Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed

1 We studied the genetic and environmental determinants of attack by the specialist stem-attacking weevil, Rhyssomatus lineaticollis on Asclepias syriaca. 2 In natural populations, the extent of stem damage and oviposition were positively correlated with stem width, but not stem height. We hypothesized that both genotypic and environmental factors influencing stem morphology would affect attack by weevils. 3 In a common garden study with 21 full-sib families of milkweed, both phenotypic and genetic correlations indicated that weevils impose more damage and lay more eggs on thicker stemmed plants. 4 Of three other putative resistance traits, only latex production showed a negative genetic correlation with weevil attack. 5 When neighbouring grasses were clipped to reduce light competition, focal milkweed plants received up to 2.6 times the photosynthetically active radiation and 1.6 times the red to far red ratio of light compared with plants with intact grass neighbours. Focal milkweed plants were therefore released from the classic neighbour avoidance response and had 20% shorter internode lengths, were 30% shorter, and had 90% thicker stems compared with controls. 6 Clipping of grass neighbours resulted in nearly 2.7 times the damage and oviposition by stem weevils, thus supporting the hypothesis of an environmental or trait-mediated indirect influence on resistance. 7 Although attack of plants by weevils strongly increases the probability of stem mortality, thicker stems experience lower mortality, thus counteracting the selective impact of weevil-induced plant mortality. 8 The determinants of attack on milkweeds include both genetic variation for stem thickness and an indirect environmental influence of plant neighbours. If milkweeds and weevils are coevolving, the interaction is diffuse because the ecological neighbourhood is likely to modify the patterns of reciprocal natural selection.