Why stay in a bad relationship? The effect of local host phenology on a generalist butterfly feeding on a low-ranked host

Hélène Audusseau, Maria de la Paz Celorio-Mancera, Niklas Janz, Sören Nylin

In plant-feeding insects, the evolutionary retention of polyphagy remains puzzling. A better understanding of the relationship between these organisms and changes in the metabolome of their host plants is likely to suggest functional links between them, and may provide insights into how polyphagy is maintained. We investigated the phenological change of Cynoglossum officinale, and how a generalist butterfly species, Vanessa cardui, responded to this change. We used untargeted metabolite profiling to map plant seasonal changes in both primary and secondary metabolites. We compared these data to differences in larval performance on vegetative plants early and late in the season. We also performed two oviposition preference experiments to test females' ability to choose between plant developmental stages (vegetative and reproductive) early and late in the season. We found clear seasonal changes in plant primary and secondary metabolites that correlated with larval performance. The seasonal change in plant metabolome reflected changes in both nutrition and toxicity and resulted in zero survival in the late period. However, large differences among families in larval ability to feed on C. officinale suggest that there is genetic variation for performance on this host. Moreover, females accepted all plants for oviposition, and were not able to discriminate between plant developmental stages, in spite of the observed overall differences in metabolite profile potentially associated with differences in suitability as larval food. In V. cardui, migratory behavior, and thus larval feeding times, are not synchronized with plant phenology at the reproductive site. This lack of synchronization, coupled with the observed lack of discriminatory oviposition, obviously has potential fitness costs. However, this "opportunistic" behavior may as well function as a source of potential host plant evolution, promoting for example the acceptance of new plants.