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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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.
Relatedness predicts phenotypic plasticity in plants better than weediness
Cook-Patton, Susan C.; Agrawal, Anurag A. (Evolutionary Ecology, 2011)
Background: Weedy non-native species have long been predicted to be more phenotypically plastic than native species. Question: Are weedy non-native species more plastic than natives? Organisms: Fourteen perennial plant species: Acer platanoides, Acer saccharum, Bromus inermis, Bromus latiglumis, Celastrus orbiculatus, Celastrus scandens, Elymus repens, Elymus trachycaulus, Plantago major, Plantago rugelii, Rosa multiflora, Rosa palustris, Solanum dulcamara, and Solanum carolinense. Field site: Mesic old-field in Dryden, NY (42°27?49?N, 76°26?40?W). Methods: We grew seven pairs of native and non-native plant congeners in the field and tested their responses to reduced competition and the addition of fertilizer. We measured the plasticity of six traits related to growth and leaf palatability (total length, leaf dry mass, maximum relative growth rate, leaf toughness, trichome density, and specific leaf area). Conclusions: Weedy non-native species did not differ consistently from natives in their phenotypic plasticity. Instead, relatedness was a better predictor of plasticity.
Phylogeny of the plant genus Pachypodium (Apocynaceae)
Burge, Dylan O.; Mugford, Kaila; Hastings, Amy P.; Agrawal, Anurag A. (PeerJ, 2013-04-23)
Background. The genus Pachypodium contains 21 species of succulent, generally spinescent shrubs and trees found in southern Africa and Madagascar. Pachypodium has diversified mostly into arid and semi-arid habitats of Madagascar, and has been cited as an example of a plant group that links the highly diverse arid-adapted floras of Africa and Madagascar. However, a lack of knowledge about phylogenetic relationships within the genus has prevented testing of this and other hypotheses about the group. Methodology/Principal Findings. We use DNA sequence data from the nuclear ribosomal ITS and chloroplast trnL-F region for all 21 Pachypodium species to reconstruct evolutionary relationships within the genus. We compare phylogenetic results to previous taxonomic classifications and geography. Results support three infrageneric taxa from the most recent classification of Pachypodium, and suggest that a group of African species (P. namaquanum, P. succulentum and P. bispinosum) may deserve taxonomic recognition as an infrageneric taxon. However, our results do not resolve relationships among major African and Malagasy lineages of the genus. Conclusions/Significance. We present the first molecular phylogenetic analysis of Pachypodium. Our work has revealed five distinct lineages, most of which correspond to groups recognized in past taxonomic classifications. Our work also suggests that there is a complex biogeographic relationship between Pachypodium of Africa and Madagascar.
Plant Genotype Shapes Ant-Aphid Interactions: Implications for Community Structure and Indirect Plant Defense
Mooney, Kailen A.; Agrawal, Anurag A. (University of Chicago Press, 2008-04-15)
Little is known about the mechanisms by which plant genotype shapes arthropod community structure. In a field experiment, we measured the effects of milkweed (Asclepias syriaca) genotype and ants on milkweed arthropods. Populations of the ant?tended aphid Aphis asclepiadis and the untended aphid Myzocallis asclepiadis varied eight? to 18?fold among milkweed genotypes, depending on aphid species and whether ants were present. There was no milkweed effect on predatory arthropods. Ants increased Aphis abundance 59%, decreased Myzocallis abundance 52%, and decreased predator abundance 56%. Milkweed genotype indirectly influenced ants via direct effects on Aphis and Myzocallis abundance. Milkweed genotype also modified ant?aphid interactions, influencing the number of ants attracted per Aphis and Myzocallis. While ant effects on Myzocallis were consistently negative, effects on Aphis ranged from antagonistic to mutualistic among milkweed genotypes. As a consequence of milkweed effects on ant?aphid interactions, ant abundance varied 13?fold among milkweed genotypes, and monarch caterpillar survival was negatively correlated with genetic variation in ant abundance. We speculate that heritable variation in milkweed phloem sap drives these effects on aphids, ants, and caterpillars. In summary, milkweed exerts genetic control over the interactions between aphids and an ant that provides defense against foliage?feeding caterpillars.
