How does evolution in a constant and fluctuating environment shape the host range and thermal niche breadth of a global crop pest mite?

Abstract: Agricultural pests face environmental fluctuations that influence their life history
traits and tolerance to biotic and abiotic factors, consequently affecting the damage they cause to crops. We investigated how the fluctuating and stable environments influence the fitness of phytophagous agricultural arthropod pests (i) on various host plant species, and (ii) at various temperatures. The model organism was an important global cereal pest, phytophagous mite Aceria tosichella (wheat curl mite). We used mite populations that experimentally evolved under (i) constant conditions, i. e., a single host environment (wheat), or (ii) fluctuating conditions, i. e., alternation of two plant species (wheat and barley). The fitness of these experimentally evolved lineages was assessed on various host plant species (wheat, barley, rye, smooth brome, quackgrass, and tall-oat grass), and at temperatures ranging from 12 °С to 36 °С. We showed that the wheat curl mite’s niche breadth evolved in response to the level of environmental variability, but its biotic and abiotic dimensions evolved in opposite directions. The constant environment resulted in mites with a narrow host range but a broad temperature tolerance. In contrast, the fluctuating environment led to an expanded host range but a narrower thermal tolerance, as compared to specialists. Our findings suggest a trade-off between biotic and abiotic niche dimensions. The study highlights the importance of explaining how agricultural pests respond to various degrees of environmental heterogeneity, which in turn helps to understand their colonization and invasive potential and may have implications for their management.