Abstract
BackgroundThe parasite Varroa destructor represents a significant threat to honeybee colonies. Indeed, development of Varroa infestation within colonies, if left untreated, often leads to the death of the colony. Although its impact on bees has been extensively studied, less is known about its biology and the functional processes governing its adult life cycle and adaptation to its host. We therefore developed a full life cycle transcriptomic catalogue in adult Varroa females and included pairwise comparisons with males, artificially-reared and non-reproducing females (10 life cycle stages and conditions in total).ResultsExtensive remodeling of the Varroa transcriptome was observed, with an upregulation of energetic and chitin metabolic processes during the initial and final phases of the life cycle (e.g. phoretic and post-oviposition stages), whereas during reproductive stages in brood cells genes showing functions related to transcriptional regulation were overexpressed. Several neurotransmitter and neuropeptide receptors involved in behavioural regulation, as well as active compounds of salivary glands, were also expressed at a higher level outside the reproductive stages. No difference was detected between artificially-reared phoretic females and their counterparts in colonies, or between females who failed to reproduce and females who successfully reproduced, indicating that phoretic individuals can be reared outside host colonies without impacting their physiology and that mechanisms underlying reproductive failure occur before oogenesis.ConclusionsWe discuss how these new findings reveal the remarkable adaptation of Varroa to its host biology and notably to the switch from living on adults to reproducing in sealed brood cells. By spanning the entire adult life cycle, our work captures the dynamic changes in the parasite gene expression and serves as a unique resource for deciphering Varroa biology and identifying new targets for mite control.
Highlights
The parasite Varroa destructor represents a significant threat to honeybee colonies
To study the underlying molecular mechanisms governing the Varroa destructor adult life cycle, we carried out transcriptomic profiling of seven stages (Fig. 1) described in the Methods section and comprising: young mites (Young, collected from Day 8 of pupal development (P8) to day 9 of pupal development (P9) cells), phoretic mites (Phor, collected on adult bees), arresting mites (Arrest, collected in unsealed Day 5 of larval development (L5) brood cells), pre-laying mites (Pre-lay, collected from sealed brood cells containing moving larva), laying mites (Laying, collected from sealed brood cells containing pre-pupae), post-laying mites (Post-lay, collected from capped brood cells containing purple-eye and white-body pupae Day 5 of pupal development (P5)), and emerging mites (Emerg, collected from P8 to P9 cells)
We sampled non-reproducing mites (NR, collected from P5 brood cells, but without offspring), males (Male, collected from P8 to P9 cells), and phoretic mites artificially reared in cages with adult bees (Cage)
Summary
The parasite Varroa destructor represents a significant threat to honeybee colonies. development of Varroa infestation within colonies, if left untreated, often leads to the death of the colony. The Varroa mite is an ectoparasite of both adult and immature bees (brood), which can lead to the rapid death of infected colonies if left untreated [3]. Varroa relies entirely on its host for its own survival and propagation, with female adult life stages showing two distinct phases: the phoretic phase spent on adult bees, and the reproductive phase during which the mites reproduce in the brood [1, 4]. During the time spent on bees, mites feed on hemolymph and often hide between the abdominal sternites of bees. They start the reproductive phase by invading a brood cell containing a larva, shortly before the cell is capped. The male mates with his sisters, which leave the brood cell with their mother upon adult bee emergence and start a new phoretic phase
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