Evolution of Plant Defence to Herbivores

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Ecology".

Deadline for manuscript submissions: closed (20 May 2023) | Viewed by 12016

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Laboratory of Ecological Genetics and Evolution, Department of Evolutionary Ecology, Institute of Ecology, National Autonomous University of Mexico (UNAM). Av. Universidad 3000, Coyoacán, Mexico City 04510, Mexico
Interests: ecological genetics
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Dear Colleagues,

The evolution of plant defence to herbivores is a paradigmatic field of ecology, encompassing a range from genomic changes to ecological communities, seeking to understand the vast array of plant adaptations, from cellular to organismic levels, that originated from/are maintained by interaction with diverse herbivores under varying environmental conditions. The diversity of resistance traits, notably chemical traits, deployed by different plant organs in response to herbivory, has stimulated the scientific search for general patterns, if any, in the conditions and/or factors that promote/limit their evolutionary outcomes. Several hypotheses for the evolution of plant defences to herbivores have been proposed in recent decades, with few maintaining their explanatory power. Advances in the study of specialized (secondary) defence chemicals, and genetic variation of these traits (even at the genomic level), in model and non-model plants have led to the refinement of these hypotheses and the advancement of new ones. This issue of Plants is intended as a forum to present new ideas, and/or empirical and experimental evidence on the evolution of plant defence to herbivores, which will call for new avenues of synthetic research in this topic in the years to come.

Dr. Juan Núñez-Farfán
Guest Editor

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Keywords

  • Phenotypic diversity of plant defence traits
  • Theories of plant defence
  • Environmental circumstances and the evolution of plant defence
  • Genomics of plant defence traits
  • Plant defence and global change

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Published Papers (8 papers)

