Fighting for Chemicals: Pharmacophagy-Induced Contest Behaviour and Its Molecular Signatures in a Sawfly

Elucidating the multifaceted effects of plant metabolites sequestered by animals from plants for non-nutritional purposes, known as pharmacophagy, is fundamental to understanding the evolution of acquired chemical defences. Some herbivorous species do not only take up plant metabolites from plants but also engage in antagonistic interactions to acquire precious metabolites from conspecifics that had access to the plant chemicals. We investigated behavioural and molecular consequences of pharmacophagy using the turnip sawfly, Athalia rosae. Adults are known to be attracted to the plant Ajuga reptans. Using behavioural assays and chemical analysis, we showed that the sawflies acquire clerodanoids by licking the leaves. Moreover, aggressively licking conspecifics that had acquired plant clerodanoids resulted in the transfer of these metabolites between individuals. Transcriptomic analyses revealed that the acquisition of clerodanoids from leaves led to only minimal upregulation of known detoxification genes and pathways. In contrast, the aggressive licking of conspecifics resulted in the upregulation of metabolic pathways associated with elevated energy consumption or detoxification. Thus, individuals attack conspecifics to acquire clerodanoids despite the apparent metabolic costs. Changes in the metabolic phenotype of A. rosae individuals have profound consequences for the individuals' physiology and interactions with conspecifics, with possible impacts on the social niche.