Background and aims – A plant’s tolerance of herbivory depends on its ability to endure and compensate for damage so as to lessen the impact that herbivores have on the plant’s performance (e.g. its growth, reproduction, or fitness). While tolerance of herbivory is beneficial to plants, it is rarely complete, and individuals in plant populations tend to vary in their levels of tolerance. The goal of this study was to investigate potential costs associated with tolerance of leaf and floral herbivory in horsenettle (Solanum carolinense), a perennial herbaceous weed that is often subjected to high levels of damage from a diversity of herbivores.
Material and methods – We exposed 96 potted individuals across eight genets of horsenettle to factorial treatments of leaf herbivory by lace bugs and simulated floral herbivory by weevils. We quantified tolerance for each plant genet for both types of herbivory in terms of the impact of damage on the number of flowers opened, number of seeds produced, and root biomass (i.e. paternal, maternal, and vegetative tolerance, respectively).
Key results – Plant genets ranged widely in their ability to compensate for leaf and flower damage. While there was little evidence for tradeoffs in tolerance through the different routes, there was strong evidence of tradeoffs in genets’ abilities to tolerate herbivore damage to leaves and damage to flowers.
Conclusion – Tolerance is a useful defence strategy to cope with damage caused by herbivores, but its evolution may be constrained by concomitant costs and tradeoffs. The evolutionary role of the tradeoffs identified in this study are likely to be greater the more species of herbivores a plant hosts, and the more that herbivore levels vary both spatially and temporally.
Agrawal A.A. 2011. Current trends in the evolutionary ecology of plant defence. Functional Ecology 25: 420–432. https://doi.org/10.1111/j.1365-2435.2010.01796.x
Avila-Sakar G. 2020. Resource allocation and defense against herbivores in wild and model plants. In: Núñez-Farfán J. & Valverde P.L. (eds) Evolutionary ecology of plant-herbivore interaction: 37–61. Springer Nature Switzerland AG, Cham, Switzerland. https://doi.org/10.1007/978-3-030-46012-9_3
Bardner R. & Fletcher K.E. 1974. Insect infestations and their effects on the growth and yield of field crops: a review. Bulletin of Entomological Research 64: 141–160. https://doi.org/10.1017/s0007485300027061
Bassett I.J. & Munro D.B. 1986. The biology of canadian weeds. 78. Solanum carolinense L. and Solanum rostratum Dunal. Canadian Journal of Plant Science 66: 977–991. https://doi.org/10.4141/cjps86-120
Boalt E. & Lehtilä K. 2007. Tolerance to apical and foliar damage: costs and mechanisms in Raphanus raphanistrum. Oikos 116: 2071–2081. https://doi.org/10.1111/j.2007.0030-1299.16056.x
Burke H.R. 1976. Bionomics of the anthonomine weevils. Annual Review of Entomology 21: 283–303. https://doi.org/10.1146/annurev.en.21.010176.001435
Carmago I.D. 2020. Toward a unifying quest for an understanding of tolerance mechamisms to herbivore damage and its eco-evolutionary dynamics. In: Núñez-Farfán J. & Valverde P.L. (eds) Evolutionary ecology of plant-herbivore interaction: 63–86. Springer Nature Switzerland AG, Cham, Switzerland. https://doi.org/10.1007/978-3-030-46012-9_4
Carmona D. & Fornoni J. 2013. Herbivores can select for mixed defensive strategies in plants. New Phytologist 197: 576–585. https://doi.org/10.1111/nph.12023
Chittenden F.H. 1895. The potato-bud weevil. Insect Life 7: 350–352
Cipollini D., Walters D. & Voelckel C. 2014. Costs of resistance in plants: from theory to evidence. Annual Plant Reviews 47: 263–308. https://doi.org/10.1002/9781118829783.ch8
Dahlgren E. & Lehtilä K. 2015. Tolerance to apical and leaf damage of Raphanus raphanistrum in different competitive regimes. Ecology and Evolution 5: 5193–5202. https://doi.org/10.1002/ece3.1759
Elle E. 1998. The quantitative genetics of sex allocation in the andromonoecious perennial Solanum carolinense (L.). Heredity 80: 481–488. https://doi.org/10.1046/j.1365-2540.1998.00319.x
Elle E. & Meagher T.R. 2000. Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). II. Paternity and functional gender. The American Naturalist 156: 622–636. https://doi.org/10.2307/3079067
Fineblum W.L. & Rausher M.D. 1995. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377: 517–520. https://doi.org/10.1038/377517a0
Fornoni J. 2011. Ecological and evolutionary implications of plant tolerance to herbivory. Functional Ecology 25: 399–407. https://doi.org/10.1111/j.1365-2435.2010.01805.x
Fornoni J. & Núñez-Farfán J. 2000. Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation. Evolution 54: 789–797. https://doi.org/10.1111/j.0014-3820.2000.tb00080.x
Fornoni J., Núñez-Farfán J. & Valverde P.L. 2003. Evolutionary ecology of tolerance to herbivory: advances and perspectives. Comments on Theoretical Biology 8: 643–663.
