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Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.)

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Abstract

Honeybee queens (Apis mellifera) show extreme levels of polyandry, but the evolutionary mechanisms underlying this behaviour are still unclear. The “sperm-limitation hypothesis”, which assumes that high levels of polyandry are essential to get a lifetime sperm supply for large and long-lived colonies, has been widely disregarded for honeybees because the semen of a single male is, in principle, sufficient to fill the spermatheca of a queen. However, the inefficient post-mating sperm transfer from the queen’s lateral oviducts into the spermatheca requires multiple matings to ensure an adequate spermatheca filling. Males of the African honeybee subspecies A. m. capensis have fewer sperm than males of the European subspecies A. m. carnica. Thus, given that sperm limitation is a cause for the evolution of multiple mating in A. mellifera, we would expect A. m. capensis queens to have higher mating frequencies than A. m. carnica. Here we show that A. m. capensis queens indeed exhibit significantly higher mating frequencies than queens of A. m. carnica, both in their native ranges and in an experiment on a North Sea island under the same environmental conditions. We conclude that honeybee queens try to achieve a minimum number of matings on their mating flights to ensure a sufficient lifetime sperm supply. It thus seems premature to reject the sperm-limitation hypothesis as a concept explaining the evolution of extreme polyandry in honeybees.

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Acknowledgements

We wish to thank N. Koeniger and S. Fuchs for providing the A. m. capensis queens for the experiments on the island of Neuwerk. Appreciation is also expressed to S. Härtel for the A. m. capensis samples from the Western Cape, and to K. Heßler and P. Leibe for technical assistance. Financial support was granted by the EU BABE network (F.B.K., R.F.A.M.) and the DFG (P.N., R.F.A.M.). All experiments and beekeeping complied with the laws of Germany.

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Correspondence to F. B. Kraus.

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Kraus, F.B., Neumann, P., van Praagh, J. et al. Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 55, 494–501 (2004). https://doi.org/10.1007/s00265-003-0706-0

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