Are adaptation costs necessary to build up a local adaptation pattern?

Ecological specialization is pervasive in phytophagous arthropods. In such specialization mode, limits to host range are imposed by trade-offs preventing adaptation to several hosts. The occurrence of such trade-offs is inferred by a pattern of local adaptation, i.e., a negative correlation between relative performance on different hosts.

To establish a causal link between local adaptation and trade-offs, we performed experimental evolution of spider mites on cucumber, tomato and pepper, starting from a population adapted to cucumber. Spider mites adapted to each novel host within 15 generations and no further evolution was observed at generation 25. A pattern of local adaptation was found, as lines evolving on a novel host performed better on that host than lines evolving on other hosts. However, costs of adaptation were absent. Indeed, lines adapted to tomato had similar or higher performance on pepper than lines evolving on the ancestral host (which represent the initial performance of all lines) and the converse was also true, e.g. negatively correlated responses were not observed on the alternative novel host. Moreover, adapting to novel hosts did not result in decreased performance on the ancestral host. Adaptation did not modify host ranking, as all lines performed best on the ancestral host. Furthermore, mites from all lines preferred the ancestral to novel hosts. Mate choice experiments indicated that crosses between individuals from the same or from a different selection regime were equally likely, hence development of reproductive isolation among lines adapted to different hosts is unlikely.

Therefore, performance and preference are not expected to impose limits to host range in our study species. Our results show that the evolution of a local adaptation pattern is not necessarily associated with the evolution of an adaptation cost.