bees was discovered by Simone et al. (2009). Honey bees living in hives whose inner walls were coated with propolis extracts (derived from resins found in Minnesota and Brazil) invested less energy on immune function compared to bees living in hives without such coating. The colonies living in the propolis enriched hives also had lower bacterial loads. Scientists believe that individual bees are not immunocompromised, but rather that they conserve energy by not upregulating their immune genes except when a pathogen is encountered. This means that the defenses provided by social immunity (e.g. the collection of tree resins for propolis) allows individual bees to divert energy resources from immune function to other hive activities such as nursing, wax building, and foraging. This strategy likely maximizes the health and fitness of the entire colony.
Bee Microbiome
An oft‐overlooked aspect of the bee environment that is essential to the good lifestyle of honey bees is their microbiome, that is, the community of specialized microbes (bacteria and yeasts) that have coevolved to live inside the bees and in their nests (e.g. in their pollen stores). We again return to the tenet of our chapter: the need to learn about the honey bee's natural biome to understand its biology, including its relationships with its pathogens. The honey bee microbiome is remarkable in that it is nearly consistent across thousands of individuals from hive to hive and even across continents. The honey bee's microbiome is similar to that of humans in that both feature specialized bacteria that have coevolved with their host and are socially transmitted (Engel et al. 2012; Zheng et al. 2018). Honey bees are first inoculated with bacteria in the larval stage, presumably through the food provided by nurse bees. However, during pupation, when bees undergo the final phase of metamorphosis, a bee's exoskeleton (including the gut lining and any associated bacteria) is shed in a process known as ecdysis. Therefore, honey bees emerge as young adults without a gut flora, except for those microorganisms they pick up when chewing through the wax cappings of their cells. The characteristic microflora of a worker bee is, therefore, developed mainly following emergence and through direct social interactions with conspecific worker bees. By four to six days of age, the population of a worker bee's gut flora stabilizes at 108–109 bacterial cells.
Although both wild honey bees and those living in apiaries possess complex microbiomes, some beekeeping practices – such as feeding pollen substitutes and treating with antibiotics – can alter the microflora of honey bees (Fleming et al. 2015; Maes et al. 2016). Dysbiosis, or unhealthy shifts in gut microflora, was observed in bees consuming aged pollen or pollen substitutes and was linked to impaired larval development, increased bee mortality and infection with pathogens such as Nosema and Frischella. Raymann et al. (2017) observed considerable changes in the gut microbial community composition and size following treatment with tetracycline, the most commonly used antibiotic in beekeeping operations globally. The authors concluded that decreased survival in honey bees was directly attributed to increased susceptibility to infection by opportunistic pathogens that colonized the gut after antibiotic use. The honey bee microbiome is thought to promote bee health and development in several ways. Gut microbes are required for normal bee weight gain, an effect which can be attributed to regulation of endocrine signaling of important bee hormones. The microbiome increases the levels of vitellogenin and juvenile hormone in worker bees, and these regulate the nutritional status and the development of their social behaviors, so it is likely that the state of the bees' microbiomes affects the health of the whole colony. Bee microbes are also implicated in modulating the worker bee's immune system (Zheng et al. 2018).
Alterations in the microbiota of the bee gut have been linked to disease and reduced fitness of the bee host. The use of tetracycline – an antibiotic commonly used to treat American foulbrood and European foulbrood, and often given prophylactically – reduces both the number and the composition of normal bacteria in the bee gut. Raymann and colleagues (2018) found that Serratia marcescens, a known pathogen of honey bees and other insects, normally inhabits the bee gut without eliciting a host immune response. However, bee disease occurs when this pathogen is inoculated into a bee's hemolymph through the bite of a Varroa mite or when the gut microbiome is disturbed with antibiotic use. Researchers studying Colony Collapse Disorder observed a shift in gut pathogen abundance and diversity, and proposed that such shifts within diseased honey bees may be a biomarker for collapsing colonies (Cornman et al. 2012). See Chapter 9 for more details on the bee microbiome.
Part 2: Epidemiology for Bee Health: How Lifestyle Impacts Disease Spread
The preceding comparison of the environments of honey bee colonies living in the wild versus in apiaries sets the stage for reviewing the host–parasite interactions that ultimately define colony health. Let us now compare the impacts of disease on colonies living in the differing settings in which honey bee colonies now find themselves. Compared to organisms that do not live in large and complex eusocial societies (i.e. ones with a reproductive division of labor and overlapping generations) honey bees have far greater complexities in their host–pathogen and host–parasite relationships.
Ecological Drivers of Disease
Living in crowded communities of thousands of individuals, honey bees interact closely through regular communication behaviors, grooming activities, and the trophallactic transfer of food and glandular secretions. This complex group living provides abundant opportunities for pathogens to spread and reproduce. Moreover, the high temperature and high humidity of a honey bee colony's home makes it a perfect environment for disease outbreaks. It comes as no surprise, then, that many of the protective mechanisms that honey bees have evolved to control the spread of disease operate at the level of the whole colony, the superorganism. The members of a colony work together closely to achieve a social immunity: they groom themselves and one another (allogroom); they work as undertakers to remove dead and diseased bees; they collect antibiotic enriched pollen and nectar; and they practice miticidal and hygienic behaviors by biting off the body parts of mites and by removing infected bee larvae and pupae from their nests (Fries and Camazine 2001). Relatively few mechanisms of disease resistance have evolved at the level of the individual bee. These include individual immune system functioning and filters in the proventriculus (the valve between esophagus and stomach) that remove spores of American foulbrood. Most of these protective mechanisms limit intra‐colony transmission of disease agents, and they work well. What is probably the primary driver of disease problems for honey bees at present, however, is inter‐colony disease transmission.
A Critical Distinction: Vertical vs. Horizontal Disease Transmission
The method by which a disease is transmitted from colony to colony is a fundamental determinant of pathogen virulence. Vertical transmission (the spread of disease from parent to offspring) favors the evolution of avirulence whereas horizontal transmission (the spread of disease among unrelated individuals) favors the evolution of virulence (Lipstich et al. 1996). This is because pathogens and parasites that spread vertically need their host to stay healthy to produce offspring, whereas those that spread horizontally do not have this need. Although numerous other host factors (i.e. host longevity, density, population structure, and novel hosts) and pathogen factors (i.e. vector availability and pathogen replication potential) also influence virulence, we will focus on how the mode of honey bee pathogen and parasite transmission within and among colonies impacts the evolution of the virulence of these agents of disease.
Vertical Transmission: Swarming
In honey bees, one way that a colony achieves reproductive success is by swarming: an established colony casts a swarm to produce a new colony. The other way that a colony achieves reproductive success is by producing drones; even though weak colonies can propagate their genes by producing drones, this does not create another colony. If a pathogen or parasite that is transmitted vertically (from parent to offspring) weakens its host and so hampers it from producing
