Molecular, physiological and behavioral responses of honey bee (Apis mellifera) drones to infection with microsporidian parasites

Honey bees are major pollinators of agricultural and non-agricultural landscapes. In recent years, honey bee colonies have exhibited high annual losses and commercial beekeepers frequently report poor queen quality and queen failure as the primary causes. Honey bee colonies are highly vulnerable to compromised queen fertility, as each hive is headed by one reproductive queen. Queens mate with multiple drones (male bees) during a single mating period early in life in which they obtain enough spermatozoa to fertilize their eggs for the rest of their reproductive life span. The process of mating initiates numerous behavioral, physiological, and molecular changes that shape the fertility of the queen and her influence on the colony. For example, receipt of drone semen can modulate queen ovary activation, pheromone production, and subsequent worker retinue behavior. In addition, seminal fluid is a major component of semen that is primarily derived from drone accessory glands. It also contains a complex mixture of proteins such as proteases, antioxidants, and antimicrobial proteins. Seminal fluid proteins are essential for inducing post-mating changes in other insects such as Drosophila and thus they may also impact honey bee queen fertility and health. However, the specific molecules in semen and seminal fluid that initiate post-mating changes in queens are still unidentified. Herein, we summarize the mating biology of honey bees, the changes queens undergo during and after copulation, and the role of drone semen and seminal fluid in post-mating changes in queens. We then review the effects of seminal fluid proteins in insect reproduction and potential roles for honey bee drone seminal fluid proteins in queen reproduction and health. We finish by proposing future avenues of research. Further elucidating the role of drone fertility in queen reproductive health may contribute towards reducing colony losses and advancing honey bee stock development.

Section: Seminal Fluid Proteins and Their Potential Roles In Queenmentioning

confidence: 99%

Putative Drone Copulation Factors Regulating Honey Bee (Apis mellifera) Queen Reproduction and Health: A Review

Brutscher

Baer

Niño

2019

“…It is commonly accepted that the older forager bees in hives have the highest frequency and most intense infection [45,46,95,96], which is thought to provoke an acceleration of foraging behavior in bees infected by N. ceranae [32][33][34]58,97]. However, given the greater susceptibility of younger worker bees evident in this study, it is possible that various strategies may be employed in the super-organism to reduce contamination by Nosema spp.…”

Section: Discussionmentioning

confidence: 76%

Age and Method of Inoculation Influence the Infection of Worker Honey Bees (Apis mellifera) by Nosema ceranae

Urbieta-Magro

Higes

Meana

et al. 2019

The microsporidian parasite Nosema ceranae is a highly prevalent, global honey bee pathogen. Apis mellifera is considered to be a relatively recent host for this microsporidia, which raises questions as to how it affects its host’s physiology, behavior and longevity, both at the individual and colony level. As such, honey bees were inoculated with fresh purified spores of this pathogen, both individually (Group A) or collectively (Group B) and they were studied from 0 to 15 days post-emergence (p.e.) to evaluate the effect of bee age and the method of inoculation at 7 days post-infection. The level of infection was analyzed individually by qPCR by measuring the relative amount of the N. ceranae polar tubule protein 3 (PTP3) gene. The results show that the bee’s age and the method of infection directly influence parasite load, and thus, early disease development. Significant differences were found regarding bee age at the time of infection, whereby the youngest bees (new-born and 1 day p.e.) developed the highest parasite load, with this load decreasing dramatically in bees infected at 2 days p.e. before increasing again in bees infected at 3–4 days p.e. The parasite load in bees infected when older than 4 days p.e. diminished as they aged. When the age cohort data was pooled and grouped according to the method of infection, a significantly higher mean concentration and lower variation in N. ceranae infection was evident in Group A, indicating greater variation in experimental infection when spores were administered collectively to bees through their food. In summary, these data indicate that both biological and experimental factors should be taken into consideration when comparing data published in the literature.

“…For instance, essential oils of E. globolus at 10.0 mg/mL caused an irregular response in bees that were inoculated with DWV-A, although some cases were significant compared to non-inoculated bees. This irregular response could be associated with a saturation of the environment by the volatiles present in the essential oils, generating nonspecific stimulation [52]. It has been proposed that, when faced with a high concentration of stimulus, a nonspecific stimulation can be generated; on the other hand, exposure to low concentrations of the stimulus may not generate a complete stimulation of the antenna [52].…”

Section: Discussionmentioning

confidence: 99%

“…This irregular response could be associated with a saturation of the environment by the volatiles present in the essential oils, generating nonspecific stimulation [52]. It has been proposed that, when faced with a high concentration of stimulus, a nonspecific stimulation can be generated; on the other hand, exposure to low concentrations of the stimulus may not generate a complete stimulation of the antenna [52]. We observed that very low concentrations of the stimulus did not induce olfactory responses, although, exceptionally, 14-day-old bees inoculated with DWV-A and exposed to 0.01 mg/mL of M. piperita essential oil showed a significant decrease in the EAG response; bee age also coincided with a higher DWV-A load (1.0 × 10 11 copy number per bee) detected in the antennas (Figures 2A and 3).…”

Section: Discussionmentioning

confidence: 99%

Variant A of the Deformed Wings Virus Alters the Olfactory Sensitivity and the Expression of Odorant Binding Proteins on Antennas of Apis mellifera

Silva

Ceballos

Arismendi

et al. 2021

Insects have a highly sensitive sense of smell, allowing them to perform complex behaviors, such as foraging and peer recognition. Their sense of smell is based on the recognition of ligands and is mainly coordinated by odorant-binding proteins (OBPs). In Apis mellifera, behavior can be affected by different pathogens, including deformed wing virus (DWV) and its variants. In particular, it has been shown that variant A of DWV (DWV-A) is capable of altering the ultra-cellular structure associated with olfactory activity. In this study was evaluated olfactory sensitivity and the expression of OBP genes in honey bees inoculated with DWV-A. Electroantennographic analyses (EAG) were carried out to determine the olfactory sensitivity to the essential oils Eucalyptus globulus and Mentha piperita. The expression of nine antenna-specific OBP genes and DWV-A load in inoculated bees was also quantified by qPCR. We observed an inverse relationship between viral load and olfactory sensitivity and the expression of some OBP proteins. Thus, high viral loads reduced olfactory sensitivity to essential oils and the gene expression of the OBP2, OBP5, OBP11, and OBP12 proteins on the antennas of middle- and forager-age bees. These results suggest that DWV-A could have negative effects on the processes of aroma perception by worker bees, affecting their performance in tasks carried out in and outside the colony.