Counter-intuitive developmental plasticity induced by host quality

Abstract

Adaptation to different hosts plays a central role in the evolution of specialization and speciation in phytophagous insects and parasites, and our ability to experimentally rank hosts by their quality is critical to research to understand these processes. Here we provide a counter-intuitive example in which growth is faster on poor quality hosts. The leaf beetles Oreina elongata and Oreina cacaliae share their host plant with the rust Uromyces cacaliae. Larvae reared on infected Adenostyles alliariae show reduced growth rate, reduced maximum weight and longer development time. However, they normally respond adaptively to the rust's mid-season arrival. When switched during development from healthy to infected leaves, larvae accelerate growth and reduce development time, but pupate at lower body weight. In this novel plant-insect-fungus interaction, infection forms the cue to trade off life-history traits in order to complete development within the brief alpine summer. It represents a novel mode of developmental plasticity, which is likely to be found in other host-parasite systems whenever host quality deteriorates due to multiple infection or ageing. This phenotypic plasticity would modify competition after co-infection and the mutual selection imposed by hosts and parasites, and creates a paradoxical negative correlation between growth rate and environmental quality.

Figure 1

Larval performance of O. elongata and O. cacaliae from two populations reared on healthy, rust-infected or switched diets. Graphs show the (a) pre-switch and (b) post-switch growth rates (calculated as daily growth multipliers, see text for details), (c) the maximum weight (in mg) reached by the larvae during their development and (d) the number of days needed to reach the maximum weight (all shown as means±standard errors, n=6 for O. elongata, n=5 for O. cacaliae). Diamonds, healthy diet; circles, infected diet; crosses, switched diet; dev. time, development time.

Figure 2

Larval performance of O. elongata from two populations reared on healthy, rust-infected or switched diets and under two day-length regimes (early and late-summer photoperiod). Graphs show the (a) pre-switch and (b) post-switch growth rates (calculated as daily growth multipliers, see text for details), (c) the maximum weight (in mg) reached by the larvae during their development and (d) the number of days needed to reach the maximum weight (all shown as means±s.e., n=10). Diamonds, healthy diet; circles, infected diet; crosses, switched diet; dev. time, development time.