following the arrival of the mite (Seeley et al. 2015; Mikheyev et al. 2015; Locke 2016). Yet, studies show that these wild colonies recovered in the absence of mite treatments without appreciable loss of genetic diversity by evolving a stable host‐parasite relationship with V. destructor.
The genetic bottleneck associated with a precipitous population decline would have devastated most species; cheetahs and Florida panthers, to name two prominent mammalian examples, exhibit extensive disease syndromes from low genetic variability. A. mellifera, however, came through its population decline with remarkable genetic variation intact because polyandry, a breeding strategy whereby the queen mates with 10–20 drones, helps maintain the genetic composition of a population. Polyandry also confers improved fitness through enhanced disease resistance (Seeley and Tarpy 2007); higher foraging rates, food storage, and population growth (Mattila and Seeley 2007); and possibly better queen physiology and lifespan in the colony (Richard et al. 2007). Fitness follows diversity and in honey bee colonies this comes through the multiple matings of the queen. In nature, there must be a trade‐off between the optimal number of drone matings and the time that queens spend on their mating flights, which sometimes extend several miles from a queen bee's home. Delaplane and colleagues (2015) showed that queens artificially inseminated with sperm from 30 to 60 drones, rather than the 12 to 15 drones that are typical for the queens of wild colonies, produced more brood and had lower mite infestation rates relative to control colonies, supporting the idea that resistance to pathogens and parasites is a strong selection pressure favoring polyandry. One hypothesis to explain the high levels of polyandry of queen honey bees is that by mating with many males, the queen captures rare alleles that regulate resistance to pests and pathogens (Sherman et al. 1998; Delaplane et al. 2015). This has been confirmed in several studies in which colonies whose queens had either a high or a low number of mates were inoculated with the spores of chalkbrood (Ascosphaera apis) or American foulbrood (Paenabacillus larvae), and the levels of infection in their colonies were compared (Tarpy and Seeley 2006; Seeley and Tarpy 2007). The higher the number of mates, the lower the level of disease.
We know that Varroa mites initially killed off many wild colonies living in the forests of New York State, so maternal lines (mitochondrial DNA lineages) were lost (Mikheyev et al. 2015). Fortunately, the multiple mating by queen honey bees enabled the maintenance of the diversity of the bees' nuclear DNA despite the massive colony losses. Today, the density of wild colonies living in forests in the northeastern United States (c. 2.5 colonies per square mile, or 1 per square kilometer) is the same as it was prior to the invasion of the Varroa mites (Seeley et al. 2015; Radcliffe and Seeley 2018), and the survivor colonies possess resistance to these mites. In a comparison of the life history traits of wild colonies living in the forests around Ithaca, NY, between the 1970s (pre Varroa) and the 2010s (post Varroa), Seeley (2017b) found no differences, which implies that the wild colonies possess defenses against the mites that are not highly costly and so do not hinder colony reproduction.
Figure 1.2 Grooming, or mite‐chewing, is a heritable trait in which honey bees remove and kill adult Varroa mites by chewing off parts of the mite's body, carapace, or legs.
Figure 1.3 Hygienic behavior or Varroa Sensitive Hygiene (VSH), is a form of social immunity in which honey bees selectively remove the varroa‐infested larvae and pupae from beneath capped cells. The mites infecting these brood cells are killed along with the developing bee upon opening of the cell.
There exist multiple mechanisms of natural Varroa resistance, a form of behavioral social immunity, that have a genetic basis. These include grooming behavior, also known as “mite chewing,” and hygienic behavior, also known as Varroa Sensitive Hygiene (VSH). Grooming behavior is the process whereby worker bees kill mites by deftly chewing off the carapace, ventral plate, or legs of a mite (Figure 1.2). The strength of a colony's ability to groom Varroa mites is indicated by the percentage of chewed mites among the mites that fall onto a sticky board placed beneath a screened bottom board in a hive (Rosenkranz et al. 1997). Hygienic behavior is the process whereby worker bees remove diseased (or dead) brood from the cells in which they are (or were) developing (Figure 1.3). VSH is measured by determining the percentage of sealed brood cells that contain Varroa mites shortly after cell capping and then again shortly before brood emergence (cell uncapping). Because this assay of a colony's VSH behavior is rather tricky to perform, people often use a different assessment of hygienic behavior: the freeze‐killed brood (FKB) assay. Because the FKB assay does not involve Varroa infested brood, it is not a direct measure of VSH. The FKB assay works by freezing a c. 3 in. diameter circle of sealed brood cells, thereby killing the brood within, followed by calculating the percentage of the dead brood that have been removed, either 24 or 48 hours after the freezing of the brood (Spivak and Downey 1998).
In a long‐term study in Norway, variation among colonies in their resistance to Varroa was found to be based on neither grooming behavior nor hygienic behavior, but on something else that was hindering mite reproduction. Oddie and colleagues (2017) examined managed honey bee colonies that had survived in the absence of Varroa control for >17 years alongside managed colonies that had received miticide treatments twice each year. Records were kept of daily mite drop counts, and of assays of the colonies' mite grooming and hygienic behaviors, for both survivor and control colonies. No difference was found in the proportion of damaged mites (~40% chewed in colonies of both groups) or in FKB removal rates (only ~5% brood removed). However, the average daily mite‐drop counts (indicators of the mite populations in colonies) were 30% lower in surviving colonies compared to susceptible ones. Evidently, there were other colony factors (besides mite grooming and hygienic behaviors) responsible for reducing the reproductive success of the mites in these colonies of Norwegian honey bees. Since donor brood was used for the testing in both groups of colonies (mite susceptible and mite resistant), the possibility of protective traits of immature bees was eliminated. What Oddie et al. found is that in the mite‐resistant colonies (but not in the mite‐susceptible ones) the worker bees are uncapping brood cells and then recapping them several hours later, and that this reduces the mites' reproductive success to a level that protects the colony. An 80% reduction in mite reproductive success, together with a reduction in brood size, independent of grooming or hygienic behavior, was also described for populations of survivor (untreated) colonies of honey bees living on the island of Gotland in Sweden (Fries and Bommarco 2007; Locke and Fries 2011).
Good Lifestyle
To understand the survival of honey bee colonies living in the wild, we must look not only at their genetic makeup but also at their lifestyle. How do the ways in which wild colonies live combine with their genes to limit mite reproductive success and the virulence of mite‐vectored pathogens? We know that modern beekeeping practices create living conditions for managed colonies that are far more stressful than the living conditions of colonies living in the wild (see Table 1.1). For example, we know that the artificial crowding of colonies in an apiary, the provision of large hives which foster Varroa reproduction, and the suppression of swarming behavior – are all apicultural manipulations that make large honey harvests possible for the beekeeper but are harmful to colony health (Seeley and Smith 2015; Loftus et al. 2016). Another important, but little understood, stressor experienced by managed colonies is the greater thermoregulation stresses
