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

Beaurepaire, Alexis; Krieger, Klemens J.; Moritz, Robin F. A.

doi:10.1016/j.meegid.2017.02.011

Cited by 70 publications

(87 citation statements)

References 39 publications

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“…This is particularly the case for the haploid drone offspring, which inherit their entire genome from their diploid mother (Wilfert et al ., ). In comparison, the short reproductive cycle of Varroa combined with high levels of inbreeding (Beaurepaire et al ., ) could allow the parasite to evolve resistance to a single resistance pathway (González‐Cabrera et al ., ) before the host‐colony queen is replaced, potentially bringing new resistance alleles into the colony. However, the presence of multiple resistance loci in a host‐colony queen, with epistatic interactions between them, provides the potential for recombination to continually shift the haplotype frequencies of resistance traits in the drone offspring.…”

Section: Discussionmentioning

confidence: 99%

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

Conlon

Frey

Rosenkranz

et al. 2018

J of Evolutionary Biology

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The Red Queen hypothesis predicts that host-parasite coevolutionary dynamics can select for host resistance through increased genetic diversity, recombination and evolutionary rates. However, in haplodiploid organisms such as the honeybee (Apis mellifera), models suggest the selective pressure is weaker than in diploids. Haplodiploid sex determination, found in A. mellifera, can allow deleterious recessive alleles to persist in the population through the diploid sex with negative effects predominantly expressed in the haploid sex. To overcome these negative effects in haploid genomes, epistatic interactions have been hypothesized to play an important role. Here, we use the interaction between A. mellifera and the parasitic mite Varroa destructor to test epistasis in the expression of resistance, through the inhibition of parasite reproduction, in haploid drones. We find novel loci on three chromosomes which explain over 45% of the resistance phenotype. Two of these loci interact only additively, suggesting their expression is independent of each other, but both loci interact epistatically with the third locus. With drone offspring inheriting only one copy of the queen's chromosomes, the drones will only possess one of two queen alleles throughout the years-long lifetime of the honeybee colony. Varroa, in comparison, completes its highly inbred reproductive cycle in a matter of weeks, allowing it to rapidly evolve resistance. Faced with the rapidly evolving Varroa, a diversity of pathways and epistatic interactions for the inhibition of Varroa reproduction could therefore provide a selective advantage to the high levels of recombination seen in A. mellifera. This allows for the remixing of phenotypes despite a fixed queen genotype.

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Section: Discussionmentioning

confidence: 99%

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

Conlon

Frey

Rosenkranz

et al. 2018

J of Evolutionary Biology

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“…Although our results suggest that V. destructor foundresses do not actively influence exogamy by coinvading a brood cell with a foundress mite of the same or different genotype, the vast majority of the cells (83.21%) contained foundress mites with different genotypes. Even if male mites would mate at random and not discriminate between sisters and unrelated females, the level of heterozygosity in the colonies would rapidly increase in the coinfestation phase when the mite-to-brood ratio is high (Calis et al, 1999;Beaurepaire et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Finally, the distributions of the different genotypes in the five colonies were compared using a Kruskall-Wallis test. (2000); VjL3B2, Vj275, Vj295, and Vj296 from Solignac et al (2003); VD305, VD306, and VD307 from Cornman et al (2010); Vdes-03 and Vdes05-Vdes10 from Beaurepaire et al (2017).…”

Section: Microsatellite Dna Analysesmentioning

confidence: 99%

“…In the reproductive phase, a "foundress" mite (the mite invading the cell) will produce only one male and an average of 1.30-1.45 mature females when infesting worker cells, but close to double this amount when infesting drone cells (Martin, 1994(Martin, , 1995. The reproduction of V. destructor is therefore highly dependent on brood availability in its host colony (Beaurepaire et al, 2017). When there are more brood cells than mites in the colony, the cells typically will be infested by a single foundress mite (single infestation).…”

Section: Introductionmentioning

confidence: 99%

“…However, as the infestation expands and the ratio of mites-to-brood cells increases, cell invasion by multiple foundresses ("multiple infestations") becomes more frequent and the progeny from different mites may admix. This differential mating dynamic essentially shapes the genetic structure of the mite population with a dramatic reduction of heterozygosity in the mite populations in the beginning of the season and an increase of recombination toward the end of the brood season (Beaurepaire et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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

2017

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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.

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Selection for outbreeding in Varroa parasitising resistant honey bee (Apis mellifera) colonies

Conlon

Kastally

Kardell

et al. 2020

Ecology and Evolution

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Parasitism is expected to select for counter‐adaptations in the host: driving a coevolutionary arms race. However, human interference between honey bees (Apis mellifera) and Varroa mites removes the effect of natural selection and restricts the evolution of host counter‐adaptations. With full‐sibling mating common among Varroa, this can rapidly select for virulent, highly inbred, Varroa populations. We investigated how the evolution of host resistance could affect the infesting population of Varroa mites.We screened a Varroa‐resistant honey bee population near Toulouse, France, for a Varroa resistance trait: the inhibition of Varroa's reproduction in drone pupae. We then genotyped Varroa which had co‐infested a cell using microsatellites. Across all resistant honey bee colonies, Varroa's reproductive success was significantly higher in co‐infested cells but the distribution of Varroa between singly and multiply infested cells was not different from random. While there was a trend for increased reproductive success when Varroa of differing haplotypes co‐infested a cell, this was not significant. This suggests local mate competition, through the presence of another Varroa foundress in a pupal cell, may be enough to help Varroa overcome host resistance traits; with a critical mass of infesting Varroa overwhelming host resistance. However, the fitness trade‐offs associated with preferentially co‐infesting cells may be too high for Varroa to evolve a mechanism to identify already‐infested cells. The increased reproductive success of Varroa when co‐infesting resistant pupal cells may act as a release valve on the selective pressure for the evolution of counter resistance traits: helping to maintain a stable host–parasite relationship.

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

Cited by 70 publications

References 39 publications

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones

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

Selection for outbreeding in Varroa parasitising resistant honey bee (Apis mellifera) colonies

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