Honey Bee Health & Food Security
The honey bee is, arguably, the most famous insect on the planet. It has been associated with human populations for thousands of years and is a model for cooperation, collaboration and interaction within a complex society. Honey bees are eusocial insects: A single queen bee generates a colony of tens of thousands of daughters who work together to promote the health, stability and maintenance of the colony. These workers sacrifice their own reproduction and spend their days caring for their developing sisters, constructing honey comb, making and storing their own food (honey and bee bread), and communicating with one another about their local environment (through waggle dancing and chemical cues).
Fame aside, honey bees are the most economically important pollinators on Earth. Because they have wide-ranging tastes for pollen and nectar, and visit a large diversity of flowers, they increase the value of crops in the U.S. by $20 billion per year . In fact, pollination by insects produces one out of every three mouthfuls of food consumed globally  – a staggering statistic. This impressive number suggests that the health of our pollinators is closely tied to the security of the world’s food supply.
Given the importance of pollinators, both monetarily and agriculturally, colony losses in recent years are particularly alarming. The syndrome termed “Colony Collapse Disorder” (CCD) first received national attention in the late 2000s. Honey bee keepers reported losing between 20 to 60 percent of their hives to CCD . Bee keepers identify hives suffering from CCD because the worker populations are completely lost. They abandon the queen and the brood, never to be seen again. The cause of this mysterious syndrome has yet to be determined.
Although no single agent has been identified as directly causing CCD, the disorder seems to be correlated with multiple stresses on honey bees. These stresses include: pesticide use, agricultural practices (including transportation of hives around the country and antibiotic use), malnutrition, parasites and pathogens (such as the Varroa mite, Nosema and Israeli acute paralysis virus). Clearly, more research is needed to better understand what makes a honey bee colony susceptible to disease and to the syndrome. Conversely, if people can better understand what makes a healthy colony, they may be able to protect their hives from these stresses.
At the center of a healthy honey bee colony is the queen bee, which is responsible for all reproduction and generation of new hive members. Her highness lays more than one thousand eggs per day – an impressive number of offspring. The workers she lays are the result of mating during her first five days of life in what is termed her “nuptial flight.”
A queen is expected to mate with between 10 to 20 male drone bees during that flight and will store all the sperm she needs to maintain her colony for the rest of her life. This mating strategy (the promiscuous behavior of the honey bee queen) is rare among eusocial insects . Most queens mate with a single male and produce colonies whose close genetic relatedness is thought to foster cooperation .
This argument is based on the concept of kin selection – that organisms are more likely to care for and promote reproduction of close relatives compared to distant or unrelated conspecifics. Add to this phenomenon the genetic quirk of the honey bee – that males contain half the genetic material of females – and this means that honey bees with the same drone father will be highly related to each other (on average, 75 percent). For comparison, consider that a person and his/her full siblings would be, on average, 50 percent related. That means a honey bee worker is more related to her sister than she would be to her own offspring – the argument of kin selection seems to make sense.
However, this argument is turned on its head when one considers that the natural state is for the queen to mate with many different drones, creating a genetically diverse colony where worker honey bees with different fathers are 25 percent related to each other. The greater number of drones contributing to the colony, the more genetic diversity found within the colony. Given that genetic relatedness is thought to foster collaboration, why is the honey bee queen promiscuous? Researchers have been investigating the effects of genetic diversity in honey bees for many years and results unambiguously point to genetic diversity improving health and function of honey bee colonies [6-11].
At this point it is worth emphasizing that honey bees are an agricultural crop; they are not natural to North America and are heavily managed. When bee keepers order queens for the season from apiaries, these queens are, for the most part, artificially inseminated with drone sperm. The quality, quantity and diversity of the sperm used in the mating is, therefore, entirely under control of the queen breeder. In the past, commercially purchased queens in the U.S. have been found lacking . These queens were found to harbor a low quantity of sperm from a few drones – an alarming result. Recently, however, it seems that insemination practices are producing quality queens , perhaps because of the attention paid to this issue of colony genetic diversity.
Another complicating factor is that honey bees have been genetically selected for particular traits: disease resistance, mite tolerance, honey production, etc. Each of these selected strains of honey bee is a diversity bottleneck, a reduction in the pool of genetic material available to bee keepers and queen breeders. We do not fully understand what this decrease in genetic diversity means for colony health, but it cannot be positive. Inbreeding is known to increase the susceptibility of an entire population to disease, thus decreasing the ability of that population to withstand pathogen attacks and increasing the possibility of genetic disorders within a strain .
Many researchers are currently interested in the natural microbes associated with honey bees and what they may mean for honey bee health. This is because bacteria are everywhere, and the vast majority are not harmful; in fact, they are likely beneficial.
