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

Abstract

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.

Injection of seminal fluid into the hemocoel of honey bee queens (Apis mellifera) can stimulate post-mating changes

“…forming a retinue around the queen is associated with the maturation of a queen's pheromone profile and is a proxy of reproductive health 114 . SF and SE queens elicited greater worker retinue responses as compared to Fig.…”

Factors affecting the reproductive health of honey bee (Apis mellifera) drones—a review

“…In the annual cycle of a typical colony, drone production occurs 3 to 4 weeks before the production of new queens at the onset of the reproductive season, in a strategy presumed to maximize the access of sexually mature drones to virgin queens from nearby colonies during swarming (Page 1981). Unlike drones, which only mate once, honey bee queens exhibit extreme polyandry, mating with an average of 12 to 14 drones (Estoup 1995;Tarpy and Page 2000;Rhodes 2002;Abdelkader et al 2014), although extreme queen matings with 50 or more drones have been recorded (Palmer and Oldroyd 2000;Koeniger et al 2005a, reviewed in Amiri et al 2017Brutscher et al 2019).…”

Histopathological Findings in Testes from Apparently Healthy Drones of Apis mellifera ligustica

“…The stressors mentioned above are able to directly or indirectly have pathological effects on the reproductive system of honeybees, impairing their fertility and often diminishing the number of future offspring that should perpetuate the species [7][8][9]. To date, many studies have focused on alterations of queen fertility, as outputs, such as low egg deposition or a high prevalence of drone brood, are easily recognizable in hives [10]. On the contrary, hypofertility of drones is often subclinical and therefore less studied, but, as the reproductive activity is strictly connected to the success of mating, all the elements that could invalidate drones' fertility, could consequently threaten colony fitness [11].…”

“…The reproductive process in honeybees shows unique features as queens only mate in the early stages of their life with multiple drones and acquire on that occasion the whole amount of spermatozoa that will be stored in the spermatheca and used during their whole life [14]. Therefore, drone fertility is strictly connected to the queen's reproductive capacity as mating with unfit drones, which are not able to produce high-quality fertile semen, could lead to queen failure, which occurs when queens stop efficient egg laying or start laying haploid male eggs [10]. Queen failure causes queen replacement by colony workers or by beekeepers, with a consequent increase in production time and costs [15].…”