EEB Papers - Anurag Agrawal

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https://hdl.handle.net/1813/66724

Professor Agrawal is the James A. Perkins Professor of Environmental Studies at Cornell University. His research program addresses questions in the ecology and evolution of interactions between plants and animals. His focus is on the generally antagonistic interactions between plants and insect herbivores and ultimately seeks to understand the complexity of community-wide interactions. What ecological factors allow the coexistence of similar species? What evolutionary factors led to the diversification of species?

His approach to science in general involves 1) rigorous, manipulative field experiments to test for the importance of conceptually or theoretically developed interactions, 2) the search for novel interactions which may be pervasive in nature but have escaped our attention, and 3) a keen interest in teaching and mentoring students at all levels of education.

A more complete and current listing of Prof. Agrawal's work and scholarly output can be found via his EEB Department web page, his Phytophagy Lab web site, or ORCID ID: http://orcid.org/0000-0003-0095-1220

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Now showing 1 - 10 of 49

Transgenerational Consequences of Plant Responses to Herbivory: An Adaptive Maternal Effect
Agrawal, Anurag A. (University of Chicago Press, 2000-12-21)
Herbivory has many effects on plants, ranging from shifts in primary processes such as photosynthesis, growth, and phenology to effects on defense against subsequent herbivores and other species interactions. In this study, I investigated the effects of herbivory on seed and seedling characteristics of several families of wild radish (Raphanus raphanistrum) to test the hypothesis that herbivory may affect the quality of offspring and the resistance of offspring to plant parasites. Transgenerational effects of herbivory may represent adaptive maternal effects or factors that constrain or amplify natural selection on progeny. Caterpillar (Pieris rapae) herbivory to greenhouse?grown plants caused plants in some families to produce smaller seeds and those in other families to produce larger seeds compared with undamaged controls. Seed mass was positively associated with probability of emergence in the field. The number of setose trichomes, a putative plant defense, was higher in the progeny of damaged plants in some families and lower in the progeny of damaged plants in other families. In a field experiment, plant families varied in their resistance to several herbivores and pathogens as well as in growth rate and time to flowering. Seeds from damaged parent plants were more likely to become infested with a plant virus. Although herbivory on maternal plants did not directly affect interactions of offspring with other plant parasites, seed mass influenced plant resistance to several attackers. Thus, herbivory affected seed characters, which mediated interactions between plants and their parasites. Finally, irrespective of seed mass, herbivory on maternal plants influenced components of progeny fitness, which was dependent on plant family. Natural selection may act on plant responses to herbivory that affect seedling?parasite interactions and, ultimately, fitness.
Toward a Predictive Framework for Convergent Evolution: Integrating Natural History, Genetic Mechanisms, and Consequences for the Diversity of Life
Agrawal, Anurag A. (University of Chicago Press, 2017-08)
A charm of biology as a scientific discipline is the diversity of life. Although this diversity can make laws of biology challenging to discover, several repeated patterns and general principles govern evolutionary diversification. Convergent evolution, the independent evolution of similar phenotypes, has been at the heart of one approach to understand generality in the evolutionary process. Yet understanding when and why organismal traits and strategies repeatedly evolve has been a central challenge. These issues were the focus of the American Society of Naturalists Vice Presidential Symposium in 2016 and are the subject of this collection of articles. Although naturalists have long made inferences about convergent evolution and its importance, there has been confusion in the interpretation of the pattern of convergence. Does convergence primarily indicate adaptation or constraint? How often should convergence be expected? Are there general principles that would allow us to predict where and when and by what mechanisms convergent evolution should occur? What role does natural history play in advancing our understanding of general evolutionary principles? In this introductory article, I address these questions, review several generalizations about convergent evolution that have emerged over the past 15 years, and present a framework for advancing the study and interpretation of convergence. Perhaps the most important emerging conclusion is that the genetic mechanisms of convergent evolution are phylogenetically conserved; that is, more closely related species tend to share the same genetic basis of traits, even when independently evolved. Finally, I highlight how the articles in this special issue further develop concepts, methodologies, and case studies at the frontier of our understanding of the causes and consequences of convergent evolution.
