Evolutionary constraints in host shifts: Limited adaptation of <i>Plutella xylostella</i> to cardenolide‐defended <i>Erysimum cheiranthoides</i>

Abstract Coevolutionary arms races between plants and insects, in which gains of novel plant defences select for counteradaptations in herbivores, are key drivers of biodiversity. In the Brassicaceae genus Erysimum , the evolution of cardenolide toxins represents a recent innovation that effectively deters many Brassicaceae herbivores. Nonetheless, some herbivores continue to attack Erysimum , potentially representing early adapters of a novel toxic host on the path towards specialization. Here, we investigated the interaction between the diamondback moth (DBM, Plutella xylostella ) and the cardenolide‐producing plant Erysimum cheiranthoides , by first assessing standing variation in DBM performance on Erysimum and then experimentally evolving DBM populations for improved performance over 25 generations. Although wild DBM populations varied in their traits, larvae consistently fed less on Erysimum leaves in choice assays, and when constrained to Erysimum , they exhibited reduced growth rate, survival and lower adult size compared to individuals feeding on broccoli controls. Growth assays in which a purified cardenolide compound was added to broccoli leaves demonstrated a partial susceptibility of DBM to this toxin. However, experimental evolution failed to enhance performance on Erysimum , and instead, phenotypes of evolved lines converged on a pre‐existing, highly plastic phenotype also observed among wild DBM populations. This phenotype was characterized by rapid development and high weight gain on control plants, but slow development and low weight gain on Erysimum . Although DBM did not evolve improved performance on Erysimum over 25 generations, our results demonstrate that existing genetic variation and phenotypic plasticity are sufficient to support long‐term development on this toxic host, thereby fulfilling a key prerequisite for the eventual evolution of specialized adaptations. Read the free Plain Language Summary for this article on the Journal blog.