Established invasive species can pose a continuous threat to biodiversity and food security, thereby calling for sustainable mitigation. There is a consensus that the ubiquitous ecto-parasitic mite Varroa destructor, an invasive species from Asia, is the main biological threat to global apiculture with Apis mellifera. V. destructor has almost completely wiped out wild European honey bee (Apis mellifera) populations. The only remedy for apiculture, to date, is frequent control measures against the mite throughout the season, which prevents possible adaptations. While targeted breeding efforts have, so far, not achieved the selection of tolerant or resistant bees, natural selection approaches have succeeded at least seven times. Here, we propose to take advantage of natural selection for honey bee resistance by stopping mite treatment in managed colonies. The main principles are within population mating of the colonies' own virgin queens and drones and selection based on survival and proliferous development of colonies. Being used for 10 years, it has shown to result in grosso modo 'normal' colonies with a high level of resistance to V. destructor. Here, we call for local groups of beekeepers and scientists to join a novel natural selection program that has started so far on three locations. This will eventually lead to several locally adapted V. destructor resistant honey bee populations around the world, and help global apiculture becoming more sustainable.

The ectoparasitic mite, Varroa destructor , is the most severe biotic threat to honeybees ( Apis mellifera ) globally, usually causing colony death within a few years without treatments. While it is known that a few A. mellifera populations survive mite infestations by means of natural selection, the possible role of mite adaptations remains unclear. To investigate potential changes in mite populations in response to host adaptations, the genetic structure of V. destructor in the mite-resistant A. mellifera population on Gotland, Sweden, was studied. Spatio-temporal genetic changes were assessed by comparing mites collected in these colonies, as well as from neighboring mite-susceptible colonies, in historic (2009) and current (2017/2018) samples. The results show significant changes in the genetic structure of the mite populations during the time frame of this study. These changes were more pronounced in the V. destructor population infesting the mite-resistant honeybee colonies than in the mite-susceptible colonies. These results suggest that V. destructor populations are reciprocating, in a coevolutionary arms race, to the selection pressure induced by their honeybee host. Our data reveal exciting new insights into host-parasite interactions between A. mellifera and its major parasite.

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 (Apismellifera) 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.

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors governing host–parasite interactions. Even though invasive parasites are considered of major biological importance, little is known about their adaptative potential when infesting the new hosts. Here, the genetic diversification of Varroa destructor , a novel parasite of Apis mellifera originating from Asia, was investigated using population genetics to determine how the genetic structure of the parasite changed in distinct European populations of its new host. To do so, mites infesting two categories of hosts in four European regions were compared: (a) adapted hosts surviving through means of natural selection, thereby expected to impose strong selective pressure on the mites, and (b) treated host populations, surviving mite infestations because acaricides are applied, therefore characterized by a relaxed selection imposed by the host on the mites. Significant genetic divergence was found across regions, partially reflecting the invasion pattern of V. destructor throughout Europe and indicating local adaptation of the mite to the host populations. Additionally, varying degrees of genotypic changes were found between mites from adapted and treated colonies. Altogether, these results indicate that V. destructor managed to overcome the genetic bottlenecks following its introduction in Europe and that host‐mediated selection fostered changes in the genetic structure of this mite at diverse geographic scales. These findings highlight the potential of parasites to adapt to their local host populations and confirm that adaptations developed within coevolutionary dynamics are a major determinant of population genetic changes.