Abstract
Previous studies have shown a causal link between mammalian herbivory, tolerance, and chemical defense in Arabidopsis thaliana, driven by the process of endoreduplication (replication of the genome without mitosis). Removal of the apical meristem by mammalian herbivores lowers auxin, which triggers entry into the endocycle. Increasing chromosome number through endoreduplication, and therefore gene copy number, provides a means of increasing gene expression promoting rapid regrowth rates, higher defensive chemistry and enhanced fitness. Here, we assess whether insect leaf-feeding elicits the same compensatory response as the removal of apical dominance. Insect feeding has been shown to downregulate auxin production, which should trigger endoreduplication. Results here support this contention; insect leaf-feeding by Trichoplusia ni elicited a compensatory response similar to that of mammalian herbivores—an ecotype-specific response consistent with the level of endoreduplication. The interactive effects of mammalian and insect herbivory were also assessed to determine whether interactions were additive (pairwise) or non-additive (diffuse) on tolerance (fitness). Specifically, results indicate that herbivory is either diffuse (a significant clipping × T. ni interaction) or pairwise (no significant interaction between clipping and T. ni herbivory), dependent upon plant genotype and compensatory ability. In general, herbivore-induced changes in plant quality appear to be responsible for the observed differences in herbivory and fitness compensation. We discuss the importance of evaluating endoreduplication among plants within a population to avoid masking the association between tolerance and resistance and the fitness consequences of multi-herbivore interactions.
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References
Anderson LL, Paige KN (2003) Multiple herbivores and coevolutionary interactions in an Ipomopsis hybrid swarm. Evol Ecol 17:139–156. https://doi.org/10.1023/A:1023066101074
Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tobacco. J Chem Ecol 15:1661–1680
Baldwin IT, Zhang Z-P, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397–404
Barow M, Meister A (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ 26:571–584. https://doi.org/10.1046/j.1365-3040.2003.00988.x
Beekwilder J, Van Leeuwen W, Van Dam NM, Bertossi M, Grandi V, Mizzi L, Verbocht H (2008) The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS One 3:e2068. https://doi.org/10.1371/journal.pone.0002068
Brodsky WY, Uryvaeva IV (1977) Cell polyploidy: its relation to tissue growth and function. Int Rev Cytol 50:275–332. https://doi.org/10.1016/S0074-7696(08)60100-X
Brown DG, Weis AE (1995) Direct and indirect effects of prior grazing of goldenrod upon the performance of a leaf beetle. Ecology 76:426–436. https://doi.org/10.2307/1941201
Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481. https://doi.org/10.1016/S0031-9422(02)00549-6
Fritz RS (1992) Community structure and species interactions of phytophagous insects on resistant and susceptible host plants. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago, pp 240–277
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051. https://doi.org/10.1126/science.220.4601.1049
Garren JM, Strauss SY (2009) Population-level compensation by an invasive thistle thwarts biological control from seed predators. Ecol Appl 19:709–721. https://doi.org/10.1890/07-0646.1
Hougen-Eitzman D, Rausher MD (1994) Interactions between herbivorous insects and plant-insect coevolution. Am Nat 143:677–697. https://doi.org/10.1086/285626
Ishida T, Adachi S, Yoshimura M, Shimizu K, Umeda M, Sugimoto K (2010) Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 137:63–71. https://doi.org/10.1242/dev.035840
Jander G, Cui J, Nhan B, Pierce NE, Ausubel FM (2001) The TASTY locus on chromosome 1 of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni. Plant Physiol 126:890–898. https://doi.org/10.1104/pp.126.2.890
Juenger T, Bergelson J (1998) Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution 52:1583–1592. https://doi.org/10.1111/j.1558-5646.1998.tb02239.x
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
Karban R (1989) Fine-scale adaptation of herbivorous thrips to individual host plants. Nature 340:60–61. https://doi.org/10.1038/340060a0
Karban R, Strauss SY (1993) Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. Ecology 74:39–46. https://doi.org/10.2307/1939499
Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J (2001) The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13:2793–2807. https://doi.org/10.1105/tpc.010261
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
Li Q, Eigenbrode SD, Stringam GR, Thiagarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419. https://doi.org/10.1007/s10886-010-9825-z
Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750. https://doi.org/10.1046/j.1365-313X.1993.04040745.x
Louda SM (1983) Seed predation and seedling mortality in the recruitment of a shrub, Haplopappus venetus (Asteraceae), along a climatic gradient. Ecology 64:511–521. https://doi.org/10.2307/1939971
Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311
McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393. https://doi.org/10.1146/annurev.ento.43.1.369
Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668. https://doi.org/10.1105/tpc.5.11.1661
Mesa JM, Scholes DR, Juvik JA, Paige KN (2017) Molecular constraints on resistance–tolerance trade-offs. Ecology 98:2528–2537. https://doi.org/10.1002/ecy.1948
Muola A, Mutikainen P, Laukkanen L, Lilley M, Leimu R (2010) Genetic variation in herbivore resistance and tolerance: the role of plant life-history stage and type of damage. J Evol Biol 23:2185–2196. https://doi.org/10.1111/j.1420-9101.2010.02077.x
