Anurag A. Agrawal

The ecology and evolution of plant tolerance to herbivory

The tolerance of plants to herbivory reflects the degree to which a plant can regrow and reproduce after damage from herbivores. Autoecological factors, as well as the influence of competitors and mutualists, affect the level of plant tolerance. Recent work indicates that there is a heritable basis for tolerance and that it can evolve in natural plant populations. Although tolerance is probably not a strict alternative to plant resistance, there could be inter- and intraspecific tradeoffs between these defensive strategies.

Transgenerational induction of defences in animals and plants

Predators are potent agents of natural selection in biological communities. Experimental studies have shown that the introduction of predators can cause rapid evolution of defensive morphologies and behaviours in prey and chemical defences in plants. Such defences may be constitutively expressed (phenotypically fixed) or induced when predators initially attack. Here we show that non-lethal exposure of an animal to carnivores, and a plant to a herbivore, not only induces a defence, but causes the attacked organisms to produce offspring that are better defended than offspring from unthreatened parents. This transgenerational effect, referred to as a maternally induced defence, is in contrast to the more common defences induced in single individuals within a generation. Transgenerational induction of defences is a new level of phenotypic plasticity across generations that may be an important component of predator–prey interactions.

PLANT DEFENSE SYNDROMES

Given that a plants defensive strategy against herbivory is never likely to be a single trait, we develop the concept of plant defense syndromes, where association with specific ecological interactions can result in convergence on suites of covarying defensive traits. Defense syndromes can be studied within communities of diverse plant species as well as within clades of closely related species. In either case, theory predicts that plant defense traits can consistently covary across species, due to shared evolutionary ancestry or due to adaptive convergence. We examined potential defense syndromes in 24 species of milkweeds (Asclepias spp.) in a field experiment. Employing phylogenetically independent contrasts, we found few correlations between seven defensive traits, no bivariate trade-offs, and notable positive correlations between trichome density and latex production, and between C:N ratio and leaf toughness. We then used a hierarchical cluster analysis to produce a phenogram of defense trait similarity among the 24 species. This analysis revealed three distinct clusters of species. The defense syndromes of these species clusters are associated with either low nutritional quality or a balance of higher nutritional quality coupled with physical or chemical defenses. The phenogram based on defense traits was not congruent, however, with a molecular phylogeny of the group, suggesting convergence on defense syndromes. Finally, we examined the performance of monarch butterfly caterpillars on the 24 milkweed species in the field; monarch growth and survival did not differ on plants in the three syndromes, although multiple regression revealed that leaf trichomes and toughness significantly reduced caterpillar growth. The discovery of convergent plant defense syndromes can be used as a framework to ask questions about how abiotic environments, communities of herbivores, and biogeography are associated with particular defense strategies of plants.

Filling key gaps in population and community ecology

We propose research to fill key gaps in the areas of population and community ecology, based on a National Science Foundation workshop identifying funding priorities for the next 5-10 years. Our vision for the near future of ecology focuses on three core areas: predicting the strength and context-dependence of species interactions across multiple scales; identifying the importance of feedbacks from individual interactions to ecosystem dynam- ics; and linking pattern with process to understand species coexistence. We outline a combination of theory devel- opment and explicit, realistic tests of hypotheses needed to advance population and community ecology.

Re-evaluating the costs and limits of adaptive phenotypic plasticity

When the optimal phenotype differs among environments, adaptive phenotypic plasticity can evolve unless constraints impede such evolution. Costs and limits of plasticity have been proposed as important constraints on the evolution of plasticity, yet confusion exists over their distinction. We attempt to clarify these concepts by reviewing their categorization and measurement, highlighting how costs and limits are defined in different currencies (and may describe the same phenomenon). Conclusions from studies that measure the costs of plasticity have been equivocal, but we caution that these conclusions may be premature owing to a potentially common correlation between environment-specific trait values and the magnitude of trait plasticities (i.e. multi-collinearity) that results in imprecise and/or biased estimates of the costs. Meanwhile, our understanding of the limits of plasticity, and how they may be underlain by the costs of plasticity, is still in its infancy. Based on our re-evaluation of these constraints, we discuss areas for future research.

Specialist versus generalist insect herbivores and plant defense

There has been a long-standing hypothesis that specialist and generalist insects interact with plants in distinct ways. Although many tests exist, they typically compare only one species of each, they sometimes confound specialization and feeding guild, and often do not link chemical or transcriptional measures of the plant to actual resistance. In this review, we synthesize current data on whether specialists and generalists actually differ, with special attention to comparisons of their differential elicitation of plant responses. Although we find few consistencies in plant induction by specialists versus generalists, feeding guilds are predictive of differential plant responses. We outline a novel set of predictions based on current coevolutionary hypotheses and make methodological suggestions for improved comparisons of specialists and generalists.

