Warp-speed adaptation to novel hosts after 300 generations of enforced dietary specialisation in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae)

Herbivorous insects are often highly specialised, likely due to trade-offs in fitness on alternative host species. However, some pest insects are extremely adaptable and readily adopt novel hosts, sometimes causing rapid expansion of their host range as they spread from their original host and geographic origin. The genetic basis of this phenomenon is poorly understood, limiting our ability to predict or mitigate global insect pest outbreaks. We investigated the trajectory of early adaptation to novel hosts in a regionally-specialised global crop pest species (the cowpea seed beetle Callosobruchus maculatus). After experimentally-enforced dietary specialisation for nearly 300 generations, we measured changes in fitness over the first 5 generations of adaptation to 6 novel hosts. Of these, C. maculatus reproduced successfully on all but one, with reduced fitness observed on three hosts in the first generation. Loss of fitness was followed by very rapid, decelerating increases in fitness over the first 1-5 generations, resulting in comparable levels of population fitness to that observed on the original host after 5 generations. Heritability of fitness on novel hosts was high. Adaptation occurred primarily via changes in behavioural and phenological traits, and never via changes in offspring survival to adulthood, despite high heritability for this trait. These results suggest that C. maculatus possesses ample additive genetic variation for very rapid host shifts, despite a prolonged period of enforced specialization, and also suggest that some previously-inferred environmental maternal effects on host use may in part actually represent (rapidly) evolved changes. We highlight the need to examine in more detail the genetic architecture facilitating retention of high additive genetic variation for host shifts in extremely adaptable global crop pests.