Seasonal cycle of inbreeding and recombination of the parasitic mite Varroa destructor in honeybee colonies and its implications for the selection of acaricide resistance

Varroa destructor is the most devastating parasite of the Western honeybee, Apis mellifera. In the light of the arm race opposing the host and its parasite, the population dynamics and genetic diversity of these organisms are key parameters. However, the life cycle of V. destructor is characterized by extreme inbreeding due to full sibling mating in the host brood cells. We here present an equation reflecting the evolution of inbreeding in such a clonal system, and compare our predictions with empirical data based on the analysis of seven microsatellite markers. This comparison revealed that the mites perform essentially incestuous mating in the beginning of the brood season. However, this pattern changes with the development of mite infestation. Despite the fact that the overall level of genetic diversity of the mites remained low through the season, multiple inbred lineages were identified in the mites we sampled in June. As a response to the decrease of brood availability and the increase of the parasite population in parallel in the colonies, these lineages recombined towards the end of the season as mites co-infest brood cells. Our results suggest that the ratio of the number of mite per brood cell in the colony determines the genetic structure of the populations of V. destructor. This intracolonial population dynamics has great relevance for the selection of acaricide resistance in V. destructor. If chemical treatments occur before the recombination phase, inbreeding will greatly enhance the fixation of resistance alleles at the colony level.Bayer AGhttp://www.elsevier.com/locate/meegid2018-06-30hb2017Zoology and Entomolog

Population genetics for insect conservation and control

Abstract Insects are essential not only for ecosystem functioning and food security but also comprise some of the world's most destructive invasive species. Therefore, both insect declines and invasions raise major conservation concerns globally and call for respective conservation or mitigation measures. However, studies of insects are hampered by intrinsic biological features of these organisms, which include extreme population fluctuations, a huge diversity of ecological strategies, and common cryptic species. Population genetics provides a large toolkit to adequately accommodate those features, thereby enabling researchers to inform and monitor the efficacy of conservation and mitigation programs. Here, we provide an overview of the molecular and analytical methods that are relevant to insect conservation or mitigation and highlight the challenges involved in their implementation. We detail how and why temporal changes in genetic diversity, population structure and migration, and the genetic basis of adaptation should be taken into account to inform insect management programs. Finally, we review the barriers to the broad adoption of population genetics in insect research and provide guidelines to facilitate the use of these methods by stakeholders. Overall, this review provides theoretical and practical guidelines for implementing population genetics in both insect conservation and control

Association of Varroa destructor females in multiply infested cells of the honeybee Apis mellifera

The genetic diversity of Varroa destructor (Anderson & Trueman) is limited outside its natural range due to population bottlenecks and its propensity to inbreed. In light of the arms race between V. destructor and its honeybee (Apis mellifera L.) host, any mechanism enhancing population admixture of the mite may be favored. One way that admixture can occur is when two genetically dissimilar mites coinvade a brood cell, with the progeny of the foundresses admixing. We determined the relatedness of 393 pairs of V. destructor foundresses, each pair collected from a single bee brood cell (n = five colonies). We used six microsatellites to identify the genotypes of mites coinvading a cell and calculated the frequency of pairs with different or the same genotypes. We found no deviation from random coinvasion, but the frequency of cells infested by mites with different genotypes was high. This rate of recombination, coupled with a high transmission rate of mites, homogenized the allelic pool of mites within the apiary.Table S1 Observed and expected genotype association. Matrices showing the number of mites we observed (top) and expected (bottom) for each of the 10 most prevalent genotypes combinations (G1–G10) and combinations with other genotypes (Others). F represents the overall frequency of each genotype sampled in the colonies. The F was used to calculate the expected frequencies of each genotype association and overall. Recombinant genotypes are italicized.Fig. S1 Distribution of the five main genotypes (G) among sampled Varroa destructor in the five Apis mellifera colonies. The percentage of the six main genotypes (dark to light blue, from the most frequent to the least common) and the other 68 genotypes (grouped together in white) in the each of the five sampled colonies.Bayer Animal Healthhttps://onlinelibrary.wiley.com/journal/17447917hj2020Zoology and Entomolog

Population genetics of ectoparasitic mites suggest arms race with honeybee hosts

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

Chito-Oligosaccharide and Propolis Extract of Stingless Bees Reduce the Infection Load of <i>Nosema ceranae</i> in <i>Apis dorsata</i> (Hymenoptera: Apidae)

