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Individual and interactive effects of herbivory on plant fitness: endopolyploidy as a driver of genetic variation in tolerance and resistance

  • J. Miles Mesa
  • John A. Juvik
  • Ken N. PaigeEmail author
Plant-microbe-animal interactions – original research


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.


Arabidopsis Endoreduplication Fitness compensation Glucosinolates Overcompensation Oxidative pentose phosphate pathway Resistance Tolerance 



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.

Author contribution statement

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.

Supplementary material

442_2019_4458_MOESM1_ESM.docx (58 kb)
Supplementary material 1 (DOCX 58 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Integrative BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Department of Crop SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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