Nagl W (1976) DNA endoreduplication and polyteny understood as evolutionary strategies. Nature 261:614–615. https://doi.org/10.1038/261614a0
Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566. https://doi.org/10.1146/annurev.ecolsys.38.091206.095822
Onkokesung N, Gális I, von Dahl CC, Matsuoka K, Saluz HP, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol 153:785–798. https://doi.org/10.1104/pp.110.156232
Paige KN (1992) The effects of fire on scarlet gilia: an alternative selection pressure to herbivory? Oecologia 92:229–235. https://doi.org/10.1086/284645
Paige KN (2018) Overcompensation, environmental stress, and the role of endoreduplication. Am J Bot 105:1105–1108. https://doi.org/10.1002/ajb2.1135
Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416
Pigliucci M (2002) Ecology and evolutionary biology of Arabidopsis. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, p e0003
Pilson D (1996) Two herbivores and constraints on selection for resistance in Brassica rapa. Evolution 50:1492–1500. https://doi.org/10.1111/j.1558-5646.1996.tb03922.x
Poelman EH, Broekgaarden C, Van Loon JJA, Docke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365. https://doi.org/10.1111/j.1365-294X.2008.03838.x
Russell-Mercier JL, Sargent RD (2015) Indirect effects of herbivory on plant–pollinator interactions in invasive Lythrum salicaria. Am J Bot 102:661–668. https://doi.org/10.3732/ajb.1500043
Schat M, Blossey B (2005) Influence of natural and simulated leaf beetle herbivory on biomass allocation and plant architecture of purple loosestrife (Lythrum salicaria L.). Environ Entomol 34:906–914. https://doi.org/10.1603/0046-225X-34.4.906
Scholes DR, Paige KN (2011) Chromosomal plasticity: mitigating the impacts of herbivory. Ecology 92:1691–1698. https://doi.org/10.1890/10-2269.1
Scholes DR, Paige KN (2014) Plasticity in ploidy underlies plant fitness compensation to herbivore damage. Mol Ecol 23:4862–4870. https://doi.org/10.1111/mec.12894
Scholes DR, Dalrymple J, Mesa JM, Banta JA, Paige KN (2017) An assessment of the molecular mechanisms contributing to tolerance to apical damage in natural populations of Arabidopsis thaliana. Plant Ecol 218:265–276. https://doi.org/10.1007/s11258-016-0685-7
Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151. https://doi.org/10.1126/science.217.4555.149
Shi Q, Li C, Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L. induced by mechanical wounding is regulated by auxin. J Exp Bot 57:2899–2907. https://doi.org/10.1093/jxb/erl051
Shorey HH, Andres LA, Hale RL Jr (1962) The biology of Trichoplusia ni (Lepidoptera: Noctuidae) I. Life history and behavior. Ann Entomol Soc Am 55:591–597. https://doi.org/10.1093/aesa/55.5.591
Siddappaji MH, Scholes DR, Bohn M, Paige KN (2013) Overcompensation in response to herbivory in Arabidopsis thaliana: the role of glucose-6-phosphate dehydrogenase and the oxidative pentose-phosphate pathway. Genetics 195:589–598. https://doi.org/10.1534/genetics.113.154351
Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595. https://doi.org/10.1146/annurev.ecolsys.31.1.565
Strauss SY, Conner JK, Lehtilä KP (2001) Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. Am Nat 158:496–504. https://doi.org/10.1086/323116
Strauss SY, Watson W, Allen MT (2003) Predictors of male and female tolerance to insect herbivory in Raphanus raphanistrum. Ecology 84:2074–2082. https://doi.org/10.1890/02-0267
Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered approach to diffuse (co) evolution. New Phytol 165:81–90. https://doi.org/10.1111/j.1469-8137.2004.01228.x
Thomsen CJ, Sargent RD (2017) Evidence that a herbivore tolerance response affects selection on floral traits and inflorescence architecture in purple loosestrife (Lythrum salicaria). Ann Bot 119:1295–1303. https://doi.org/10.1093/aob/mcx026
Utsumi S, Ohgushi T (2009) Community-wide impacts of herbivore-induced plant regrowth on arthropods in a multi-willow species system. Oikos 118:1805–1815. https://doi.org/10.1111/j.1600-0706.2009.17580.x
Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629. https://doi.org/10.1890/03-0622
Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790. https://doi.org/10.1016/j.cub.2007.09.025
Wathelet JP, Iori R, Mabon N, Palmieri S, Leoni O, Rollin P, Marlier M (2001) Determination of the response factors of several desulfo-glucosinolates used for quantitative analysis of Brassicaceae. International Rapeseed Congress Technical Meeting, Poznan, Poland, June 5-7 2001
Wise MJ, Sacchi CF (1996) Impact of two specialist insect herbivores on reproduction of horse nettle, Solanum carolinense. Oecologia 108:328–337. https://doi.org/10.1007/BF00334658
Acknowledgements
We thank the Flow Cytometry Facility at Iowa State for their aid in measuring endopolyploidy. We also thank Katy Heath and Ray Zielinski for their comments that helped improve this manuscript. This research was supported by awards from the National Science Foundation (DEB-1146085) and the University of Illinois Campus Research Board to KNP.
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KNP and JMM conceived and designed the experiments. JMM performed the experiments. JMM and KNP analyzed the data. JAJ and JMM conducted the chemical analyses. JMM and KNP wrote the manuscript, JAJ provided editorial services.
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Communicated by Merijn Kant.
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Mesa, J.M., Juvik, J.A. & Paige, K.N. Individual and interactive effects of herbivory on plant fitness: endopolyploidy as a driver of genetic variation in tolerance and resistance. Oecologia 190, 847–856 (2019). https://doi.org/10.1007/s00442-019-04458-1
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DOI: https://doi.org/10.1007/s00442-019-04458-1