Prospects, challenges and perspectives in harnessing natural selection to solve the 'varroa problem' of honey bees.

Honey bees, Apis mellifera, of European origin are major pollinators of crops and wild flora. Their endemic and exported populations are threatened by a variety of abiotic and biotic factors. Among the latter, the ectoparasitic mite Varroa destructor is the most important single cause behind colony mortality. The selection of mite resistance in honey bee populations has been deemed a more sustainable solution to its control than varroacidal treatments. Because natural selection has led to the survival of some European and African honey bee populations to V. destructor infestations, harnessing its principles has recently been highlighted as a more efficient way to provide honey bee lineages that survive infestations when compared with conventional selection on resistance traits against the parasite. However, the challenges and drawbacks of harnessing natural selection to solve the varroa problem have only been minimally addressed. We argue that failing to consider these issues could lead to counterproductive results, such as increased mite virulence, loss of genetic diversity reducing host resilience, population collapses or poor acceptance by beekeepers. Therefore, it appears timely to evaluate the prospects for the success of such programmes and the qualities of the populations obtained. After reviewing the approaches proposed in the literature and their outcomes, we consider their advantages and drawbacks and propose perspectives to overcome their limitations. In these considerations, we not only reflect on the theoretical aspects of host-parasite relationships but also on the currently largely neglected practical constraints, that is, the requirements for productive beekeeping, conservation or rewilding objectives. To optimize natural selection-based programmes towards these objectives, we suggest designs based on a combination of nature-driven phenotypic differentiation and human-directed selection of traits. Such a dual strategy aims at allowing field-realistic evolutionary approaches towards the survival of V. destructor infestations and the improvement of honey bee health

Advances and perspectives in selecting resistance traits against the parasitic mite Varroa destructor in honey bees.

In spite of the implementation of control strategies in honey bee (Apis mellifera) keeping, the invasive parasitic mite Varroa destructor remains one of the main causes of colony losses in numerous countries. Therefore, this parasite represents a serious threat to beekeeping and agro-ecosystems that benefit from the pollination services provided by honey bees. To maintain their stocks, beekeepers have to treat their colonies with acaricides every year. Selecting lineages that are resistant to infestations is deemed to be a more sustainable approach. Over the last three decades, numerous selection programs have been initiated to improve the host-parasite relationship and to support honey bee survival in the presence of the parasite without the need for acaricide treatments. Although resistance traits have been included in the selection strategy of honey bees, it has not been possible to globally solve the V. destructor problem. In this study, we review the literature on the reasons that have potentially limited the success of such selection programs. We compile the available information to assess the relevance of selected traits and the potential environmental effects that distort trait expression and colony survival. Limitations to the implementation of these traits in the field are also discussed. Improving our knowledge of the mechanisms underlying resistance to V. destructor to increase trait relevance, optimizing selection programs to reduce environmental effects, and communicating selection outcomes are all crucial to efforts aiming at establishing a balanced relationship between the invasive parasite and its new host

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

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

Population genetics of ectoparasitic mites Varroa spp. in Eastern and Western honey bees.

Host shifts of parasites are often causing devastating effects in the new hosts. The Varroa genus is known for a lineage of Varroa destructor that shifted to the Western honey bee, Apis mellifera, with disastrous effects on wild populations and the beekeeping industry. Despite this, the biology of Varroa spp. remains poorly understood in its native distribution range, where it naturally parasitizes the Eastern honey bee, Apis cerana. Here, we combined mitochondrial and nuclear DNA analyses with the assessment of mite reproduction to determine the population structure and host specificity of V. destructor and Varroa jacobsonii in Thailand, where both hosts and several Varroa species and haplotypes are sympatric. Our data confirm previously described mite haplogroups, and show three novel haplotypes. Multiple infestations of single host colonies by both mite species and introgression of alleles between V. destructor and V. jacobsonii suggest that hybridization occurs between the two species. Our results indicate that host specificity and population genetic structure in the genus Varroa is more labile than previously thought. The ability of the host shifted V. destructor haplotype to spillback to A. cerana and to hybridize with V. jacobsonii could threaten honey bee populations of Asia and beyond

Paenibacillus melissococcoides sp. nov., isolated from a honey bee colony affected by European foulbrood disease.

A novel, facultatively anaerobic, Gram-stain-positive, motile, endospore-forming bacterium of the genus Paenibacillus, designated strain 2.1T, was isolated from a colony of Apis mellifera affected by European foulbrood disease in Switzerland. The rod-shaped cells of strain 2.1T were 2.2–6.5 μm long and 0.7–1.1 μm wide. Colonies of strain 2.1T were orange-pigmented under oxic growth conditions on solid basal medium at 35–37 °C. Strain 2.1T showed catalase and cytochrome c oxidase activity. Its polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, aminophospholipid and phospholipid. The only respiratory quinone was menaquinone 7, and the major cellular fatty acids were anteiso-C15 : 0, anteiso-C17 : 0, iso-C15 : 0, iso-C17 : 0 and palmitic acid (C16 : 0), which is consistent with other members of the genus Paenibacillus. The G+C content of the genomic DNA of strain 2.1T was 53.3 mol%. Phylogenetic analyses based on the 16S rRNA gene sequence similarity showed that strain 2.1T was closely related to Paenibacillus dendritiformis LMG 21716T (99.7 % similarity) and Paenibacillus thiaminolyticus DSM 7262T (98.8 %). The whole-genome average nucleotide identity between strain 2.1T and the type strains of P. dendritiformis and P. thiaminolyticus was 92 and 91 %, respectively, and thus lower than the 95 % threshold value for delineation of genomic prokaryotic species. Based on the results of phylogenetic, genomic, phenotypic and chemotaxonomic analyses we propose the name Paenibacillus melissococcoides sp. nov. for this novel Paenibacillus species. The type strain is 2.1T (=CCOS 2000T=DSM 113619T=LMG 32539T)

Go East for Better Honey Bee Health: Apis cerana Is Faster at Hygienic Behavior than A. mellifera.

