Honey Bee Colonies Headed by Hyperpolyandrous Queens Have Improved Brood Rearing Efficiency and Lower Infestation Rates of Parasitic Varroa Mites.

Keith S Delaplane,Stéphane Pietravalle,Mike A Brown,Giles E Budge,Olav Rueppell

doi:10.1371/journal.pone.0142985

Keith S Delaplane, Stéphane Pietravalle + Show 3 more

Open Access

https://doi.org/10.1371/journal.pone.0142985

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Abstract

A honey bee queen mates on wing with an average of 12 males and stores their sperm to produce progeny of mixed paternity. The degree of a queen’s polyandry is positively associated with measures of her colony’s fitness, and observed distributions of mating number are evolutionary optima balancing risks of mating flights against benefits to the colony. Effective mating numbers as high as 40 have been documented, begging the question of the upper bounds of this behavior that can be expected to confer colony benefit. In this study we used instrumental insemination to create three classes of queens with exaggerated range of polyandry– 15, 30, or 60 drones. Colonies headed by queens inseminated with 30 or 60 drones produced more brood per bee and had a lower proportion of samples positive for Varroa destructor mites than colonies whose queens were inseminated with 15 drones, suggesting benefits of polyandry at rates higher than those normally obtaining in nature. Our results are consistent with two hypotheses that posit conditions that reward such high expressions of polyandry: (1) a queen may mate with many males in order to promote beneficial non-additive genetic interactions among subfamilies, and (2) a queen may mate with many males in order to capture a large number of rare alleles that regulate resistance to pathogens and parasites in a breeding population. Our results are unique for identifying the highest levels of polyandry yet detected that confer colony-level benefit and for showing a benefit of polyandry in particular toward the parasitic mite V. destructor.

Highlights

The honey bee queen (Apis mellifera L) mates with many males, stores their sperm in her spermatheca, and thereafter uses the sperm to fertilize her life’s output of eggs
Our results add to a growing base of evidence showing adaptive benefits of polyandry to the honey bee colony
Among colonies whose queens were inseminated with 15, 30, or 60 drones we found significantly more brood per bee and a lower proportion of samples positive for Varroa mites in colonies whose queens were inseminated with 30 or 60 drones

Summary

Introduction

The honey bee queen (Apis mellifera L) mates with many males, stores their sperm in her spermatheca, and thereafter uses the sperm to fertilize her life’s output of eggs. Numerous hypotheses have been put forward to explain colony-level adaptive benefits of this behavior: Polyandry (1) provides for beneficial non-additive interactions among subfamilies resulting in a more resilient colony [3,4], (2) increases environmental stability by “averaging out” extreme phenotypes [5], (3) reduces variance in the production of diploid males (which are sterile and normally killed by workers) [6], and (4) increases genetic variation within colonies, reducing the likelihood that parasites or pathogens will decrease worker populations to a point that jeopardizes colony survival and reproduction [7]. In the context of genetic resistance to novel parasites, the rare allele model may be of key importance and begs the question of the constraints limiting higher mating numbers in nature These constraints are thought to be risks to the queen from sexually-transmitted diseases [22] and hazards associated with repeated mating flights. Given the ongoing honey bee health crisis, it is important to examine the extent to which benefits of polyandry can be delivered to managed systems

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Discussion