Avoiding the tragedies of parasite tolerance in Darwinian beekeeping

Abstract

Bee declines have been partly attributed to the impacts of invasive or emerging parasite outbreaks. For western honeybees, Apis mellifera, major losses are associated with the virus-vectoring mite, Varroa destructor. In response, beekeepers have focused breeding efforts aimed at conferring resistance to this key parasite. One method of many is survival-based beekeeping where colonies that survive despite significant Varroa infestations produce subsequent colonies. We argue that this 'hands-off' approach will not always lead to Varroa resistance evolving but rather tolerance. Tolerance minimizes host fitness costs of parasitism without reducing parasite abundance, whereas resistance either prevents parasitism outright or keeps parasitism intensity low. With clear epidemiological distinctions, and as honeybee disease dynamics impact other wild bees owing to shared pathogens, we discuss why tolerance outcomes in honeybee breeding have important implications for wider pollinator health. Crucially, we argue that unintentional selection for tolerance will not only lead to more spillover from honeybees but may also select for pathogens that are more virulent in wild bees leading to 'tragedies of tolerance'. These tragedies can be avoided through successful breeding regimes that specifically select for low Varroa. We emphasize how insights from evolutionary ecology can be applied in ecologically responsible honeybee management.

Keywords: disease; honeybees; parasite; resistance; tolerance; varroa.

Figure 1.

Graphical abstract illustrating the ecological consequences between tolerance and resistance to Varroa destructor in honeybees. With parasite tolerance (left) a honeybee shows high Varroa (red) infestation, shedding more viruses into the environment (green). This leads to an increased risk of environmental transmission between honeybees and co-foraging bumblebees. In this example, all three bumblebees are infected and two have higher viral loads. Alternatively, (right) a Varroa-resistant honeybee is shown free of mites, shedding fewer viral particles into the environment, leading to decreased rates of infection with one infected bumblebee showing a low viral load (green) and two healthy bumblebees (blue).

Figure 2.

The phenotypic combinations possible in the honeybee hosts resistance/tolerance to Varroa (red) and viruses (green). Varroa/virus tolerance (top left) is a likely combination of natural selection via undirected ‘survival-stock’ breeding wherein the host tolerates viral infection which by proxy tolerates the mite. The Varroa tolerance, virus resistance (top right) and Varroa resistance, virus tolerance (bottom left) phenotypes are less supported in the literature. Varroa/virus resistance (bottom right) occurs through control of the mite population that controls viral infections by limiting host–vector interactions.