Spermatozoa capacitation in female Varroa destructor and its influence on the timing and success of female reproduction

Abstract

Mating of Varroa destructor takes place inside the sealed honey bee brood cell. During copulation, male mites transfer the spermatozoa into the genital openings of the females. Before the fertilization of female germ cells, the transferred spermatozoa have to pass through a final maturation process inside the genital tract of the female, the so-called capacitation. We here describe for the first time the morphological changes and chronological sequence of spermatozoa capacitation within female V. destructor. We have defined seven distinct stages of spermatozoa during the process of capacitation and have shown that it takes about 5 days from mating to the occurrence of spermatozoa ready for fertilization. This might explain the results of an additional experiment where we could show that freshly mated daughter mites need a phoretic phase on bees before their first reproduction cycle. The transfer of non-capacitated spermatozoa from male V. destructor and the resulting long capacitation period within the female mites seems to be a consequence of an adaptive pressure for the male mites to inseminate several daughter mites within the short time span inside the sealed honey bee brood cell.

Feeding by Tropilaelaps mercedesae on pre- and post-capped brood increases damage to Apis mellifera colonies

“…Whether or not tropilaelaps mites are truly phoretic on adult honey bees has not been studied although they appeared to be feeding on soft membranes of the wing axillaries 26 . In general, phoresy on adult honey bees is important in transporting mites to a new host or location or to meet the maturation process of spermatozoa as observed in varroa mites 27 . For tropilaelaps mites, phoresy is not required for successful reproduction 5 .…”

Reproductive parameters of female Varroa destructor and the impact of mating in worker brood of Apis mellifera

“…A cover glass was put on the dissected genital tract; then, it was analyzed under a VWR TR 500 light microscope (magnification 100-400). Spermatozoa were counted, and stages were diagnosed according to Häußermann et al (2016). The pictures were taken with a Canon EOS 60 D camera.…”

“…These spermatozoa are stored inside the spermatheca of female mites and have to undergo a further maturation process, the socalled capacitation, before being able to fertilize oocytes (Alberti and Hänel 1986). During capacitation, a spermatozoon drastically changes its cell shape from roundish to fusiform taking about 5 days (Häußermann et al 2016). Only adult daughter mites are able to survive outside the brood cell in contrast to younger and more sensitive stages like protonymphs and deutonymphs.…”

<em>Varroa destructor</em>: A Complex Parasite, Crippling Honey bees Worldwide

“…Under laboratory conditions, a female mite can have up to seven reproductive cycles during her lifetime and lay up to 30 eggs [32]. At the time she first matures, she receives 30-40 spermatophores via multiple matings with the male(s) in the cell, which she stores and uses during her lifespan [33]. In A. mellifera worker brood, a foundress with seven reproductive cycles would theoretically produce ~ 5-10 mature daughters, or ~ 10-17 mature daughters in drone brood.…”

“…When a parasitized honey bee emerges from its cell, it carries the mature female mites (mother and daughters). The daughters frequently switch to a nurse-aged bee [11] to activate their ovaries, allow the spermatophores to mature [33], and feed on adult bees. It was long believed that varroa was a tick-like parasite, feeding on hemolymph.…”