Differential gene expression toward species of Aristolochia impairing the performance of the Troidini butterfly Battus polydamas

The swallowtail butterfly Battus polydamas L. (Lepidoptera: Papilionidae) is a specialist on Aristolochia (Aristochiaceae). Larvae sequester secondary compounds, such as aristolochic acids (AAs), from their host plants and transfer them to adults through the pupae. In this study, we evaluated the performance of B. polydamas larvae fed from 1st instar through pupation on two host plants with distinct chemical compositions, Aristolochia ringens Vahl. (which has several diterpenes) and Aristolochia gigantea Mart. (which has acyclic monoterpenoids and sesquiterpenoids, but no diterpenoids or AAs). Differential gene expression in gut and fat body tissues in response to two larval host plants was evaluated in 5th-instar larvae. We found significant differences in the survival of larvae feeding on the two host plants; the survival in A. gigantea is significantly higher than survival in A. ringens. In A. gigantea, 46% of the larvae persisted until pupation, whereas none of the larvae feeding on A. ringens survived until the end of larval development. Upregulated and downregulated contigs comprise genes encoding ribosomal proteins, protein farnesyltransferase, phosphomevalonate kinase, dolichyl-phosphate-mannose-protein mannosyltransferase 4, and O-glucosyltransferase (possibly involved in AA metabolization), as well as genes encoding superoxide dismutase, P450s, UGTs, glutathione S-transferase, and many proteases. As expected, larvae of B. polydamas were strongly influenced by host plants containing different compounds, leading to worse larval performance on key fitness components, such as life cycle performance attributes and larval survival. We suggest that there is a threshold of toxicity in the host plant that larvae can tolerate, and above such a threshold, the impact of plant secondary chemicals is no longer beneficial for the larvae but negative, disrupting their detoxification mechanism.