The raison d'etre of chemical ecology
Raguso, Robert A.; Agrawal, Anurag A.; Douglas, Angela E.; Jander, Georg; Kessler, Andre; Poveda, Katja; Thaler, Jennifer S. (Ecological Society of America, 2015-03-01)
Chemical ecology is a mechanistic approach to understanding the causes and consequences of species interactions, distribution, abundance, and diversity. The promise of chemical ecology stems from its potential to provide causal mechanisms that further our understanding of ecological interactions and allow us to more effectively manipulate managed systems. Founded on the notion that all organisms use endogenous hormones and chemical compounds that mediate interactions, chemical ecology has flourished over the past 50 years since its origin. In this essay we highlight the breadth of chemical ecology, from its historical focus on pheromonal communication, plant–insect interactions, and coevolution to frontier themes including community and ecosystem effects of chemically mediated species interactions. Emerging approaches including the ?omics, phylogenetic ecology, the form and function of microbiomes, and network analysis, as well as emerging challenges (e.g., sustainable agriculture and public health) are guiding current growth of this field. Nonetheless, the directions and approaches we advocate for the future are grounded in classic ecological theories and hypotheses that continue to motivate our broader discipline.
The importance of plant genotype and contemporary evolution for terrestrial ecosystem processes
Fitzpatrick, C. R.; Agrawal, Anurag A.; Basiliko, N.; Hastings, Amy P.; Isaac, M. E.; Preston, M.; Johnson, Mark T. (Ecological Society of America, 2015-10-01)
Plant genetic variation and evolutionary dynamics are predicted to impact ecosystem processes but these effects are poorly understood. Here we test the hypothesis that plant genotype and contemporary evolution influence the flux of energy and nutrients through soil, which then feedback to affect seedling performance in subsequent generations. We conducted a multiyear field evolution experiment using the native biennial plant Oenothera biennis. This experiment was coupled with experimental assays to address our hypothesis and quantify the relative importance of evolutionary and ecological factors on multiple ecosystem processes. Plant genotype, contemporary evolution, spatial variation, and herbivory affected ecosystem processes (e.g., leaf decay, soil respiration, seedling performance, N cycling), but their relative importance varied between specific ecosystem variables. Insect herbivory and evolution also contributed to a feedback that affected seedling biomass of O. biennis in the next generation. Our results show that heritable variation among plant genotypes can be an important factor affecting local ecosystem processes, and while effects of contemporary evolution were detectable and sometimes strong, they were often contingent on other ecological factors.
The Benefits of Induced Defenses Against Herbivores
Karban, Richard; Agrawal, Anurag A.; Mangel, Marc (Ecological Society of America, 1997-07-01)
Previous explanations for the evolution of induced resistance of plants to herbivory emphasized arguments based on saving costs when allocations to defense were not needed; these models met with limited empirical support. We offer a novel explanation based on induced resistance providing increased variability in defense. As long as maximal levels of defense are constrained, variability will increase the effectiveness of a given level of investment in defense. We show that variability can decrease herbivore performance if herbivore performance is a concave function of the level of resistance. In particular, if herbivores can choose among different plants and plant tissues, then variability created by induced resistance may benefit plants under attack and hence may be favored by selection. The key assumptions of this model are broadly supported by empirical data from many plant–herbivore systems.
Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)
Agrawal, Anurag A.; Patrick, Eamonn T.; Hastings, Amy P. (Ecological Society of America, 2014-10-21)