Fornoni J., Valverde P.L. & Núñez-Farfán J. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58: 1696–1704. https://doi.org/10.1554/03-481
Frank J.R. 1990. Influence of horsenettle (Solanum carolinense) on snapbean (Phaseolus vulgaris). Weed Science 38: 220–223. https://doi.org/10.1017/S0043174500056435
Garcia L.C. & Eubanks M.D. 2019. Overcompensation for insect herbivory: a review and meta-analysis of the evidence. Ecology 100: e02585. https://doi.org/10.1002/ecy.2585
Garrido E., Llamas-Guzmán L.P. & Fornoni J. 2016. The effect of frequency-dependent selection on resistance and tolerance to herbivory. Journal of Evolutionary Biology 29: 483–489. https://doi.org/10.1111/jeb.12768
Gómez J.M. & Fuentes M. 2001. Compensatory responses of an arid land crucifer, Chorispora tenella (Brassicaceae), to experimental flower removal. Journal of Arid Environments 49: 855–863. https://doi.org/10.1006/jare.2001.0798
Gorrell R.M., Bingham S.W. & Foy C.L. 1981. Control of horsenettle (Solanum carolinense) fleshy roots in pastures. Weed Science 29: 586–589. https://doi.org/10.1017/s0043174500063773
Hakes A.S. & Cronin J.T. 2011. Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): genetic variability, costs, and selection for multiple traits. American Journal of Botany 98: 1446–1455. https://doi.org/10.3732/ajb.1000485
Hendrix S.D. 1984. Reactions of Heracleum lanatum to floral herbivory by Depressaria pastinacella. Ecology 65: 191–197. https://doi.org/10.2307/1939470
Hendrix S.D. & Trapp E.J. 1981. Plant-herbivore interactions: insect induced changes in host plant sex expression and fecundity. Oecologia 49: 119–122. https://doi.org/10.1007/bf00376908
Hochwender C.G., Marquis R.J. & Stowe K.A. 2000. The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca. Oecologia 122: 361–370. https://doi.org/10.1007/s004420050042
Ilnicki R.D., Tisdell T.F., Fertig S.N. & Furrer A.H. Jr. 1962. Life history studies as related to weed control in the northeast – horse nettle. Bulletin 368. Agricultural Experimental Station, University of Rhode Island, Kingston, RI.
Imura O. 2003. Herbivorous arthropod community of an alien weed Solanum carolinense L. Applied Entomology and Zoology 38: 293–300. https://doi.org/10.1303/aez.2003.293
Juenger T. & Bergelson J. 2000. The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54: 764–777. https://doi.org/10.1111/j.0014-3820.2000.tb00078.x
Juenger T. & Lennartsson T. 2000. Tolerance in plant ecology and evolution: toward a more unified theory of plant-herbivore interaction. Evolutionary Ecology 14: 283–287. https://doi.org/10.1023/a:1017323621181
Karban R. & Baldwin I.T. 1997. Induced responses to herbivory. University of Chicago Press, Chicago. https://doi.org/10.7208/chicago/9780226424972.001.0001
König M.A.E., Lehtilä K., Wiklund C. & Ehrlén J. 2014. Among-population variation in tolerance to larval herbivory by Anthocharis cardamines in the polyploid herb Cardamine pratensis. PLoS ONE 9: e99333. https://doi.org/10.1371/journal.pone.0099333
Krupnick G.A. & Weis A.E. 1998. Floral herbivore effect on the sex expression of an andromonoecious plant, Isomeris arborea (Capparaceae). Plant Ecology 134: 151–162.
