Anurag A Agrawal

Cornell University | CU · Department of Ecology and Evolutionary Biology

Mutualisms are mediated by adaptive traits of interacting organisms and play a central role in the ecology and evolution of species. Thousands of plant species possess tiny structures called “domatia” that house mites which protect plants from pests, yet these traits remain woefully understudied. Here, we release a worldwide database of species wit...

Multiple hypotheses have been put forth to understand why defense chemistry in individual plants is so diverse. A major challenge has been teasing apart the importance of concentration versus composition of defense compounds, and resolving the mechanisms of diversity effects that determine plant resistance against herbivores. Accordingly, we first...

Over the last decade, a large effort has been made to understand how extreme climate events disrupt species interactions. Yet, it is unclear how these events affect plants and herbivores directly, via metabolic changes, and indirectly, via their subsequent altered interaction. We exposed common milkweed ( Asclepias syriaca ) and monarch caterpillar...

Repeatable macroevolutionary patterns provide hope for rules in biology, especially when we can decipher the underlying mechanisms. Here we synthesize natural history, genetic adaptations, and toxin sequestration in herbivorous insects that specialize on plants with cardiac glycoside defenses. Work on the monarch butterfly provided a model for evol...

Despite long-standing theory for classifying plant ecological strategies, limited data directly links organismal traits to whole-plant growth. We compared trait-growth relationships based on three prominent theories: growth analysis, Grime’s CSR triangle, and the leaf economics spectrum (LES). Under these schemes, growth is hypothesized to be predi...

The chemical arms race between plants and insects is foundational to the generation and maintenance of biological diversity. We asked how the evolution of a novel defensive compound in an already well‐defended plant lineage impacts interactions with diverse herbivores. Erysimum cheiranthoides (Brassicaceae), which produces both ancestral glucosinol...

Herbivores that sequester toxins are thought to have cracked the code of plant defences. Nonetheless, coevolutionary theory predicts that plants should evolve toxic variants that also negatively impact specialists. We propose and test the selective sequestration hypothesis, that specialists preferentially sequester compounds that are less toxic to...

Plants have evolved a diverse arsenal of defensive secondary metabolites in their evolutionary arms race with insect herbivores. In addition to the bottom-up forces created by plant chemicals, herbivores face top-down pressure from natural enemies, such as predators, parasitoids and parasites. This has led to the evolution of specialist herbivores...

The chemical arms race between plants and insects is foundational to the generation and maintenance of biological diversity. We asked how the evolution of a novel defensive compound in an already well-defended plant lineage impacts interactions with diverse herbivores. Erysimum cheiranthoides (Brassicaceae), which produces both ancestral glucosinol...

A major predicted constraint on the evolution of anti-herbivore defense in plants is the non-independent expression of traits mediating resistance. Since herbivore attack can be highly variable across plant tissues, we hypothesized that correlations in toxin expression within and between plant tissues may limit population differentiation and, thus,...

Plant toxicity shapes the dietary choices of herbivores. Especially when herbivores sequester plant toxins, they may experience a trade-off between gaining protection from natural enemies and avoiding toxicity. The availability of toxins for sequestration may additionally trade off with the nutritional quality of a potential food source for sequest...

In intimate ecological interactions, the interdependency of species may result in correlated demographic histories. For species of conservation concern, understanding the long-term dynamics of such interactions may shed light on the drivers of population decline. Here, we address the demographic history of the monarch butterfly, Danaus plexippus, a...

In coevolution between plants and insects, reciprocal selection often leads to phenotype matching between chemical defense and herbivore offense. Nonetheless, it is not well understood whether distinct plant parts are differentially defended and how herbivores adapted to those parts cope with tissue-specific defense. Milkweed plants produce a diver...

Despite long‐standing theory for classifying plant ecological strategies, limited data directly link organismal traits to whole‐plant growth rates (GRs). We compared trait‐growth relationships based on three prominent theories: growth analysis, Grime's competitive–stress tolerant–ruderal (CSR) triangle, and the leaf economics spectrum (LES). Under...

Plant secondary metabolites that defend leaves from herbivores also occur in floral nectar. While specialist herbivores often have adaptations providing resistance to these compounds in leaves, many social insect pollinators are generalists, and therefore are not expected to be as resistant to such compounds. The milkweeds, Asclepias spp., contain...