The coexpression of plant resistance traits suggests the hypothesis that they may have complementary functions in defense against herbivory. To address the extent to which defensive traits are necessarily coupled in plants grown under various conditions, we focused on latex and cardenolides, two potent defenses of milkweeds. We measured defenses across ontogenetic stages, different biotic and abiotic environments, and across genetic families of the common milkweed Asclepias syriaca. We first addressed the extent to which foliar cardenolides are derived from latex because latex actively flows through canals in leaves. We rinsed latex out of shredded leaves, which had no impact on foliar cardenolides, suggesting cardenolides are allocated to leaves independently of latex. Accordingly, there is potential for independent expression of the two traits. We next followed a cohort of plants from germination over three years; expression of both latex exudation and cardenolides increased annually, with the exception of a second year dip in cardenolides. Damage by monarch caterpillars induced ?50% increases of both latex and cardenolides, with the former occurring rapidly within a day and the latter taking five days of herbivory; these responses were preceded by an earlier peak of the signaling hormones jasmonic acid and abscisic acid. Endogenous jasmonic acid showed an instantaneous positive correlation with latex exudation and foliar cardenolides. Under drought stress, latex and cardenolide expression were reversed, with water stress suppressing latex exudation, but nearly doubling cardenolide concentrations. These drought effects were not driven by phytohormones in the expected manner, as jasmonic acid was unaffected, salicylic acid was strongly suppressed, and abscisic acid tripled in response to drought. Finally, a meta?analysis of four previously published field studies representing 85 genetic families of A. syriaca revealed no evidence for a genetic correlation between latex exudation and foliar cardenolide concentrations. The same lack of a correlation was observed across 22 populations of A. syriaca when grown in a common environment. Thus, the two most important defensive traits of milkweeds, although often coexpressed, can become uncoupled during some ontogenetic stages, under some biotic and abiotic conditions, and there is no evidence that they evolve together.
Salicylate-mediated interactions between pathogens and herbivores
Thaler, Jennifer S.; Agrawal, Anurag A.; Halitschke, Rayko (Ecological Society of America, 2010-01-01)
Plants employ hormone?mediated signaling pathways to defend against pathogens and insects. We tested predictions about the relative effect of jasmonate and salicylate pathways and how they mediate interactions between pathogens and herbivores. We employed two pathogens of tomato, Pseudomonas syringae (Pst) and tobacco mosaic virus (TMV), that are known to elicit distinct components of the two pathways, and we address the consequences of their induction for resistance in wild?type and salicylate?deficient transgenic plants in field experiments. We report that Pst infection induced jasmonic acid and proteinase inhibitors (PIs), and reduced the growth of Spodoptera exigua caterpillars on wild?type and salicylate?deficient plants. Pst and TMV both induced salicylic acid in wild?type but not salicylate?deficient plants. Although TMV did not affect jasmonic acid or PIs, infection increased caterpillar growth on wild?type plants, but not on salicylate?deficient plants. Aphid population growth was higher on salicylate?deficient compared to wild?type plants, and lower on salicylate?induced plants compared to controls. Natural aphid colonization was reduced on TMV?infected wild types, but not on salicylate?deficient plants. In sum, jasmonate?mediated resistance is induced by some pathogens, independent of salicylate, and salicylate?mediated induction by other pathogens results in induced susceptibility to a chewer and resistance to an aphid. We conclude with a predictive model for the expression of defense pathways and their consequences.
Spillover of a biological control agent (Chrysolina quadrigemina) onto native St. Johnswort (Hypericum punctatum)
Tingle, Jessica L.; Cook-Patton, Susan C.; Agrawal, Anurag A. (PeerJ, 2016-03-31)
Biological control agents may have unintended effects on native biota, particularly species that are closely related to the target invader. Here, we explored how Chrysolina quadrigemina, a beetle introduced to control the invasive weed Hypericum perforatum, impacts native H. punctatum in Tompkins County, New York, USA. Using a suite of complementary field surveys and experimental manipulations, we examined beetle preference for native and exotic Hypericum species and whether beetle herbivory influences the spatial distribution of H. punctatum. We found that the introduced beetle readily consumes native H. punctatum in addition to its intended target, and that H. punctatum at our field sites generally occurs along forest edges despite higher performance of experimental plants in more open habitats. However, we found no evidence that the beetle limits H. punctatum to forest edge habitats.
Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation
Agrawal, Anurag A. (Ecological Society of America, 2004-08-01)