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Research

15 pages, 2545 KiB  
Article
Effect of Plant Defenses and Plant Nutrients on the Performance of Specialist and Generalist Herbivores of Datura: A Macroevolutionary Study
by Eunice Kariñho-Betancourt, Alejandra Vázquez-Lobo and Juan Núñez-Farfán
Plants 2023, 12(14), 2611; https://doi.org/10.3390/plants12142611 - 11 Jul 2023
Viewed by 900
Abstract
Macroevolutionary patterns in the association between plant species and their herbivores result from ecological divergence promoted by, among other factors, plants’ defenses and nutritional quality, and herbivore adaptations. Here, we assessed the performance of the herbivores Lema trilineata daturaphila, a trophic specialist [...] Read more.
Macroevolutionary patterns in the association between plant species and their herbivores result from ecological divergence promoted by, among other factors, plants’ defenses and nutritional quality, and herbivore adaptations. Here, we assessed the performance of the herbivores Lema trilineata daturaphila, a trophic specialist on Datura, and Spodoptera frugiperda, a polyphagous pest herbivore, when fed with species of Datura. We used comparative phylogenetics and multivariate methods to examine the effects of Datura species’ tropane alkaloids, leaf trichomes, and plant macronutrients on the two herbivores´ performances (amount of food consumed, number of damaged leaves, larval biomass increment, and larval growth efficiency). The results indicate that species of Datura do vary in their general suitability as food host for the two herbivores. Overall, the specialist performs better than the generalist herbivore across Datura species, and performance of both herbivores is associated with suites of plant defenses and nutrient characteristics. Leaf trichomes and major alkaloids of the Datura species are strongly related to herbivores’ food consumption and biomass increase. Although hyoscyamine better predicts the key components of the performance of the specialist herbivore, scopolamine better predicts the performance of the generalist; however, only leaf trichomes are implicated in most performance components of the two herbivores. Nutrient quality more widely predicts the performance of the generalist herbivore. The contrasting effects of plant traits and the performances of herbivores could be related to adaptive differences to cope with plant toxins and achieve nutrient balance and evolutionary trade-offs and synergisms between plant traits to deal with a diverse community of herbivores. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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16 pages, 1263 KiB  
Article
Assessing the Benefits and Costs of the Hydrogen Cyanide Antiherbivore Defense in Trifolium repens
by Hind Emad Fadoul, Lucas J. Albano, Matthew E. Bergman, Michael A. Phillips and Marc T. J. Johnson
Plants 2023, 12(6), 1213; https://doi.org/10.3390/plants12061213 - 07 Mar 2023
Cited by 4 | Viewed by 1624
Abstract
Understanding the evolution of plant defenses against herbivores requires identifying the benefits and costs of defense. Here, we tested the hypothesis that the benefits and costs of hydrogen cyanide (HCN) defense against herbivory on white clover (Trifolium repens) are temperature dependent. [...] Read more.
Understanding the evolution of plant defenses against herbivores requires identifying the benefits and costs of defense. Here, we tested the hypothesis that the benefits and costs of hydrogen cyanide (HCN) defense against herbivory on white clover (Trifolium repens) are temperature dependent. We first tested how temperature affected HCN production in vitro, and then examined how temperature influenced the efficacy of HCN defense of T. repens against a generalist slug (Deroceras reticulatum) herbivore using no-choice and choice feeding trial assays. To understand how temperature affected the costs of defense, plants were exposed to freezing, and HCN production, photosynthetic activity, and ATP concentration were quantified. HCN production increased linearly from 5 °C to 50 °C, and cyanogenic plants experienced reduced herbivory compared to acyanogenic plants only at warmer temperatures when fed upon by young slugs. Freezing temperatures induced cyanogenesis in T. repens and decreased chlorophyll fluorescence. Cyanogenic plants experienced lower ATP levels than acyanogenic plants due to freezing. Our study provides evidence that the benefits of HCN defense against herbivores are temperature dependent, and freezing may inhibit ATP production in cyanogenic plants, but the physiological performance of all plants recovered quickly following short-term freezing. These results contribute to understanding how varying environments alter the benefits and costs of defense in a model system for the study of plant chemical defenses against herbivores. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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15 pages, 2270 KiB  
Article
The Joint Evolution of Herbivory Defense and Mating System in Plants: A Simulation Approach
by Edson Sandoval-Castellanos and Juan Núñez-Farfán
Plants 2023, 12(3), 555; https://doi.org/10.3390/plants12030555 - 26 Jan 2023
Cited by 1 | Viewed by 1248
Abstract
Agricultural losses brought about by insect herbivores can be reduced by understanding the strategies that plants use against insect herbivores. The two main strategies that plants use against herbivory are resistance and tolerance. They are, however, predicted to be mutually exclusive, yet numerous [...] Read more.
