Histological atlas of the internal anatomy of female varroa destructor mites in relation to feeding and reproduction

Authors: SONENSHINE, DANIEL - Old Dominion University; POSADA-FLOREZ, FRANCISCO - Non ARS Employee; LAUDIER, DAMIEN - Non ARS Employee; GULBRONSON, CONNOR - Indiana University; RAMSEY, SAMUEL - Orise Fellow; Cook, Steven

Submitted to: Annals of the Entomological Society of America
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/27/2021
Publication Date: 12/18/2021
Citation: Sonenshine, D.E., Posada-Florez, F., Laudier, D., Gulbronson, C.J., Ramsey, S., Cook, S.C. 2021. Histological atlas of the internal anatomy of female varroa destructor mites in relation to feeding and reproduction. Annals of the Entomological Society of America. 115(2):163-193. https://doi.org/10.1093/aesa/saab043.
DOI: https://doi.org/10.1093/aesa/saab043

Interpretive Summary: Varroa destructor mites are harmful ectoparasites of Apis mellifera honey bees. These mites have evolved physical and physiological adaptations that might facilitate their nutrient acquisition and rapid reproduction. In this study, histological methods and histochemical staining are employed to explore these features of Varroa mites. Numerous images are produced from coronal, sagittal and transverse oriented stained sections that reveal the body plan. These images are inspected and differences between the status of selected internal organs related to feeding and reproduction are compared between starved and recently fed female mites. Varroa mites imbibe fluids using a specialized gnathosoma (mouthparts) together with a powerful sucking pharynx having ~11 alternating dialator and constructor muscles. The midgut epithelial cells of fed mites are replete with globular structures filled with lipoproteins, including polyunsaturated lipids, imbibed from their host honey bees. In contrast, the midgut cells of starved mites is devoid of these nutrient-filled globules. The lyrate organ, which is associated with both feeding and reproduction is featured prominently in histological sections of fed females. The bilobed lyrate orgain lies adjacent to the midgut on one side and the ovary on the other appears to have very close cell-cell junctions forming a syncytium. The ovary of fed mites contains at least enormously enlarged ovum (egg), and several smaller, less developed oocytes, and numerous elongated nurse cells extending from the lyrate organ to the ova. Selective staining suggests rapid incorporation of lipids, including both neutral and polyunsaturated lipids and lipoproteins imbibed from hosts. Also evident near the ovary of fed mites is the seminal receptical (spermatheca) filled will elongated, fully matured sperm cells. The fresh insights provided by this manuscript will help clarify our understanding of the feeding and reproduction of these harmful ectoparasites.

Technical Abstract: The internal anatomy of the female of the mite, Varroa destructor, a deadly parasite of the honey bee Apis mellifera, is described using histological methods and staining with haematoxylin-eosin (H&E) and various other histochemical stains. Numerous images are viewed from sections collected in the coronal, sagittal and transverse planes that reveal the internal body plan. Differences between the status of selected internal organs, e.g., the midgut and ovary, in starved versus recently fed mites are compared. The gnathosoma is revealed comprising the powerful sucking phar ynx with ~ 11 alternating dilator and constrictor muscles, the chelicerae, cheliceral retractors, and the salivary ducts and salivarium. Posterior to the gnathosoma, in the podosomal body region, the remarkably large (400 µM long x 260 µM high) synganglion is shown, with the four unbranched pedal nerves, an opisthosomal nerve and other nerves and associated ganglia. The esophagus is shown in the center of the synganglial neuropile, between the supraesophageal and subesophageal regions. Posterior to the synganglion, the midgut and adjacent diverticulae in starved mites is found mostly empty of food particles. In contrast, the epithelial cells lining the midgut and several diverticulae of freshly fed mites are filled with innumerable globular structures of many different sizes imbibed from the host bees. The lumen is filled with amorphous fluids. The midgut contents of these fed mites were shown by selective histochemical staining to consist of lipoproteins, including polyunsaturated lipids, while the lumen is filled mostly with saturated lipids or other unidentified nutrients also imbibed from the host bees. In the opisthosomal body region, the large lyrate organ and adjacent ovary are revealed, mostly prominently in the freshly fed female. The bilobed lyrate organ lies adjacent to the midgut on one side and the ovary on the opposite side, with very close cell to cell linkages with the ovary that appear to form a syncytium. The ovary of the fed females contains at least one enormously enlarged ovum, several smaller but expanding ova, and numerous elongated nurse cells extending from the lyrate organ to these ova. Selective staining, especially with toluidine blue dye selective for lipoproteins and osmium tetroxide suggests rapid incorporation of lipids, including both neutral and polyunsaturated lipids and lipoproteins recently imbibed from host bees. Also evident near the ovary in fed females is the seminal receptacle (spermatheca) filled with elongated, fully capacitated spermatozoa. The histological & histochemical findings reported in this study provide a fresh insight into the body structure, nutrition, and reproductive activity of the female of this important honey bee parasite and disease vector.