The poor health status of the Western honey bee, Apis mellifera, compared to its Eastern counterpart, Apis cerana, is remarkable. This has been attributed to lower pathogen prevalence in A. cerana colonies and to their ability to survive infestations with the ectoparasitic mite, Varroa destructor. These properties have been linked to an enhanced removal of dead or unhealthy immature bees by adult workers in this species. Although such hygienic behavior is known to contribute to honey bee colony health, comparative data of A. mellifera and A. cerana in performing this task are scarce. Here, we compare for the first time the removal of freeze-killed brood in one population of each species and over two seasons in China. Our results show that A. cerana was significantly faster than A. mellifera at both opening cell caps and removing freeze-killed brood. The fast detection and removal of diseased brood is likely to limit the proliferation of pathogenic agents. Given our results can be generalized to the species level, a rapid hygienic response could contribute to the better health of A. cerana. Promoting the fast detection and removal of worker brood through adapted breeding programs could further improve the social immunity of A. mellifera colonies and contribute to a better health status of the Western honey bee worldwide

Neonicotinoids and ectoparasitic mites synergistically impact honeybees.

The Western honeybee, Apis mellifera, is the most important managed pollinator globally and has recently experienced unsustainably high colony losses. Synergistic interactions among stressors are believed to be primarily responsible. However, despite clear evidence of strong effect on honeybee longevity of widely-employed neonicotinoid insecticides and of the ubiquitous ectoparasitic mite Varroa destructor, no data exist to show synergistic effects between these two stressors. Even though neonicotinoids had no significant impact by themselves, we here show for the first time a synergistic time-lag interaction between mites and neonicotinoids that resulted in significantly reduced survival of long-lived winter honeybees. Even though these mites are potent vectors of viruses, the virus-insecticide interaction had no significant impact. The data suggest a previously overlooked mechanism possibly explaining recent unsustainably high losses of managed A. mellifera honeybee colonies in many regions of the world. Future mitigation efforts should concentrate on developing sustainable agro-ecosystem management schemes that incorporate reduced use of neonicotinoids and sustainable solutions for V. destructor mites

Reproduction of parasitic mites <i>Varroa destructor</i> in original and new honeybee hosts.

The ectoparasitic mite, &lt;i&gt;Varroa destructor&lt;/i&gt; , shifted host from the eastern honeybee, &lt;i&gt;Apis cerana&lt;/i&gt; , to the western honeybee, &lt;i&gt;Apis mellifera&lt;/i&gt; . Whereas the original host survives infestations by this parasite, they are lethal to colonies of its new host. Here, we investigated a population of &lt;i&gt;A. cerana&lt;/i&gt; naturally infested by the &lt;i&gt;V. destructor&lt;/i&gt; Korea haplotype that gave rise to the globally invasive mite lineage. Our aim was to better characterize traits that allow for the survival of the original host to infestations by this particular mite haplotype. A known major trait of resistance is the lack of mite reproduction on worker brood in &lt;i&gt;A. cerana&lt;/i&gt; . We show that this trait is neither due to a lack of host attractiveness nor of reproduction initiation by the parasite. However, successful mite reproduction was prevented by abnormal host development. Adult &lt;i&gt;A. cerana&lt;/i&gt; workers recognized this state and removed hosts and parasites, which greatly affected the fitness of the parasite. These results confirm and complete previous observations of brood susceptibility to infestation in other honeybee host populations, provide new insights into the coevolution between hosts and parasites in this system, and may contribute to mitigating the large-scale colony losses of &lt;i&gt;A. mellifera&lt;/i&gt; due to &lt;i&gt;V. destructor&lt;/i&gt;

Novel mutations in the voltage-gated sodium channel of pyrethroid-resistant Varroa destructor populations from the Southeastern USA

The parasitic mite Varroa destructor has a significant worldwide impact on bee colony health. In the absence of control measures, parasitized colonies invariably collapse within 3 years. The synthetic pyrethroids tau-fluvalinate and flumethrin have proven very effective at managing this mite within apiaries, but intensive control programs based mainly on one active ingredient have led to many reports of pyrethroid resistance. In Europe, a modification of leucine to valine at position 925 (L925V) of the V. destructor voltage-gated sodium channel was correlated with resistance, the mutation being found at high frequency exclusively in hives with a recent history of pyrethroid treatment. Here, we identify two novel mutations, L925M and L925I, in tau-fluvalinate resistant V. destructor collected at seven sites across Florida and Georgia in the Southeastern region of the USA. Using a multiplexed TaqMan® allelic discrimination assay, these mutations were found to be present in 98% of the mites surviving tau-fluvalinate treatment. The mutations were also found in 45% of the non-treated mites, suggesting a high potential for resistance evolution if selection pressure is applied. The results from a more extensive monitoring programme, using the Taqman® assay described here, would clearly help beekeepers with their decision making as to when to include or exclude pyrethroid control products and thereby facilitate more effective mite management programmes