Lehtilä K. 1999. Impact of herbivore tolerance and resistance on plant life histories. In: Vuorisalo T.O. & Mutikainen P.K. (eds) Life history evolution in plants: 303–328. Kluwer Academic Publishers, Dordrecht.
Leimu R. & Koricheva J. 2006. A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112: 1–9. https://doi.org/10.1111/j.0030-1299.2006.41023.x
Lloyd D.G. 1980. Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytologist 86: 69–79. https://doi.org/10.1111/j.1469-8137.1980.tb00780.x
Loeb M.L.G. 2003. Evolution of egg dumping in a subsocial insect. The American Naturalist 161: 129–142. https://doi.org/10.1086/344918
Loeb M.L.G., Diener L.M. & Pfennig D.W. 2000. Egg-dumping lace bugs preferentially oviposit with kin. Animal Behaviour 59: 379–383. https://doi.org/10.1006/anbe.1999.1328
Manzaneda A.J., Prasad K.V.S.K. & Mitchell-Olds T. 2010. Variation and fitness costs for tolerance to different types of herbivore damage in Boechera stricta genotypes with contrasting glucosinolate structures. New Phytologist 188: 464–477. https://doi.org/10.1111/j.1469-8137.2010.03385
Mauricio R. 2000. Natural selection and the joint evolution of tolerance and resistance as plant defenses. Evolutionary Ecology 14: 491–507. https://doi.org/10.1023/a:1010909829269
Mauricio R., Rausher M.D. & Burdick D.S. 1997. Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78: 1301–1311. https://doi.org/fwkv9x
May P.G. & Spears E.E. Jr. 1988. Andromonoecy and variation in phenotypic gender of Passiflora incarnata (Passifloraceae). American Journal of Botany 75: 1830–1841. https://doi.org/10.1002/j.1537-2197.1988.tb11263.x
NAPPO 2003. Pra/grains panel facts sheet – Solanum carolinense L. North American Plant Protection Organization, Ottawa.
Nichols R.L., Cardina J. & Gaines T.P. 1991. Growth, reproduction and chemical composition of horsenettle (Solanum carolinense). Weed Technology 5: 513–520. https://doi.org/10.1017/s0890037x00027251
Nihranz C.T., Walker W.S., Brown S.J., Mescher M.C., De Moraes C.M. & Stephenson A.G. 2020. Transgenerational impacts of herbivory and inbreeding on reproductive output in Solanum carolinense. American Journal of Botany 107: 1–12. https://doi.org/10.1002/ajb2.1402
Núñez-Farfán J., Fornoni J. & Valverde P.L. 2007. The evolution of resistance and tolerance to herbivores. Annual Review of Ecology, Evolution and Systematics 38: 541–566. https://doi.org/10.1146/annurev.ecolsys.38.091206.095822
Núñez-Farfán J. & Valverde P.L. 2020. Evolutionary ecology of plant-herbivore interaction. Springer Nature Switzerland AG, Cham, Switzerland. https://doi.org/10.1007/978-3-030-46012-9
Painter R.H. 1958. Resistance of plants to insects. Annual Review of Entomology 3: 267–290.