Plant chemical defense indirectly mediates aphid performance via interactions with tending ants
Zust, Tobias; Agrawal, Anurag A. (Ecological Society of America, 2017-01-06)
The benefits of mutualistic interactions are often highly context dependent. We studied the interaction between the milkweed aphid Aphis asclepiadis and a tending ant, Formica podzolica. Although this interaction is generally considered beneficial, variation in plant genotype may alter it from mutualistic to antagonistic. Here we link the shift in strength and relative benefit of the ant?aphid interaction to plant genotypic variation in the production of cardenolides, a class of toxic defensive chemicals. In a field experiment with highly variable genotypes of the common milkweed (Asclepias syriaca), we show that plant cardenolides, especially polar forms, are ingested by aphids and excreted in honeydew proportionally to plant concentrations without directly affecting aphid performance. Ants consume honeydew, and aphids that excreted high amounts of cardenolides received fewer ant visits, which in turn reduced aphid survival. On at least some plant genotypes, aphid numbers per plant were reduced in the presence of ants to levels lower than in corresponding ant?exclusion treatments, suggesting antagonistic ant behavior. Although cardenolides appear ineffective as direct plant defenses against aphids, the multi?trophic context reveals an ant?mediated negative indirect effect on aphid performance and population dynamics.
Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis)
Johnson, Mark T.; Agrawal, Anurag A. (Ecological Society of America, 2005-04-01)
Both an individual's 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 (Simpson's 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.
Phylogenetic escalation and decline of plant defense strategies
Agrawal, Anurag A.; Fishbein, Mark (National Academy of Sciences, 2008-07-22)
As the basal resource in most food webs, plants have evolved myriad strategies to battle consumption by herbivores. Over the past 50 years, plant defense theories have been formulated to explain the remarkable variation in abundance, distribution, and diversity of secondary chemistry and other defensive traits. For example, classic theories of enemy-driven evolutionary dynamics have hypothesized that defensive traits escalate through the diversification process. Despite the fact that macroevolutionary patterns are an explicit part of defense theories, phylogenetic analyses have not been previously attempted to disentangle specific predictions concerning (i) investment in resistance traits, (ii) recovery after damage, and (iii) plant growth rate. We constructed a molecular phylogeny of 38 species of milkweed and tested four major predictions of defense theory using maximum-likelihood methods. We did not find support for the growth-rate hypothesis. Our key finding was a pattern of phyletic decline in the three most potent resistance traits (cardenolides, latex, and trichomes) and an escalation of regrowth ability. Our neontological approach complements more common paleontological approaches to discover directional trends in the evolution of life and points to the importance of natural enemies in the macroevolution of species. The finding of macroevolutionary escalating regowth ability and declining resistance provides a window into the ongoing coevolutionary dynamics between plants and herbivores and suggests a revision of classic plant defense theory. Where plants are primarily consumed by specialist herbivores, regrowth (or tolerance) may be favored over resistance traits during the diversification process
Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores
Agrawal, Anurag A. (Evolutionary Ecology, 2005)
Hypothesis: Genetic variation in plant defence structures a community of herbivores and ultimately mediates co-evolution. Organisms: Common milkweed (Asclepias syriaca) and five natural insect herbivores (seed bug, leaf mining fly, monarch caterpillar and two beetles). Methods: Quantitative genetic field experiment over 2 years, genetic selection analyses, and measurement of five defensive traits (cardenolides, latex, trichomes, leaf toughness and nitrogen content). Results: All plant traits were genetically variable; directional selection favoured resistance to herbivory, latex production and the nitrogen content of leaves. Trichomes and latex were each negatively genetically correlated with abundances of herbivores, but not with herbivore damage; cardenolides and induced plant resistance were negatively genetically correlated with growth of monarchs. Conclusion: Selection for plant defence was influenced by: (1) genetic correlations in plant susceptibility to multiple herbivores; (2) resistance traits affecting some, but not all, aspects of the insect community; and (3) early season herbivory inducing changes in milkweed influencing later season herbivores.
Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae)
Weber, Marjorie G.; Clement, Wendy L.; Donoghue, Michael J.; Agrawal, Anurag A. (University of Chicago Press, 2012-10)
Plant traits that mediate mutualistic interactions are widespread, yet few studies have linked their macroevolutionary patterns with the ecological interactions they mediate. Here we merged phylogenetic and experimental approaches to investigate the evolution of two common mutualistic plant traits, extrafloral nectaries (EFNs) and leaf domatia. By using the flowering plant clade Viburnum, we tested whether macroevolutionary patterns support adaptive hypotheses and conducted field surveys and manipulative experiments to examine whether ecological interactions are concordant with evolutionary predictions. Phylogenetic reconstructions suggested that EFN-bearing species are monophyletic, whereas the evolution of domatia correlated with leaf production strategy (deciduous or evergreen) and climate. Domatia were also more common in the EFN clade, suggesting that the two traits may jointly mediate ecological interactions. This result was further investigated in a common-garden survey, where plants with domatia and EFNs on the leaf blade had more mutualistic mites than plants with other trait combinations, and in manipulative field experiments, where the traits additively increased mutualist abundance. Taken together, our results suggest that mutualistic traits in Viburnum are not ecologically independent, as they work in concert to attract and retain mutualists, and their long-term evolution may be influenced by complex interactions among multiple traits, mutualists, and geography.
Microsatellites for Oenothera gayleana and O. hartwegii subsp. filifolia (Onagraceae), and their utility in section Calylophus
Lewis, E. M.; Fant, J. B.; Moore, M. J.; Hastings, Amy P.; Larson, E. L.; Agrawal, Anurag A.; Skogen, K. A. (Botanical Society of America, 2016-02-09)
Premise of the study: Eleven nuclear and four plastid microsatellite markers were screened for two gypsum endemic species, Oenothera gayleana and O. hartwegii subsp. filifolia, and tested for cross?amplification in the remaining 11 taxa within Oenothera sect. Calylophus (Onagraceae). Methods and Results: Microsatellite markers were tested in two to three populations spanning the ranges of both O. gayleana and O. hartwegii subsp. filifolia. The nuclear microsatellite loci consisted of both di? and trinucleotide repeats with one to 17 alleles per population. Several loci showed significant deviation from Hardy–Weinberg equilibrium, which may be evidence of chromosomal rings. The plastid microsatellite markers identified one to seven haplotypes per population. The transferability of these markers was confirmed in all 11 taxa within Oenothera sect. Calylophus. Conclusions: The microsatellite loci characterized here are the first developed and tested in Oenothera sect. Calylophus. These markers will be used to assess whether pollinator foraging distance influences population genetic parameters in predictable ways.
Love thy neighbor? Reciprocal impacts between plant community structure and insect herbivory in co-occurring Asteraceae
Stastny, Michael; Agrawal, Anurag A. (Ecological Society of America, 2014-10-01)
Patterns of herbivory may vary with fine?scale plant community structure: the degree of damage plants experience may depend on their neighbors (i.e., associational resistance or susceptibility). Differential herbivory, in turn, may facilitate a shift in plant community structure. We investigated these reciprocal effects of plant community structure and insect herbivory in a field mesocosm experiment with closely related, native Asteraceae that co?occur in early?successional habitats (old fields). After one year of establishment, we excluded or augmented insect herbivores for two years in equal?density communities of three types: goldenrod?dominated (Solidago spp.) or aster?dominated (Symphyotrichum spp.) congeneric communities and mixtures of the two genera. In manipulated outbreaks, overall and species?specific patterns of herbivory by the main herbivore, the leaf beetle Trirhabda virgata, varied dramatically with community composition. In both years, the preferred goldenrods suffered 25?70% higher defoliation in mixtures with the less?preferred asters (i.e., associational susceptibility), compared to when growing with congeners; in contrast, asters experienced lower damage in mixtures (i.e., associational resistance). Insect herbivory consistently reduced overall plant productivity, and promoted colonization by other old?field species. Importantly, herbivory also initiated a shift in the structure of the plant communities, and this effect depended on the starting community composition, implying potential reciprocal effects. For instance, only in mixtures did elevated herbivory reduce the proportional abundance of the preferred host, and the old?field dominant, Solidago altissima. Our findings underscore the importance of plant community composition for variation in and impacts of herbivory and suggest the possibility of feedbacks between herbivory and local community structure as one of the mechanisms contributing to the maintenance of vegetation heterogeneity.

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