The response of herbivorous insects to plant drought stress can range from positive to negative, and it has been challenging to understand the causes of this variation. We tested whether plant trait values associated with aridity gradients might underlie this variation and how such effects vary between two insect feeding guilds. Here, we propose th...

As major consumers of plants, insect herbivores have strong potential to influence long‐term patterns of plant abundance and community structure. Nonetheless, remarkably few manipulative experiments exclude insects for three or more years. Thus, how often, and under what conditions insects have enduring impacts remains unclear. Here we summarize th...

The biosynthesis of cardiac glycosides, broadly classified as cardenolides and bufadienolides, has evolved repeatedly among flowering plants. Individual species can produce dozens or even hundreds of structurally distinct cardiac glycosides. Although all cardiac glycosides exhibit biological activity by inhibiting the function of the essential Na⁺/...

Spatiotemporal variation in herbivory is a major driver of intraspecific variation in plant defense. Comparatively little is known, however, about how changes in herbivory regime affect the balance of constitutive and induced resistance, which are often considered alternative defensive strategies. Here, we investigated how nearly a decade of insect...

Environmental clines in organismal defensive traits are usually attributed to stronger selection by enemies at lower latitudes or near the host’s range center. Nonetheless, little functional evidence has supported this hypothesis, especially for coevolving plants and herbivores. We quantified cardenolide toxins in seeds of 24 populations of common...

In intimate ecological interactions, the interdependency of species may result in correlated demographic histories. For species of conservation concern, understanding the long-term dynamics of such interactions may shed light on the drivers of population decline. Here we address the demographic history of the monarch butterfly, Danaus plexippus , a...

Co-occurring herbivorous pests may have shared or divergent responses to plant- and insect- derived cues, creating challenges for effective pest management in agroecosystems. We examined how behaviors of two endemic specialist herbivores of Cucurbitaceae crops, squash bugs (Anasa tristis, Hemiptera: Coreidae) and striped cucumber beetles (Acalymma...

Premise: Mismatches between light conditions and light-capture strategy can reduce plant performance and prevent colonization of novel habitats. Although light-capture strategies tend to be highly conserved among closely related species, evolutionary transitions from shaded to unshaded habitats (and vice versa) occur in numerous plant lineages. M...

Significance Studies that experimentally examine evolution have provided critical insight in biology. Indeed, rigorous and replicated laboratory experiments have revealed parallel evolution and have proved essential to understanding evolutionary processes. Nonetheless, a typical limitation of such work is the lack of ecological realism. We report o...

The study of reciprocal adaptation in interacting species has been an active and inspiring area of evolutionary research for nearly 60 years. Perhaps owing to its great natural history and potential consequences spanning population divergence to species diversification, coevolution continues to capture the imagination of biologists. Here we trace d...

Despite long-standing theory for classifying plant ecological strategies, limited data directly links organismal traits to whole-plant growth. We compared trait-growth relationships based on three prominent theories: growth analysis, Grime’s CSR triangle, and the leaf economics spectrum (LES). Under these schemes, growth is hypothesized to be predi...

Significance Interactions between plants and herbivores constitute a major pathway of energy transfer up the food chain. As a consequence, evolution by natural selection has honed the chemically mediated antagonistic interactions between these groups. Monarch butterflies and milkweeds serve as royal representatives in deciphering such coevolution,...

Despite long-standing interest in local adaptation of plants to their biotic and abiotic environment, existing theory, and many case studies, little work to date has addressed within-species evolution of concerted strategies and how these might contrast with patterns across species. Here we consider the interactions between pollinators, herbivores,...

At small spatial scales, attraction or deterrence of herbivores by plant neighbors can alter the susceptibility of plants to damage (i.e., associational effects). Given the patchy nature of plants and insect herbivory, we hypothesized that induced resistance may play an important role in mitigating such spatial variability. To test this notion, we...

Erysimum cheiranthoides L (Brassicaceae; wormseed wallflower) accumulates not only glucosinolates, which are characteristic of the Brassicaceae, but also abundant and diverse cardenolides. These steroid toxins, primarily glycosylated forms of digitoxigenin, cannogenol, and strophanthidin, inhibit the function of essential Na⁺/K⁺-ATPases in animal c...

Background Oviposition decisions are critical to the fitness of herbivorous insects and are often impacted by the availability and condition of host plants. Monarch butterflies ( Danaus plexippus ) rely on milkweeds ( Asclepias spp.) for egg-laying and as food for larvae. Previous work has shown that monarchs prefer to oviposit on recently regrown...