Pearse I.S., Aguilar J., Schroder J. & Strauss S.Y. 2017. Macroevolutionary constraints to tolerance: trade-offs with drought tolerance and phenology, but not resistance. Ecology 98: 2758–2772. https://doi.org//10.1002/ecy.1995
Pilson D. 2000. The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evolutionary Ecology 14: 457–489. https://doi.org/10.1023/a:1010953714344
Richman A.D., Kao T.-H., Schaeffer S.W. & Uyenoyama M.K. 1995. S-allele sequence diversity in natural populations of Solanum carolinense (horsenettle). Heredity 75: 405–415. https://doi.org/10.1038/hdy.1995.153
Rosenthal J.P. & Kotanen P.M. 1994. Terrestrial plant tolerance to herbivory. Trends in Ecology & Evolution 9: 145–148. https://doi.org/10.1016/0169-5347(94)90180-5
Scholes D.R., Rasnick E.N. & Paige K.N. 2017. Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance. Oecologia 184: 643–652. https://doi.org//10.1007/s00442-017-3897-1
Simms E.L. 2000. Defining tolerance as a norm of reaction. Evolutionary Ecology 14: 563–570. https://doi.org/10.1023/a:1010956716539
Simms E.L. & Triplett J. 1994. Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48: 1973–1985. https://doi.org/10.1111/j.1558-5646.1994.tb02227.x
Solomon B.P. 1985. Environmentally influenced changes in sex expression in an andromonoecious plant. Ecology 66: 1321–1332. https://doi.org/10.2307/1939185
Solomon B.P. 1986. Sexual allocation and andromonoecy: resource investment in male and hermaphrodite flowers of Solanum carolinense (Solanaceae). American Journal of Botany 73: 1215–1221. https://doi.org/10.1002/j.1537-2197.1986.tb08568.x
Solomon B.P. 1988. Patterns of pre- and postfertilization resource allocation within an inflorescence: evidence for interovary competition. American Journal of Botany 75: 1074–1079. https://doi.org/10.1002/j.1537-2197.1988.tb08814.x
Stephenson A.G. 1992. The regulation of maternal investment in plants. In: Marshall C. & Grace J. (eds) Fruit and seed production. Aspects of development, environmental physiology and ecology: 151–171. Cambridge University Press, Cambridge, UK. https://doi.org/10.1017/cbo9780511752322
Steven J.C., Peroni P.A. & Rowell E. 1999. The effects of pollen addition on fruit set and sex expression in the andromonoecious herb horsenettle (Solanum carolinense). The American Midland Naturalist 141: 247–252. https://doi.org/c56rdg
Stinchcombe J.R. & Rausher M.D. 2002. The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proceedings of the Royal Society of London B. 269: 1241–1246. https://doi.org/10.1098/rspb.2002.2015
Stowe K.A., Marquis R.J., Hochwender C.G. & Simms E.L. 2000. The evolutionary ecology of tolerance to consumer damage. Annual Review of Ecology and Systematics 31: 565–595. https://doi.org/10.1146/annurev.ecolsys.31.1.565
Strauss S.Y. & Agrawal A.A. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution 14: 179–185. https://doi.org/10.1016/s0169-5347(98)01576-6
Strauss S.Y., Watson W. & Allen M.T. 2003. Predictors of male and female tolerance to insect herbivory in Raphanus raphanistrum. Ecology 84: 2074–2082. https://doi.org/10.1890/02-0267
Tallamy D.W. & Denno R.F. 1981. Maternal care in Gargaphia solani (Hemiptera: Tingidae). Animal Behavior 29: 771–778. https://doi.org/10.1016/s0003-3472(81)80010-3
Tallamy D.W. & Denno R.F. 1982. Life history trade-offs in Gargaphia solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63: 616–620. https://doi.org/10.2307/1936779
Tallamy D.W. & Horton L.A. 1990. Costs and benefits of the egg-dumping alternative in Gargaphia lace bugs (Hemiptera: Tingidae). Animal Behaviour 39: 352–359. https://doi.org/10.1016/s0003-3472(05)80881-4
Tiffin P. 2000. Mechanisms of tolerance to herbivore damage: what do we know? Evolutionary Ecology 14: 523–536. https://doi.org/10.1023/a:1010881317261
Tiffin P. & Inouye B.D. 2000. Measuring tolerance to herbivory: accuracy and precision of estimates using natural versus imposed damage. Evolution 54: 1024–1029. https://doi.org/10.1111/j.0014-3820.2000.tb00101.x