For example, the community of microbes that exists on and within human bodies outnumbers (by count) its own cells. This community, called “the human microbiome,” has co-evolved with people for millions of years  and is involved in helping them digest food [16,17], in protecting them from disease [18-20], in training their immune system  and can be used to prevent [18,21] and to treat disease (e.g., [22,23]). The popularity and efficacy of probiotics is a testament to the beneficial role these organisms play in human physiology. But what role might bacteria play in honey bee health and vitality?
Just like those found on human bodies, bacteria associated with honey bees may be helping them to acquire nutrients from their food and to protect them from disease. For instance, middle-aged workers (so called “food processors”) manipulate pollen that older foragers collect into a food product called “bee bread” by essentially regurgitating into pollen before storing it in comb. This mixture is allowed to mature for weeks before being consumed by the bees. It is as though the bees “know” that microbial processing of this important food is necessary as honey bees fed bee bread live longer than those fed raw pollen .
It is presumed that the metabolic activity of microorganisms found in bee bread (but absent in unprocessed pollen) are responsible for transforming it into a more nutritious and storable food product [25-28] by increasing its vitamin content , lowering its levels of indigestible polysaccharides and decreasing its pH [25,30]. Bee bread provides almost all essential nutrients to honey bees (e.g., protein, lipids, vitamins and minerals), and colonies cannot survive without it. However, the means by which microorganisms generate these changes and which ones are predominantly involved in this metabolic transformation had never been determined before.
Recently, the role of within-colony genetic diversity in shaping the microbiome of the honey bee was investigated . Of particular interest to bee researchers and bee keepers are microbial differences between colonies generated by promiscuous queens (mated with many drones) and those by chaste ones (mated with a single drone). In this study, two kinds of colonies were compared with regards to the kinds of bacteria actively metabolizing within: genetically diverse colonies (the offspring of promiscuous queens) and genetically uniform colonies (the offspring of single matings). A total of 12 diverse colonies were compared to 10 uniform colonies and samples were taken from bee guts, whole bees and the important food product bee bread.
These samples were subjected to a relatively new molecular technique that allows researchers to identify the bacteria associated with those samples. The study results are based on a total of 70,562 sequences from bacteria within those colonies and, as such, is the first study to so deeply sample the bacterial communities associated with honey bees. Interestingly, bacteria associated with honey bees and bee bread were similar to bacteria known from other “fermentation environments,” such as wine, cow rumens and yogurt. This result suggests that these bacteria may be helping bees process the complex polysaccharides found in plant materials and, perhaps, also to provide missing nutrients . This work also identified a possible probiotic organism in honey bee colonies.
Colonies that had higher loads of a particular bacterium (Bifidobacterium) tended to have lower numbers of pathogenic bacteria. This association proved to be significant – only colonies with a low number of Bifidobacterium related microbes were infected with Melissococcus, a known bee pathogen. This result suggests that, if cultivated, Bifidobacterium species from honey bees could serve as a probiotic for the colonies, thus protecting them from disease. Finally, this study also investigated the difference between genetically diverse and genetically uniform colonies, with regards to their resident bacteria, with interesting results.
First, colonies that were genetically diverse were host to more diverse bacteria; a greater diversity and number of bacterial species were found when queens were promiscuous. Second, promiscuous queens produced colonies with a greater number of probiotic microbes and a reduced number of pathogens. This last result is quite interesting as it suggests that the quality and quantity of bacterial species present in the honey bee colony may depend on the mating quality of the queen. Researchers do not yet understand how the microbiome is assembled in the context of a social environment. Is it the case that each honey bee brings to the colony its own special mix of associated bacteria, or is there some other emergent property of the honey bee society that alters the composition of the microbiome in fundamental ways?
Fundamentally, by building an understanding of the honey bee microbiome researchers may find out how microbial metabolism might contribute to honey bee nutrition (Are these microorganisms fermenting pollen in bee bread, and what is the result for the honey bee?), whether microbes provide protective benefits to colonies (such as Bifidobacterium’s protective advantage) and whether these benefits are enhanced when colonies are genetically diverse. Importantly, these kinds of studies suggest that current colony management practices may be harming the natural state of the honey bee microbiome in ways currently not appreciated.
The prophylactic treatment of honey bees with oxytetracycline may reduce the number of beneficial microbes in a colony with wide-ranging consequences. For example, a reduction in the bacteria associated with the bees would likely affect the ability of these microbes to process bee bread and to protect the hive from disease. Decreasing the genetic diversity within a honey bee colony can clearly have negative impacts with regards to the microbes associated. So it is important for bee keepers to know the quality of mating of their queens. Thinking holistically about CCD and honey bee health, bee researchers and microbiologists are working hard to understand the natural microbial state for the honey bee, as generating a healthier colony will necessarily mean they are less likely to succumb to disease.