In eusocial insect colonies nestmates cooperate to combat parasites, a trait called social immunity. However, social immunity failed for Western honey bees (Apis mellifera) when the ectoparasitic mite Varroa destructor switched hosts from Eastern honey bees (Apis cerana). This mite has since become the most severe threat to A. mellifera world-wide. Despite this, some isolated A. mellifera populations are known to survive infestations by means of natural selection, largely by supressing mite reproduction, but the underlying mechanisms of this are poorly understood. Here, we show that a cost-effective social immunity mechanism has evolved rapidly and independently in four naturally V. destructor-surviving A. mellifera populations. Worker bees of all four ‘surviving’ populations uncapped/recapped worker brood cells more frequently and targeted mite-infested cells more effectively than workers in local susceptible colonies. Direct experiments confirmed the ability of uncapping/recapping to reduce mite reproductive success without sacrificing nestmates. Our results provide striking evidence that honey bees can overcome exotic parasites with simple qualitative and quantitative adaptive shifts in behaviour. Due to rapid, parallel evolution in four host populations this appears to be a key mechanism explaining survival of mite infested colonies.

Background: Managed, feral and wild populations of European honey bee subspecies, Apis mellifera, are currently facing severe colony losses globally. There is consensus that the ectoparasitic mite Varroa destructor, that switched hosts from the Eastern honey bee Apis cerana to the Western honey bee A. mellifera, is a key factor driving these losses. For >20 years, breeding efforts have not produced European honey bee colonies that can survive infestations without the need for mite control. However, at least three populations of European honey bees have developed this ability by means of natural selection and have been surviving for >10 years without mite treatments. Reduced mite reproductive success has been suggested as a key factor explaining this natural survival. Here, we report a managed A. mellifera population in Norway, that has been naturally surviving consistent V. destructor infestations for >17 years. Methods: Surviving colonies and local susceptible controls were evaluated for mite infestation levels, mite reproductive success and two potential mechanisms explaining colony survival: grooming of adult worker bees and Varroa Sensitive Hygiene (VSH): adult workers specifically detecting and removing mite-infested brood. Results: Mite infestation levels were significantly lower in surviving colonies and mite reproductive success was reduced by 30% when compared to the controls. No significant differences were found between surviving and control colonies for either grooming or VSH. Discussion: Our data confirm that reduced mite reproductive success seems to be a key factor for natural survival of infested A. mellifera colonies. However, neither grooming nor VSH seem to explain colony survival. Instead, other behaviors of the adult bees seem to be sufficient to hinder mite reproductive success, because brood for this experiment was taken from susceptible donor colonies only. To mitigate the global impact of V. destructor, we suggest learning more from nature, i.e., identifying the obviously efficient mechanisms favored by natural selection.

The ectoparasitic mite Varroa destructor is a key factor for colony losses in European honey bee subspecies (Apis mellifera), but it is also known that some host populations have adapted to the mite by means of natural selection. The role of a shorter host brood postcapping period in reducing mite reproductive success has been investigated in other surviving subspecies, however its role in the adaptation of European honey bee populations has not been addressed. Here, we use a common garden approach to compare the length of the worker brood postcapping period in a Norwegian surviving honey bee population with the postcapping period of a local susceptible population. The data show a significantly shorter postcapping period in the surviving population for ~10% of the brood. Since even small differences in postcapping period can significantly reduce mite reproductive success, this mechanism may well contribute to natural colony survival. It appears most likely that several mechanisms acting together produce the full mite-surviving colony phenotype.

Cell recapping is a behavioural trait of honeybees (Apis mellifera) where cells with developing pupae are uncapped, inspected, and then recapped, without removing the pupae. The ectoparasitic mite Varroa destructor, unarguably the most destructive pest in apiculture world-wide, invades the cells of developing pupae to feed and reproduce. Honeybees that target mite infested cells with this behaviour may disrupt the reproductive cycle of the mite. Hence, cell recapping has been associated with colony-level declines in mite reproduction. In this study we compared the colony-level efficacy of cell recapping (how often infested cells are recapped) to the average mite fecundity in A. mellifera. Our study populations, known to be adapted to V. destructor, were from Avignon, France, Gotland, Sweden, and Oslo, Norway, and were compared to geographically similar, treated control colonies. The results show that colonies with a higher recapping efficacy also have a lower average mite reproductive success. This pattern was likely driven by the adapted populations as they had the largest proportion of highly-targeted cell recapping. The consistent presence of this trait in mite-resistant and mite-susceptible colonies with varying degrees of expression may make it a good proxy trait for selective breeding on a large scale.

Nest predation is the leading cause of reproductive mortality in oviparous tetrapods and can limit population growth in some species. Rates of nest predation could be influenced through modification of the cues used to find nests, but this requires a clear understanding of how nests are located. Here, we used a buffet-style choice experiment to test the relative role of three cue types (visual, tactile, and chemosensory) on the detection and depredation of Snapping Turtle (Chelydra serpentina (L., 1758)) nests by a suite of predators dominated by raccoons (Procyon lotor (L., 1758)). We created sets of artificial nests along an authentic nesting site, presenting single or multiple cues. We interspersed artificial nests with authentic nests and monitored predation rates on both. Predators used all three cues to locate potential nests for investigation. However, nests with tactile cues were significantly more likely to be depredated than nests with only visual and chemosensory cues. Multiple cues had additive effects on predation probability. Addition of chemosensory cues to tactile treatments increased the probability of predation. The importance of tactile cues in this system supports the use of nest cages to protect nests in early stages of development, but cannot explain the recently described late-stage peak in predation.