google Scholar]
  107. Pellmyr O. 2003. Yuccas, yucca moths, and coevolution: a review. Ann. Mo. Bot. Gard. 90:35–55 [Google Scholar]
  108. Penet L, Collin CL, Ashman T-L. 2009. Florivory increases selfing: an experimental study in the wild strawberry, Fragaria virginiana. Plant Biol. 11:38–45 [Google Scholar]
  109. Pérez-Barrales R, Bolstad GH, Pélabon C, Hansen TF, Armbruster WS. 2013. Pollinators and seed predators generate conflicting selection on Dalechampia blossoms. Oikos 122:1411–28 [Google Scholar]
  110. Rausher MD. 2008. Evolutionary transitions in floral color. Int. J. Plant Sci. 169:7–21 [Google Scholar]
  111. Renner SS. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101:1588–96 [Google Scholar]
  112. Salathé M, Kouyos RD, Bonhoeffer S. 2008. The state of affairs in the kingdom of the Red Queen. Trends Ecol. Evol. 23:439–45 [Google Scholar]
  113. Schiestl FP. 2015. Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytol. 206:571–77 [Google Scholar]
  114. Simms EL, Bucher MA. 1996. Pleiotropic effects of flower-color intensity on herbivore performance on Ipomoea purpurea. Evolution 50:957–63 [Google Scholar]
  115. Sletvold N, Moritz KK, Ågren J. 2014. Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits. Ecology 96:214–21 [Google Scholar]
  116. Stamp N. 2003. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78:23–55 [Google Scholar]
  117. Steets JA, Ashman T-L. 2004. Herbivory alters the expression of a mixed-mating system. Am. J. Bot. 91:1046–51 [Google Scholar]
  118. Steets JA, Hamrick JL, Ashman T-L. 2006. Consequences of vegetative herbivory for maintenance of intermediate outcrossing in an annual plant. Ecology 87:2717–27 [Google Scholar]
  119. Steets JA, Wolf DE, Auld JE, Ashman T-L. 2007. The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals. Evolution 61:2043–55 [Google Scholar]
  120. Stevens MT, Esser SM. 2009. Growth-defense tradeoffs differ by gender in dioecious trembling aspen (Populus tremuloides). Biochem. Syst. Ecol. 37:567–73 [Google Scholar]
  121. Stinchcombe JR, Rutter MT, Burdick DS, Tiffin P, Rausher MD, Mauricio R. 2002. Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice. Am. Nat. 160:511–23 [Google Scholar]
  122. Strauss SY. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640–45 [Google Scholar]
  123. Strauss SY, Conner JK, Rush SL. 1996. Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness. Am. Nat. 147:1098–107 [Google Scholar]
  124. Strauss SY, Irwin RE, Lambrix VM. 2004. Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish. J. Ecol. 92:132–41 [Google Scholar]
  125. Strauss SY, Siemens DH, Decher MB, Mitchell-Olds T. 1999. Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution 53:1105–13 [Google Scholar]
  126. Strauss SY, Whittall JB. 2006. Non-pollinator agents of selection on floral traits. Ecology and Evolution of Flowers LD Harder, SCH Barrett 120–38 Oxford, UK: Oxford Univ. Press [Google Scholar]
  127. Tamari G, Borochov A, Atzorn R, Weiss D. 1995. Methyl jasmonate induces pigmentation and flavonoid gene expression in petunia corollas: a possible role in wound response. Physiol. Plant. 94:45–50 [Google Scholar]
  128. Theis N. 2006. Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J. Chem. Ecol. 32:917–27 [Google Scholar]
  129. Theis N, Adler LS. 2012. Advertising to the enemy: Enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93:430–35 [Google Scholar]
  130. Theis N, Barber NA, Gillespie SD, Hazzard RV, Adler LS. 2014. Attracting mutualists and antagonists: Plant trait variation explains the distribution of specialist floral herbivores and pollinators on crops and wild gourds. Am. J. Bot. 101:1314–22 [Google Scholar]
  131. Theis N, Kesler K, Adler LS. 2009. Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers. Am. J. Bot. 96:897–903 [Google Scholar]
  132. Travers SE, Mena-Ali J, Stephenson AG. 2004. Plasticity in the self-incompatibility system of Solanum carolinense. Plant Species Biol. 19:127–35 [Google Scholar]
  133. Turcotte MM, Davies TJ, Thomsen CJM, Johnson MTJ. 2014. Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proc. R. Soc. B 281:20140555 [Google Scholar]
  134. Uno GE. 1982. Comparative reproductive biology of hermaphroditic and male sterile Iris douglasiana Herb. (Iridaceae). Am. J. Bot. 69:818–23 [Google Scholar]
  135. Weiblen GD. 2000. Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphology. Am. J. Bot. 87:1342–57 [Google Scholar]
  136. Wright SI, Kalisz S, Slotte T. 2013. Evolutionary consequences of self-fertilization. Proc. R. Soc. B 280:20130133 [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-112414-054215
Loading
/content/journals/10.1146/annurev-ecolsys-112414-054215
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error