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.

Keywords: drones; honey bees; pathogens; queens; reproduction; seminal fluid.

Figure 1

Stressors impacting queen and drone fertility and their downstream effects on queen quality and post-mating changes and worker behavior and physiology. The small arrows inside of the boxes indicate an increase or decrease of queen post-mating changes or subsequent worker behavioral or physiological traits as observed during ideal natural conditions, but disruptions in male fertility may subsequently affect the intensity and manifestation of these phenotypes. Multiple stressors impact queen and drone fertility, including pathogens and parasites, such as Nosema spp. and Varroa destructor mites, which affect drone mating flight behavior and seminal fluid proteome composition. These and other drone mating factors, such as insemination volume and insemination fluid composition also impact queen fertility, which subsequently affect the behavior and physiology of workers. In turn, altered queen-worker interactions may affect colony level productivity and health.