Morphological and metabolic adaptations facilitate rapid ovarian development and reproduction in female Varroa destructor

Histologic study of female Varroa destructor mites revealed morphological adaptations of the internal body plan that facilitate rapid feeding and transport of ingested lipoproteins via the lyrate organ to developing oocytes, leading to enormous oocyte growth and early oviposition. Histological images revealed a powerful sucking pharynx, employing 11 alternating dilator and constrictor muscles and the esophagus extending through the synganglion to the multilobed midgut. In fed mites, the midgut epithelial cells were observed filled with innumerable globular spheroids replete with lipoproteins, both saturated and polyunsaturated lipids for intracellular digestion. Varroa mites have a specialized organ, the bilobed lyrate organ adjacent to the midgut with close cell to cell linkages that form a syncytium. Nutrients taken up (mostly) from honey bee fat body are transcytosed rapidly from the midgut epithelial cells via the lyrate organ to elongated nurse cells in the adjacent ovary. The nurse cells align closely with rapidly expanding oocytes to nourish these cells and enhance their growth. Evidence from western blots, histochemical stains, MS/MS mass spectrometry and protein sequence alignments support the hypothesis that Varroa mites enhance their exceptionally rapid reproductive success by imbibing honey bee vitellogenin, apolipoproteins and other high molecular weight lipoproteins from their bee hosts. Honey bee proteins transferred to mite eggs constituted 24.7% of the total protein composition of the mite eggs. This novel form of nutritional support of rapid reproduction in a honey bee ectoparasite was named Kleptotrancytosis.