INDUCED RESPONSES TO HERBIVORY IN WILD RADISH: EFFECTS ON SEVERAL HERBIVORES AND PLANT FITNESS

Induced responses to herbivory are changes in plant quality following initial damage by herbivores. These changes can negatively affect subsequent herbivores. I studied induced responses in annual wild radish plants, Raphanus raphanistrum and R. sativus (Brassicaceae), which included increased density and total number of setose trichomes on newly formed leaves of previously damaged plants compared to undamaged controls. I also characterized the effects of induced responses on the preference and performance of several herbivores and the net consequences for plant performance in the field. Wild radish plants damaged by caterpillars or sprayed with a natural plant response elicitor, jasmonic acid, supported reduced growth of generalist noctuid larvae compared to unmanipulated control plants. Induced responses did not affect the growth of specialist Pieris rapae larvae. In choice and no-choice experiments, induction reduced the feeding by noctuid larvae but did not reduce gross growth efficiency, an indicator...

COSTS OF INDUCED RESPONSES AND TOLERANCE TO HERBIVORY IN MALE AND FEMALE FITNESS COMPONENTS OF WILD RADISH

Theory predicts that plant defensive traits are costly due to trade‐offs between allocation to defense and growth and reproduction. Most previous studies of costs of plant defense focused on female fitness costs of constitutively expressed defenses. Consideration of alternative plant strategies, such as induced defenses and tolerance to herbivory, and multiple types of costs, including allocation to male reproductive function, may increase our ability to detect costs of plant defense against herbivores. In this study we measured male and female reproductive costs associated with induced responses and tolerance to herbivory in annual wild radish plants (Raphanus raphanistrum). We induced resistance in the plants by subjecting them to herbivory by Pieris rapae caterpillars. We also induced resistance in plants without leaf tissue removal using a natural chemical elicitor, jasmonic acid; in addition, we removed leaf tissue without inducing plant responses using manual clipping. Induced responses included increased concentrations of indole glucosinolates, which are putative defense compounds. Induced responses, in the absence of leaf tissue removal, reduced plant fitness when five fitness components were considered together; costs of induction were individually detected for time to first flower and number of pollen grains produced per flower. In this system, induced responses appear to impose a cost, although this cost may not have been detected had we only quantified the traditionally measured fitness components, growth and seed production. In the absence of induced responses, 50% leaf tissue removal, reduced plant fitness in three out of the five fitness components measured. Induced responses to herbivory and leaf tissue removal had additive effects on plant fitness. Although plant sibships varied greatly (49–136%) in their level of tolerance to herbivory, costs of tolerance were not detected, as we did not find a negative association between the ability to compensate for damage and plant fitness in the absence of damage. We suggest that consideration of alternative plant defense strategies and multiple costs will result in a broader understanding of the evolutionary ecology of plant defense.

PLANT GENOTYPE AND ENVIRONMENT INTERACT TO SHAPE A DIVERSE ARTHROPOD COMMUNITY ON EVENING PRIMROSE (OENOTHERA BIENNIS )

Both an individuals genotype and environment govern its phenotype, and this phenotype may have extended consequences for species interactions and communities. We examined the importance of plant genotype and environmental factors operating at large (habitat) and small (microhabitat) spatial scales in affecting a multitrophic arthropod community on plants. We planted 926 plants from 14 genotypes of Oenothera biennis into five natural habitats that represent the range of environments in which this plant locally occurs. Genotypic differences among plants accounted for as much as 41% of the variation in arthropod diversity (Simpsons diversity index) and also affected arthropod evenness, richness, abundance, and biomass on individual plants. However, the effects of particular plant genotypes on the arthropod community varied across habitats (i.e., there were significant plant genotype-by-habitat interactions). Plant genotype explained more variation in the arthropod community than did environmental variation among microhabitats, but less variation than habitats, as predicted by the scale-dependent hypothesis. Herbivores and omnivores were more strongly affected by plant genetic variation than predators, consistent with the notion that phytophagous insects undergo stronger reciprocal interactions with plants than do predators. We detected heritable variation in arthropod community variables and the ability for the herbivore community to select on plant traits, suggesting that evolution in O. biennis can lead to changes in the arthropod community. Genetic variation in plant size, architecture, and reproductive phenology were the plant traits most strongly correlated with arthropod community variables. Our results demonstrate that genotype-by-environment interactions are a major determinant of arthropod community structure.

A Role for Isothiocyanates in Plant Resistance Against the Specialist Herbivore Pieris rapae

We experimentally reanalyzed the classic interaction between Pieris rapae, a specialist lepidopteran herbivore, and isothiocyanates (mustard oils) that are characteristic phytochemicals of the Brassicaceae. Previous investigations have suggested that P. rapae is unaffected by isothiocyanates. Using whole plants, root extracts, and a microencapsulated formulation of allyl isothiocyanate, we now show that isothiocyanates reduce herbivore survival and growth, and increase development time, each in a dose-dependent manner. Neither the substrate allyl glucosinolate, nor myrosinase, the enzyme that results in the breakdown of glucosinolates, negatively affected P. rapae. Thus, we present strong evidence for a role for isothiocyanates in plant resistance against the specialist herbivore P. rapae.