Beetles in the genus Tetraopes share a long evolutionary history with milkweeds (Asclepias spp.), feeding on roots as larvae and leaves as adults. Despite their extreme specialization on milkweed, Tetraopes require drying grass stems as oviposition sites, even though they do not consume grass. The natural history of the interaction suggests that herbivory may be likely only when milkweeds are in close proximity to grasses. Theory also predicts that two stresses on plants, competition and herbivory, may have non?additive negative impacts on correlates of fitness. In field experiments conducted over two years, I followed the consequences of grass competition and beetle attack for herbivory, growth, and reproduction of milkweed, and reciprocal effects of milkweed on grass in common gardens. To assess the effect of milkweed traits on beetles, I conducted a quantitative genetic experiment using full?sibling families of milkweed and measured the effects of putative resistance traits on the abundance of Tetraopes adults. Milkweeds growing next to grass were initially unaffected in growth but suffered 10% greater leaf herbivory by adult Tetraopes than did milkweeds growing alone. This effect was caused by direct attraction of beetles to grass, not by a competitive modification of milkweed's phenotype. In late summer of the first growing season, when Tetraopes naturally oviposits, I experimentally added larvae to milkweed roots with and without grass competition. Within a month, I detected an interaction between competition and herbivory: neither had an individual impact, but jointly they reduced milkweed growth. In spring of the second growing season, when Tetraopes had completed development, I again found strong evidence for a non?additive effect of competition and herbivory together, severely reducing plant growth compared to their individual effects. Root herbivory induced a plant response that reduced the abundance of leaf?mining flies by 40%, but only for milkweeds with grass competition. Neither competition nor herbivory affected the production of defensive latex, cardenolides, or carbon, but they interacted to affect leaf nitrogen content. Thus, although trait?mediated indirect interactions were implicated in the effect of competition and root herbivory on leaf miner abundance, I did not uncover the mechanism. In the final harvest, beetle herbivory reduced reproductive characters (fruit production, fruit mass, aboveground biomass) by 20– 30%, whereas competition had negligible effects. The net interaction effect for grass was competitive, with a 23% reduction in grass biomass caused by milkweed in the absence of herbivory. However, the presence of beetle herbivory on milkweed roots completely alleviated the competitive effect of milkweed on grass. Thus, the associational effect of grass on milkweed resulted in milkweed suffering the non?additive effects of competition and herbivory, whereas grass enjoyed competitive release by facilitating its neighbor's herbivore. Many traits of milkweed (e.g., growth, reproduction, and several resistance traits) showed variation among 23 full?sibling families, indicating that competitive ability and resistance may be subject to natural selection. A multiple regression analysis on family means revealed that leaf trichome density and nitrogen content were negatively genetically correlated with abundance of Tetraopes adults, but probability of flowering and plant height were positively associated. Leaf miners were most strongly negatively affected by latex and trichomes. Thus, complex interactions among competition, root herbivory, and plant genetic variation affect the herbivore and plant community and may result in diffuse coevolution between milkweed and its herbivores. I present a general model that predicts the conditions in which plant–plant interactions result in net competition or facilitation.
Relative Selectivity of Plant Cardenolides for Na+/K+-ATPases From the Monarch Butterfly and Non-resistant Insects
Petschenka, G.; Fei, C. S.; Araya, J. J.; Schröder, S.; Timmermann, B. N.; Agrawal, Anurag A. (Frontiers Media, 2018-09-28)
A major prediction of coevolutionary theory is that plants may target particular herbivores with secondary compounds that are selectively defensive. The highly specialized monarch butterfly (Danaus plexippus) copes well with cardiac glycosides (inhibitors of animal Na+/K+-ATPases) from its milkweed host plants, but selective inhibition of its Na+/K+-ATPase by different compounds has not been previously tested. We applied 17 cardiac glycosides to the D. plexippus-Na+/K+-ATPase and to the more susceptible Na+/K+-ATPases of two non-adapted insects (Euploea core and Schistocerca gregaria). Structural features (e.g., sugar residues) predicted in vitro inhibitory activity and comparison of insect Na+/K+-ATPases revealed that the monarch has evolved a highly resistant enzyme overall. Nonetheless, we found evidence for relative selectivity of individual cardiac glycosides reaching from 4- to 94-fold differences of inhibition between non-adapted Na+/K+-ATPase and D. plexippus-Na+/K+-ATPase. This toxin receptor specificity suggests a mechanism how plants could target herbivores selectively and thus provides a strong basis for pairwise coevolutionary interactions between plants and herbivorous insects.

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