Nosema ceranae is a microsporidian that infects Apis species. Recently, natural compounds have been proposed to control nosemosis and reduce its transmission among honey bees. We investigated how ethanolic extract of Tetrigona apicalis’s propolis and chito-oligosaccharide (COS) impact the health of N. ceranae-infected Apis dorsata workers. Nosema ceranae spores were extracted from the guts of A. florea workers and fed 106 spores dissolved in 2 µL 50% (w/v) sucrose solution to A. dorsata individually. These bees were then fed a treatment consisting either of 0% or 50% propolis extracts or 0 ppm to 0.5 ppm COS. We found that propolis and COS significantly increased the number of surviving bees and lowered the infection ratio and spore loads of N. ceranae-infected bees 14 days post-infection. Our results suggest that propolis extract and COS could be possible alternative treatments to reduce N. ceranae infection in A. dorsata. Moreover, N. ceranae isolated from A. florea can damage the ventricular cells of A. dorsata, thereby lowering its survival. Our findings highlight the importance of considering N. ceranae infections and using alternative treatments at the community level where other honey bee species can act as a reservoir and readily transmit the pathogen among the honey bee species

Extensive population admixture on drone congregation areas of the giant honeybee, Apis dorsata (Fabricius, 1793)

Abstract The giant honeybee Apis dorsata often forms dense colony aggregations which can include up to 200 often closely related nests in the same location, setting the stage for inbred matings. Yet, like in all other Apis species, A. dorsata queens mate in mid‐air on lek like drone congregation areas (DCAs) where large numbers of males gather in flight. We here report how the drone composition of A. dorsata DCAs facilitates outbreeding, taking into the account both spatial (three DCAs) and temporal (subsequent sampling days) dynamics. We compared the drones’ genotypes at ten microsatellite DNA markers with those of the queen genotypes of six drone‐producing colonies located close to the DCAs (Tenom, Sabah, Malaysia). None of 430 sampled drones originated from any of these nearby colonies. Moreover, we estimated that 141 unidentified colonies were contributing to the three DCAs. Most of these colonies were participating multiple times in the different locations and/or during the consecutive days of sampling. The drones sampled in the DCAs could be attributed to six subpopulations. These were all admixed in all DCA samples, increasing the effective population size an order of magnitude and preventing matings between potentially related queens and drones

Host Specificity in the Honeybee Parasitic Mite, <i>Varroa spp</i>. in <i>Apis mellifera</i> and <i>Apis cerana</i>

<div><p>The ectoparasitic mite <i>Varroa destructor</i> is a major global threat to the Western honeybee <i>Apis mellifera</i>. This mite was originally a parasite of <i>A</i>. <i>cerana</i> in Asia but managed to spill over into colonies of <i>A</i>. <i>mellifera</i> which had been introduced to this continent for honey production. To date, only two almost clonal types of <i>V</i>. <i>destructor</i> from Korea and Japan have been detected in <i>A</i>. <i>mellifera</i> colonies. However, since both <i>A</i>. <i>mellifera</i> and <i>A</i>. <i>cerana</i> colonies are kept in close proximity throughout Asia, not only new spill overs but also spill backs of highly virulent types may be possible, with unpredictable consequences for both honeybee species. We studied the dispersal and hybridisation potential of <i>Varroa</i> from sympatric colonies of the two hosts in Northern Vietnam and the Philippines using mitochondrial and microsatellite DNA markers. We found a very distinct mtDNA haplotype equally invading both <i>A</i>. <i>mellifera</i> and <i>A</i>. <i>cerana</i> in the Philippines. In contrast, we observed a complete reproductive isolation of various Vietnamese <i>Varroa</i> populations in <i>A</i>. <i>mellifera</i> and <i>A</i>. <i>cerana</i> colonies even if kept in the same apiaries. In light of this variance in host specificity, the adaptation of the mite to its hosts seems to have generated much more genetic diversity than previously recognised and the <i>Varroa</i> species complex may include substantial cryptic speciation.</p></div

Principal Component Analysis.

<p>Genetic clustering of the <i>Varroa</i> mites based on their genotype at six microsatellite markers. The <i>Varroa</i> mites were sampled in <i>A</i>. <i>cerana</i> (<b>Vc</b>) and <i>A</i>. <i>mellifera</i> (<b>Vm</b>) colonies in the Philippines and Vietnam. The genotypes of the mites sampled in Los Banos (<b>LB</b>) are shown in green (groups 1 and 2). The mites from Lipa city (<b>LC</b>, group 3) and sampled in <i>A</i>. <i>mellifera</i> from Dien Bien (<b>DB</b>, group 5) and Son La (<b>SL</b>, group 7) are represented in orange. The mites from <i>A</i>. <i>cerana</i> colonies located in Vietnam from Dien Bien (<b>DB</b>, group 4), Son La (<b>SL</b>, group 6) and Cat Ba (<b>CB</b>, group 8) are represented in blue. Each dot represents a distinct individual, and each inertia ellipsoid shows the population’s prediction ellipses for each group.</p

Overall information on the microsatellite loci used.

<p>For each of the six microsatellite markers used, the name of the locus (<b>Locus</b>), the overall number of Alleles (<b>N</b>_<b>A</b>) and the overall Allelic Richness (<b>R</b>) are represented.</p><p>Overall information on the microsatellite loci used.</p