A Varroa destructor protein atlas reveals molecular underpinnings of developmental transitions and sexual differentiation*

Varroa destructor is the most economically damaging honey bee pest, weakening colonies by simultaneously parasitizing bees and transmitting harmful viruses. Despite these impacts on honey bee health, surprisingly little is known about its fundamental molecular biology. Here, we present a Varroa protein atlas crossing all major developmental stages (egg, protonymph, deutonymph, and adult) for both male and female mites as a web-based interactive tool (http://foster.nce.ubc.ca/varroa/index.html). We used intensity-based label-free quantitation to find 1,433 differentially expressed proteins across developmental stages. Enzymes for processing carbohydrates and amino acids were among many of these differences as well as proteins involved in cuticle formation. Lipid transport involving vitellogenin was the most significantly enriched biological process in the foundress (reproductive female) and young mites. In addition, we found that 101 proteins were sexually regulated and functional enrichment analysis suggests that chromatin remodeling may be a key feature of sex determination. In a proteogenomic effort, we identified 519 protein-coding regions, 301 of which were supported by two or more peptides and 169 of which were differentially expressed. Overall, this work provides a first-of-its-kind interrogation of the patterns of protein expression that govern the Varroa life cycle and the tools we have developed will support further research on this threatening honey bee pest.