Despite the ubiquity of parental effects and their potential effect on evolutionary dynamics, their contribution to the evolution of predator-prey interactions remains poorly understood. Using quantitative genetics, here we demonstrate that parental effects substantially contribute to the evolutionary potential of larval antipredator responses in a...

Crop domestication and improvement often concurrently affect plant resistance to pests and production of secondary metabolites, creating challenges for isolating the ecological implications of selection for specific metabolites. Cucurbitacins are bitter triterpenoids with extreme phenotypic differences between Cucurbitaceae lineages, yet we lack in...

While morphological differences such as tongue length are often featured as drivers of pollinator floral preferences, differences in chemical detection and tolerance to secondary compounds may also play a role. We sought to better understand the role of secondary compounds in floral preference by examining visitation of milkweed flowers, which can...

Successful management of insect crop pests requires an understanding of the cues and spatial scales at which they function to affect rates of attack of preferred and non‐preferred host plants. A long‐standing conceptual framework in insect–plant ecology posits that there is hierarchical structure spanning host location, acceptance and attack that c...

1. An herbivore's life‐history strategy, including optimization of resource use, is constrained by its evolutionary history and ecological factors varying across the landscape. 2. We asked if related and co‐distributed herbivore species maintain consistency of host preference and oviposition behaviours along the species' range. We surveyed two puta...

A meandering investigation hints at how much is left to learn about these charismatic insects

Many plants produce structurally related defensive metabolites with the same target sites in insect herbivores. Two possible drivers of this chemical diversity are: (i) interacting effects of structurally related compounds increase resistance against individual herbivores, and (ii) variants of the same chemical structures differentially affect dive...

Milkweeds have ecological significance for insect herbivores that rely on them as hosts for either part of or the entirety of their life cycles. Interesting interactions, some of which are not completely understood, have evolved over time. To develop these species as models to elucidate the interplay with insect herbivores, we established Agrobacte...

Biodiversity is defined by trait differences between organisms, and biologists have long sought to predict associations among ecologically important traits. Why do some traits trade off but others are coexpressed? Why might some trait associations hold across levels of organization, from individuals and genotypes to populations and species, whereas...

Latex occurs in 10% of plant families, has evolved independently many times, and is the most effective defense of milkweeds against its chewing herbivores. Here we report on new experiments on the heritability and inducibility of latex in several milkweed species. In addition, we review what is known about the genetic and environmental determinants...

Phenotypic plasticity is the primary mechanism of organismal resilience to abiotic and biotic stress, and genetic differentiation in plasticity can evolve if stresses differ among populations. Inducible defense is a common form of adaptive phenotypic plasticity and long‐standing theory predicts that its evolution is shaped by costs of the defensive...

Identifying the genetic mechanisms of adaptation requires the elucidation of links between the evolution of DNA sequence, phenotype, and fitness¹. Convergent evolution can be used as a guide to identify candidate mutations that underlie adaptive traits2,3,4, and new genome editing technology is facilitating functional validation of these mutations...

Despite the ubiquity of parental effects and their potential impact on evolutionary dynamics, their contribution to the evolution of ecologically relevant adaptations remains poorly understood. Using quantitative genetics, here we demonstrate that parental effects contribute substantially to the evolutionary potential of larval antipredator respons...

Inducible defense is a common form of phenotypic plasticity, and inducibility (change in defense after herbivore attack) has long been predicted to trade off with constitutive (or baseline) defense to manage resource allocation. Although such trade‐offs likely constrain evolution within species, the extent to which they influence divergence among s...

The fundamental tradeoff between carbon gain and water loss has long been predicted as an evolutionary driver of plant strategies across environments. Nonetheless, challenges in measuring carbon gain and water loss in ways that integrate over leaf lifetime have limited our understanding of the variation in and mechanistic bases of this tradeoff. Fu...

More than five decades ago, Ehrlich and Raven proposed a revolutionary idea–that the evolution of novel plant defense could spur adaptive radiation in plants. Despite motivating much work on plant–herbivore coevolution and defense theory, Ehrlich and Raven never proposed a mechanism for their "escape and radiate" model. Recent intriguing mechanisms...

Although crop wild ancestors are often reservoirs of resistance traits lost during domestication, examining diverse cultivated germplasm may also reveal novel resistance traits due to distinct breeding histories. Using ten cultivars from two independent domestication events of Cucurbita pepo (ssp. pepo and texana), we identified divergences in cons...