Agricultural losses brought about by insect herbivores can be reduced by understanding the strategies that plants use against insect herbivores. The two main strategies that plants use against herbivory are resistance and tolerance. They are, however, predicted to be mutually exclusive, yet numerous populations have them both (hence a mixed defense strategy). This has been explained, among other alternatives, by the non-linear behavior of the costs and benefits of resistance and tolerance and their interaction with plants’ mating system. Here, we studied how non-linearity and mating system affect the evolutionary stability of mixed defense strategies by means of agent-based model simulations. The simulations work on a novel model that was built upon previous ones. It incorporates resistance and tolerance costs and benefits, inbreeding depression, and a continuously scalable non-linearity. The factors that promoted the evolutionary stability of mixed defense strategies include a multiplicative allocation of costs and benefits of resistance and tolerance, a concave non-linearity, non-heritable selfing, and high tolerance costs. We also found new mechanisms, enabled by the mating system, that are worth considering for empirical studies. One was a double trade-off between resistance and tolerance, predicted as a consequence of costs duplication and the inducibility of tolerance, and the other was named the resistance-cost-of-selfing, a term coined by us, and was derived from the duplication of costs that homozygous individuals conveyed when a single resistance allele provided full protection. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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17 pages, 2460 KiB  
Article
Density-Dependent Effects of Simultaneous Root and Floral Herbivory on Plant Fitness and Defense
by Martin Aguirrebengoa, Caroline Müller, Peter A. Hambäck and Adela González-Megías
Plants 2023, 12(2), 283; https://doi.org/10.3390/plants12020283 - 07 Jan 2023
Viewed by 1531
Abstract
Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, [...] Read more.
Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, plants often face co-occurring root and floral herbivory, but few studies have focused on such interactions. Here, we investigated in the field the combined density-dependent effects of root-chewing cebrionid beetle larvae and flower-chewing pierid caterpillars on the fitness and defense of a semiarid Brassicaceae herb. We found that the fitness impact of both herbivore groups was independent and density-dependent. Increasing root herbivore density non-significantly reduced plant fitness, while the relationship between increasing floral herbivore density and the reduction they caused in both seed number and seedling emergence was non-linear. The plant defensive response was non-additive with regard to the different densities of root and floral herbivores; high floral herbivore density provoked compensatory investment in reproduction, and this tolerance response was combined with aboveground chemical defense induction when also root herbivore density was high. Plants may thus prioritize specific trait combinations in response to varying combined below- and aboveground herbivore densities to minimize negative impacts on fitness. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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14 pages, 1903 KiB  
Article
Herbivory in Myrtillocactus geometrizans (Cactaceae): Do Parasitoids Provide Indirect Defense or a Direct Advantage?
by Alicia Callejas-Chavero, Diana Guadalupe Martínez-Hernández, Carlos Fabian Vargas-Mendoza and Arturo Flores-Martínez
Plants 2023, 12(1), 47; https://doi.org/10.3390/plants12010047 - 22 Dec 2022
Cited by 1 | Viewed by 1541
Abstract
Plants respond to herbivory in diverse, complex ways, ranging from avoidance or tolerance to indirect defense mechanisms such as attracting natural enemies of herbivores, i.e., parasitoids or predators, to strengthen their defense. Defense provided by parasitoids to cultivated plants is well documented and [...] Read more.
Plants respond to herbivory in diverse, complex ways, ranging from avoidance or tolerance to indirect defense mechanisms such as attracting natural enemies of herbivores, i.e., parasitoids or predators, to strengthen their defense. Defense provided by parasitoids to cultivated plants is well documented and is used in biological control programs. However, its effectiveness on wild plants under natural conditions has been little studied. Such is the case of the cactus Myrtilllocactus geometrizans (known in Mexico as garambullo), which is consumed by the soft-scale insect Toumeyella martinezae (herbivore) which, in turn, is host to the parasitoid wasp Mexidalgus toumeyellus, and mutualist with the ant Liometopum apiculatum, that tenders and protects it. This study explores the role of the parasitoid as an indirect defense, by examining its effect on both the herbivore and the plant, and how this interaction is affected by the presence of the mutualistic ant. We found that scales adversely affect the cactus’ growth, flower, and fruit production, as well as its progeny’s performance, as seedlings from scale-infested garambullo plants were shorter, and it also favors the presence of fungus (sooty mold). The parasitoid responded positively to herbivore abundance, but the presence of ants reduced the intensity of parasitism. Our results show that parasitoids can function as an indirect defense, but their effectiveness is reduced by the presence of the herbivore’s mutualistic ant. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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8 pages, 1187 KiB  
Communication
Priming by Insects: Differential Effects of Sympatric and Allopatric Priming upon Plant Performance and Tolerance to Herbivory
by Etzel Garrido, Karina Boege, César A. Domínguez and Juan Fornoni
Plants 2022, 11(24), 3567; https://doi.org/10.3390/plants11243567 - 17 Dec 2022
Viewed by 944
Abstract
Plants have evolved multiple mechanisms to defend themselves from their multiple herbivores. Thus, being able to recognise among them and respond accordingly is fundamental for plant survival and reproduction. Defence priming prepares the plant to better or more rapidly respond to future damage; [...] Read more.
