Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co-occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource-use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co-occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource-use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities.

1. Initial herbivory and induced plant responses can influence subsequent above- and belowground herbivore attack. When two life stages of the same herbivore damage different plant parts sequentially, there is strong potential for plants to respond with induced plant defense against the later attacker. Alternatively, the earlier attacker could manipulate the host plant to facilitate the later-feeding life stage. 2. We studied herbivory by foliage-feeding adults and root-feeding larvae of the red milkweed beetle (Tetraopes tetraophthalmus) on common milkweed (Asclepias syriaca) in laboratory and field experiments. We applied factorial above- and belowground herbivory treatments to test for induced responses, effects on later-feeding conspecific larvae, and damage by naturally colonizing herbivores, including adult T. tetraophthalmus. 3. We found that the inducibility of toxic cardenolides was systemic across the root-shoot barrier, with the highest concentrations in plants damaged both above- and belowground. Initial aboveground herbivory increased root damage and larval survival, suggesting an increase in root quality following leaf herbivory. Initial belowground herbivory did not affect the performance of later-feeding larvae, indicating limited importance of induced root cardenolides and competition between clutches of T. tetraophthalmus. 4. In a natural milkweed population, initial aboveground herbivory attracted conspecific adults and milkweed leaf beetles (Labidomera clivicollis), and ultimately reduced fruit production by 33%. Nonetheless, the probability of damage by monarch caterpillars (Danaus plexippus) was reduced on plants initially damaged by T. tetraophthalmus aboveground, perhaps due to reduced oviposition following induced plant responses. 5. Synthesis: Induced plant responses of common milkweed to aboveground damage by adult T. tetraophthalmus both facilitate further damage by adults, and enhance the performance of their root-feeding larvae, most likely as a result of host plant manipulation. Although the same induction reduced monarch herbivory, the net effect of these interactions was reduced fruit production. Host plant manipulation may be especially common by specialist herbivores that have sequential above- and belowground life stages.