Monarch butterflies, Danaus plexippus, migrate long distances over which they encounter host plants that vary broadly in toxic cardenolides. Remarkably little is understood about the mechanisms of sequestration in Lepidoptera that lay eggs on host plants ranging in such toxins. Using closely-related milkweed host plants that differ more than ten-fo...

The connection between adult preferences and offspring performance is long‐standing issue in understanding the evolutionary and ecological forces that dictate host associations and specialization in herbivorous insects. Indeed, decisions made by females about where to lay their eggs have direct consequences for fitness and are influenced by interac...

Migratory animals are imperiled worldwide. Because they cross geopolitical boundaries and rely on diverse habitats and resources, conserving migratory populations presents many challenges. We assess conservation policy for migratory animals and identify multiple scales at which analysis and action are needed: 1) local- and landscape-scale conservat...

Cardenolides are classically studied steroidal defenses in chemical ecology and plant-herbivore coevolution. Although milkweed plants (Asclepias spp.) produce up to 200 structurally different cardenolides, all compounds seemingly share the same well-characterized mode of action, inhibition of the ubiquitous Na⁺/K⁺ ATPase in animal cells. Over their...

A central tenet of plant defense theory is that adaptation to the abiotic environment sets the template for defense strategies, imposing a trade-off between plant growth and defense. Yet this trade-off, commonly found among species occupying divergent resource environments, may not occur across populations of single species. We hypothesized that mo...

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...

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...

Migratory failure may contribute to the dwindling of this iconic butterfly's population

Specialized insect herbivores commonly co‐opt plant defences for protection against predators, but the costs, benefits and mechanisms of sequestration are poorly understood. We quantified sequestration of toxic cardenolides by the specialist aphid Aphis nerii when reared on four closely related milkweed ( Asclepias ) species with >20‐fold variation...

To address the role of insect herbivores in adaptation of plant populations and the persistence of selection through succession, we manipulated herbivory in a long-term field experiment. We suppressed insects in half of 16 plots over nine years and examined the genotypic structure and chemical defense of common dandelion (Taraxacum officinale), a n...

Many clonal organisms occasionally outcross, but the long-term consequences of such infrequent events are often unknown. During five years, representing three to five plant generations, we followed 16 experimental field populations of the forb, Oenothera biennis, originally planted with the same 18 original genotypes. Oenothera biennis usually self...

Premise of the Study Pachypodium (Apocynaceae) is a genus of iconic stem‐succulent and poisonous plants endemic to Madagascar and southern Africa. We tested hypotheses about the mode of action and macroevolution of toxicity in this group. We further hypothesized that while monarch butterflies are highly resistant to cardenolide toxins (a type of ca...

We study how knowledge is produced at the intersection of science, environmental policy and public engagement. Based on analysis of monarch butterfly conservation, we critically evaluate models of knowledge production. The monarch butterfly and its migration have engaged science and enchanted people for over a century, and current threats to monarc...

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 unders...

Costs of defense are central to our understanding of interactions between organisms and their environment, and defensive phenotypes of plants have long been considered to be constrained by trade-offs that reflect the allocation of limiting resources. Recent advances in uncovering signal transduction networks have revealed that defense trade-offs ar...

The relationship between plants and insects is influenced by insects' behavioral decisions during foraging and oviposition. In mutualistic pollinators and antagonistic herbivores, past experience (learning) affects such decisions, which ultimately can impact plant fitness. The higher levels of dietary generalism in pollinators than in herbivores ma...

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. While this interaction is generally considered beneficial, variation in plant genotype may alter it from mutualistic to antagonistic. Here we link the shift in str...

Genotypic diversity in plant populations is known to enhance plant performance and ecosystem function. Nonetheless, the effect of genotypic diversity has rarely been examined across a population's lifecycle despite the expectation that changing conditions, such as population density, will alter the benefits of diversity. We simultaneously manipulat...

Attraction of mutualists and defense against antagonists are critical challenges for most organisms and can be especially acute for plants with pollinating and non-pollinating flower visitors. Secondary compounds in flowers have been hypothesized to adaptively mediate attraction of mutualists and defense against antagonists, but this hypothesis has...

Trade‐offs in an herbivore's ability to feed, avoid predation and succeed on alternative hosts are thought to be major driving factors in host specialization. In this study, we compared how two closely related milkweed beetles ( Tetraopes spp.) that have specialized on separate Asclepias species respond to host switching to alternative milkweed pla...