Macroevolution of protective coloration across caterpillars reflects relationships with host plants.

A critical function of animal coloration is avoiding attack, either by warning predators or reducing detectability. Evolution of these divergent strategies may depend on prey palatability and apparency to predators: conspicuous coloration may be favoured if species are distasteful, or habitats make hiding difficult; by contrast, camouflage may be effective if prey lack defences or environments are visually complex. For insect herbivores, host plants provide both chemical defence and the background against which they are detected or obscured; thus, plant traits may be key to coloration in these foundational terrestrial organisms. We use 1808 species of larval Lepidoptera to explore macroevolution of protective coloration strategy. We find that colour and pattern evolve jointly in caterpillars, similar to an array of species across the animal kingdom, while individual elements of coloration evolve closely with diet ecology. Consistent with key tenets of plant defence and plant-herbivore coevolutionary theory, conspicuous colours are associated with herbaceous host plants-thought to be defended by toxins-while camouflage colours and patterns are associated with woody plants and grasses. Contrary to theory, dietary specialization is not associated with conspicuous coloration. Our results add valuable insights into the evolutionary forces shaping colour and pattern in nature.

A domestic plant differs from its wild relative along multiple axes of within-plant trait variability and diversity.

For 10,000 years humans have altered plant traits through domestication and ongoing crop improvement, shaping plant form and function in agroecosystems. To date, studies have focused on how these processes shape whole-plant or average traits; however, plants also have characteristic levels of trait variability among their repeated parts, which can be heritable and mediate critical ecological interactions. Here, we examine an underappreciated scale of trait variation-among leaves, within plants-that may have changed through the process of domestication and improvement. Variability at this scale may itself be a target of selection, or be shaped as a by-product of the domestication process. We explore how levels of among-leaf trait variability differ between cultivars and wild relatives of alfalfa (Medicago sativa), a key forage crop with a 7,000-year domestication history. We grew individual plants from 30 wild populations and 30 cultivars, and quantified variability in a broad suite of physical, nutritive, and chemical leaf traits, including measures of chemical dissimilarity (beta diversity) among leaves within each plant. We find that trait variability has changed over the course of domestication, with effects often larger than changes in trait means. Domestic alfalfa had elevated among-leaf variability in SLA, trichomes, and C:N; increased diversity in defensive compounds; and reduced variability in phytochemical composition. We also elucidate fundamental relationships between trait means and variability, and between overall production of secondary metabolites and patterns of chemical diversity. We conclude that within-plant variability is an overlooked dimension of trait diversity in a globally critical agricultural crop. Trait variability is actually higher in cultivated plants compared to wild progenitors for multiple nutritive, physical, and chemical traits, highlighting a scale of variation that may mitigate loss of trait diversity at other scales in alfalfa agroecosystems, and in other crops with similar histories of domestication and improvement.

Generalists are more specialized in low-resource habitats, increasing stability of ecological network structure.

Linking mechanistic processes to the stability of ecological networks is a key frontier in ecology. In trophic networks, "modules"-groups of species that interact more with each other than with other members of the community-confer stability, mitigating effects of species loss or perturbation. Modularity, in turn, is shaped by the interplay between species' diet breadth traits and environmental influences, which together dictate interaction structure. Despite the importance of network modularity, variation in this emergent property is poorly understood in complex natural systems. Using two years of field data, we quantified interactions between a rich community of lepidopteran herbivores and their host plants across a mosaic of low-resource serpentine and high-resource nonserpentine soils. We used literature and our own observations to categorize herbivore species as generalists (feeding on more than one plant family) or specialists (feeding on one plant family). In both years, the plant-herbivore network was more modular on serpentine than on nonserpentine soils-despite large differences in herbivore assemblage size across years. This structural outcome was primarily driven by reduction in the breadth of host plant use by generalist species, rather than by changes in the composition of species with different fundamental diet breadths. Greater modularity-and thus greater stability-reflects environmental conditions and plastic responses by generalist herbivores to low host plant quality. By considering the dual roles of species traits and ecological processes, we provide a deeper mechanistic understanding of network modularity, and suggest a role for resource availability in shaping network persistence.

Cascading effects of soil type on assemblage size and structure in a diverse herbivore community.

Soil type is understudied as a driver of herbivore community size and structure across host plants. This study extends predictions of resource availability hypotheses to understand how soil types of different resource levels alter plant resistance and structure of herbivore assemblages. In this 2-yr study we use seven dominant chaparral shrub species that grow across a natural mosaic of low and high resource soils to explore effects of soil type on plant resistance, and relate these soil-based differences in resistance to the abundance and diversity of the larval lepidopteran community. We show that growing on low-resource soils increases plant resistance, as measured by herbivore performance, both within and across host plant species, and that resistance may be driven by variation in plant nutritive and defensive traits. We then show that more resistant plants on low-resource soils host less abundant and less diverse herbivore assemblages across a natural soil mosaic in the field.

Variability in plant nutrients reduces insect herbivore performance.

The performance and population dynamics of insect herbivores depend on the nutritive and defensive traits of their host plants. The literature on plant-herbivore interactions focuses on plant trait mean values, but recent studies showing the importance of plant genetic diversity for herbivores suggest that plant trait variance may be equally important. The consequences of plant trait variance for herbivore performance, however, have been largely overlooked. Here we report an extensive assessment of the effects of within-population plant trait variance on herbivore performance using 457 performance datasets from 53 species of insect herbivores. We show that variance in plant nutritive traits substantially reduces mean herbivore performance via non-linear averaging of performance relationships that were overwhelmingly concave down. By contrast, relationships between herbivore performance and plant defence levels were typically linear, with variance in plant defence not affecting herbivore performance via non-linear averaging. Our results demonstrate that plants contribute to the suppression of herbivore populations through variable nutrient levels, not just by having low average quality as is typically thought. We propose that this phenomenon could play a key role in the suppression of herbivore populations in natural systems, and that increased nutrient heterogeneity within agricultural crops could contribute to the sustainable control of insect pests in agroecosystems.