Plants have evolved multiple mechanisms to defend themselves from their multiple herbivores. Thus, being able to recognise among them and respond accordingly is fundamental for plant survival and reproduction. Defence priming prepares the plant to better or more rapidly respond to future damage; however, while it is considered an adaptive trait, to date, no studies have evaluated the extent and specificity of the priming recognition. To estimate the costs, benefits and specificity of priming, we used a highly specialist plant–insect system (Datura stramoniumLema daturaphila) and performed a reciprocal transplant experiment with two populations where a priming stimulus (sympatric vs. allopatric) and a damage treatment (sympatric) were applied. We found no evidence of a fitness cost of priming, given that primed plants without damage showed no reduction in fitness. In contrast, our treatments affected the probability of bud abortion. That is, when damaged plants received no priming or the priming came from an allopatric insect, the likelihood of aborting the first bud was 1.9 times greater compared to plants being primed by their sympatric insect. We also found that damaged plants primed with an allopatric insect produced 14% fewer seeds compared to plants receiving a sympatric priming stimulus. Tolerance to herbivore damage was also the lowest when plants received the priming stimulus from an allopatric insect. Overall, these results suggest that, in our study system, plants recognise their local insect population reducing the negative effect of damage through a tolerance response. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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15 pages, 3755 KiB  
Article
Does Domestication Affect Structural and Functional Leaf Epidermal Traits? A Comparison between Wild and Cultivated Mexican Chili Peppers (Capsicum annuum)
by Carlos Serrano-Mejía, Rafael Bello-Bedoy, María Clara Arteaga and Guillermo R. Castillo
Plants 2022, 11(22), 3062; https://doi.org/10.3390/plants11223062 - 11 Nov 2022
Viewed by 1707
Abstract
During domestication, lineages diverge phenotypically and genetically from wild relatives, particularly in preferred traits. In addition to evolutionary divergence in selected traits, other fitness-related traits that are unselected may change in concert. For instance, the selection of chili pepper fruits was not intended [...] Read more.
During domestication, lineages diverge phenotypically and genetically from wild relatives, particularly in preferred traits. In addition to evolutionary divergence in selected traits, other fitness-related traits that are unselected may change in concert. For instance, the selection of chili pepper fruits was not intended to change the structure and function of the leaf epidermis. Leaf stomata and trichome densities play a prominent role in regulating stomatal conductance and resistance to herbivores. Here, we assessed whether domestication affected leaf epidermis structure and function in Capsicum annuum. To do this, we compared leaf stomata and trichome densities in six cultivated varieties of Mexican Capsicum annuum and their wild relative. We measured stomatal conductance and resistance to herbivores. Resistance to (defense against) herbivores was measured as variation in the herbivory rate and larvae mortality of Spodoptera frugiperda fed with leaves of wild and cultivated plants. As expected, the different varieties displayed low divergence in stomatal density and conductance. Leaf trichome density was higher in the wild relative, but variation was not correlated with the herbivory rate. In contrast, a higher mortality rate of S. frugiperda larvae was recorded when fed with the wild relative and two varieties than larvae fed with four other varieties. Overall, although domestication did not aim at resistance to herbivores, this evolutionary process produced concerted changes in defensive traits. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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12 pages, 1323 KiB  
Article
Population-Specific Plant-To-Plant Signaling in Wild Lima Bean
by Patrick Grof-Tisza, Stéphanie Morelon, Gaylord A. Desurmont and Betty Benrey
Plants 2022, 11(18), 2320; https://doi.org/10.3390/plants11182320 - 06 Sep 2022
Viewed by 1418
Abstract
The exposure to volatiles from damaged plants can increase the resistance of the neighboring plants to herbivores. Studies have demonstrated that the strength of this response depends on the level of relatedness between the interacting plants. Indeed, a field study with Phaseolus lunatus [...] Read more.
The exposure to volatiles from damaged plants can increase the resistance of the neighboring plants to herbivores. Studies have demonstrated that the strength of this response depends on the level of relatedness between the interacting plants. Indeed, a field study with Phaseolus lunatus found that the responses to induced volatiles were population-specific; individuals exposed to damaged conspecifics from the ‘local’ population exhibited greater resistance to herbivores than those exposed to damaged conspecifics from ‘foreign’ populations. Here, we repeated this study in the laboratory by placing undamaged plants near damaged plants from either their local or a foreign population. The former plants experienced less herbivory than the latter after a subsequent challenge by a generalist herbivore. To understand the role of the volatiles underlying this observed specificity, we explored the variability in the constitutively released volatiles and volatiles released after mechanical or herbivore damage among the three tested populations of P. lunatus. The total volatile emissions were 5× and 10× higher from the mechanically and herbivore-damaged plants, respectively, compared to the undamaged plants. The populations differed in their relative ratios of dominant constitutive compounds, but no pattern was observed that could explain the differential responses to induced volatiles among the populations. Overall, this study confirms the population-specific volatile-mediated interactions in P. lunatus. Full article
(This article belongs to the Special Issue Evolution of Plant Defence to Herbivores)
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