Host-Parasite Co-Evolution in Real-Time: Changes in Honey Bee Resistance Mechanisms and Mite Reproductive Strategies

Simple Summary Parasitic mites, Varroa destructor, are a major threat for Western honey bees, Apis mellifera, colonies globally. Nevertheless, some honey bee populations can survive infestations with this mite, probably due to behaviors that suppress parasite reproduction. However, possible changes in mites associated with these surviving bees and the potential variations of bee behavior over time are poorly understood. Here, we show that mites can change their reproduction when associated with surviving hosts and that the bee behaviors suppressing mite reproduction can vary over time. In a fully-crossed field experiment on Dutch surviving colonies (Amsterdam Water Dunes (AWD) selection), worker brood cell recapping and varroa sensitive hygiene (VSH) performed by bees and mite reproductive parameters were investigated. Neither recapping nor VSH were significantly expressed even though a previous study showed VSH in these AWD bees. A larger proportion of mites that co-evolved with AWD surviving bees reproduced compared to mites in routinely treated colonies, but had lower fecundity. Overall, our study suggests that honeybee colonies can survive infestations with these mites by not yet understood means and shows for the first time adaptive changes in the reproduction of their coevolved mites. Abstract Co-evolution is a major driving force shaping the outcome of host-parasite interactions over time. After host shifts, the lack of co-evolution can have a drastic impact on novel host populations. Nevertheless, it is known that Western honey bee (Apis mellifera) populations can cope with host-shifted ectoparasitic mites (Varroa destructor) by means of natural selection. However, adaptive phenotypic traits of the parasites and temporal variations in host resistance behavior are poorly understood. Here, we show that mites made adaptive shifts in reproductive strategy when associated with resistant hosts and that host resistance traits can change over time. In a fully-crossed field experiment, worker brood cells of local adapted and non-adapted (control) A. mellifera host colonies were infested with mites originating from both types of host colonies. Then, mite reproduction as well as recapping of cells and removal of infested brood (i.e., Varroa Sensitive Hygiene, VSH) by host workers were investigated and compared to data from the same groups of host colonies three years earlier. The data suggest adaptive shifts in mite reproductive strategies, because mites from adapted hosts have higher probabilities of reproduction, but lower fecundity, when infesting their associated hosts than mites in treated colonies. The results confirm that adapted hosts can reduce mite reproductive success. However, neither recapping of cells nor VSH were significantly expressed, even though the latter was significantly expressed in this adapted population three years earlier. This suggests temporal variation in the expression of adaptive host traits. It also appears as if mechanisms not investigated here were responsible for the reduced mite reproduction in the adapted hosts. In conclusion, a holistic view including mite adaptations and studies of the same parasite/host populations over time appears overdue to finally understand the mechanisms enabling survival of V. destructor-infested honey bee host colonies.