Tiffin P. & Rausher M.D. 1999. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. The American Naturalist 154: 700–716. https://doi.org/10.1086/303271
Trumble J.T., Kolodny-Hirsch D.M. & Ting I.P. 1993. Plant compensation for arthropod herbivory. Annual Review of Entomology 38: 93–119. https://doi.org/10.1146/annurev.en.38.010193.000521
Turley N.E., Godfrey R.M. & Johnson M.T.J. 2013. Evolution of mixed strategies of plant defense against herbivores. New Phytologist 197: 359–361. https://doi.org/10.1111/nph.12103
Tuttle D.M. 1956. Notes on the life history of seven species of Anthonomus occurring in illinois (Curculionidae, Coleoptera). Annals of the Entomological Society of America 49: 170–173. https://doi.org/10.1093/aesa/49.2.170
Vallejo-Marín M. & Rausher M.D. 2007. The role of male flowers in andromonoecious species: energetic costs and siring success in Solanum carolinense L. Evolution 61: 404–412. https://doi.org/10.1111/j.1558-5646.2007.00031.x
Wise M.J. 2007a. Evolutionary ecology of resistance to herbivory: an investigation of potential genetic constraints in the multiple-herbivore community of Solanum carolinense. New Phytologist 175: 773–784. https://doi.org/10.1111/j.1469-8137.2007.02143.x
Wise M.J. 2007b. The herbivores of horsenettle, Solanum carolinense, in northern Virginia: natural history and damage assessment. Southeastern Naturalist 6: 505–522. https://doi.org/fgntq5
Wise M.J. 2010. Diffuse interactions between two herbivores and constraints on the evolution of resistance in horsenettle (Solanum carolinense). Arthropod-Plant Interactions 4: 159–164. https://doi.org/10.1007/s11829-010-9094-3
Wise M.J. 2018. The notoriously destructive potato stalk borer (Trichobaris trinotata) has negligible impact on its native host, Solanum carolinense (horsenettle). Arthropod-Plant Interactions 12: 385–394. https://doi.org/10.1007/s11829-017-9587-4
Wise M.J. & Abrahamson W.G. 2017. Constraints of the evolution of resistance to gall flies in Solidago altissima: resistance sometimes costs more than it is worth. New Phytologist 215: 423–433. https://doi.org/10.1111/nph.14583
Wise M.J. & Cummins J.J. 2002. Nonfruiting hermaphroditic flowers as reserve ovaries in Solanum carolinense. The American Midland Naturalist 148: 236–245. https://doi.org/btggvk
Wise M.J. & Cummins J.J. 2006. Strategies of Solanum carolinense for regulating maternal investment in response to foliar and floral herbivory. Journal of Ecology 94: 629–636. https://doi.org/10.1111/j.1365-2745.2006.01118.x
Wise M.J. & Cummins J.J. 2007. Herbivory as an agent of natural selection for floral-sex ratio in horsenettle (Solanum carolinense). Evolutionary Ecology Research 9: 1319–1328.
Wise M.J. & Hébert J.B. 2010. Herbivores exert natural selection for floral-sex ratio in a field population of horsenettle, Solanum carolinense. Ecology 91: 937–943. https://doi.org/10.1890/09-1373.1
Wise M.J. & Rausher M.D. 2013. Evolution of resistance to a multiple-herbivore community: genetic correlations, diffuse coevolution, and constraints on the plant’s response to selection. Evolution 67: 1767–1779. https://doi.org/10.1111/evo.12061
Wise M.J. & Sacchi C.F. 1996. Impact of two specialist insect herbivores on reproduction of horse nettle, Solanum carolinense. Oecologia 108: 328–337. https://doi.org/10.1007/bf00334658
Wise M.J., Abrahamson W.G. & Landis K. 2006. Edaphic environment, gall midges, and goldenrod clonal expansion in a mid-successional old-field. Acta Oecologica 30: 365–373. https://doi.org/10.1016/j.actao.2006.07.001
Wise M.J., Cummins J.J. & De Young C. 2008. Compensation for floral herbivory in Solanum carolinense: identifying mechanisms of tolerance. Evolutionary Ecology 22: 19–37. https://doi.org/10.1007/s10682-007-9156-x
Züst T. & Agrawal A.A. 2017. Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology 68: 10.11–10.22. https://doi.org/10.1146/annurev-arplant-042916-040856
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