Alternative Developmental and Transcriptomic Responses to Host Plant Water Stress in a Butterfly metapopulation

Predicting how climate change affects biotic interactions and their evolution poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. In order to assess the prospects for population persistence under climate change, it is therefore crucial to characterise response mechanisms to climate change induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA seq analysis of the larval transcriptome. We observed that responses to feeding on water limited plants, in which amino acids and aromatic compounds are enriched, showed marked intrapopulation variation, with individuals of some families performing better on control and others on water limited plants. The transcriptomic responses were concordant with the developmental responses: Families exhibiting opposite developmental responses also produced opposite transcriptomic responses, e.g. in growth associated intracellular signalling. The opposite developmental and transcriptomic responses are associated with between families differences in organic compound catabolism and storage protein production. The results reveal heritable intrapopulation variability in plasticity, suggesting potential for evolutionary responses to drought-induced changes in host plant quality in the Finnish M. cinxia metapopulation. We fed Melitaea cinxia pre-diapause larvae representing various genetic backgrounds with control watered and water limited Plantago lanceolata and examined their developmental and transcriptomic responses to host plant water limitation.