its own reproductive success. In short, the natural mode of colony reproduction in honey bees favors the evolution of avirulence in most of its pathogens and parasites. The two exceptions to this generalization are American foulbrood and Varroa destructor, both of which are easily transmitted horizontally when one colony robs honey from another.
Swarming also helps inhibit the reproduction of Varroa mites (and other agents of brood diseases) by creating a natural break in brood production, which forces the mites to likewise suspend their reproduction (Seeley 2017b). Once a daughter queen emerges to replace the mother queen that has left in a swarm, this daughter queen must leave the hive to fly to a drone congregation area, where she will mate with multiple drones before returning to the hive to commence egg laying. This transition from mother queen to daughter queen creates a period without sealed brood (needed for mite reproduction) that can last from 7 to 14 days. This imposes a break in the reproduction of the Varroa mites. Furthermore, with each swarming event a sizable fraction (approximately a third) of the colony's mite population is exported with the departing workforce: the fraction of mites shed can be readily calculated since about half of the female breeding‐age mites are on the workers in a colony at any given time, and nearly three‐quarters of these workers depart in the prime swarm (Rangel and Seeley 2012). In a six‐year study of the life‐histories of wild honey bee colonies living in a forest in the northeast US, Seeley (2017b) found that most (~87%) swarmed each summer.
In contrast to the relatively small nest cavities of wild honey bee colonies, the colonies kept by beekeepers occupy large hives, and they are less apt to produce swarms (Oliver 2015). The swarm control methods of beekeepers include transferring sealed brood to the top of the hive and queen exclusion (the Demaree method), cutting out queen cells, preventing the filling of cells around the brood nest with nectar (possibly a cue for swarming) by providing empty combs above the brood nest, reversing the brood boxes and inserting empty combs in the brood nest, and reducing the worker populations of colonies by splitting them. All of these methods weaken the stimuli that trigger swarming, but only one helps control the Varroa mites: the removal of bees. We propose instead controlled colony fission by making “splits” to mimic the beneficial effects of swarming on mite control (Loftus et al. 2016).
Horizontal Transmission: Bee Drift, Robbing, Forager Contact, and Contamination
Fries and Camazine (2001) outline three distinct things that a pathogen must do to reproduce and disperse to a new honey bee colony. A pathogen must: (i) infect a single honey bee; (ii) infect multiple honey bees; and (iii) infect another colony. Of these, it is the spread to another colony that should most concern beekeepers and bee doctors:
In terms of fitness, the successful transfer of a pathogen's offspring to a new colony is a critical step in its life history. If a parasite or pathogen fails to achieve a foothold in another host colony, the parasite will not increase its reproductive fitness, regardless of how prolific it has been within the original host colony. Thus, hurdles #1 and #2 (intra‐individual and intra‐colony transmission) are important aspects of pathogen fitness only to the extent that they contribute to more efficient inter‐colony transmission
(Fries and Camazine 2001).
The transfer of pathogens or parasites from one colony to another horizontally can occur by four main routes: drifting, robbing, contact while foraging, and shared use of a contaminated environment. Drifting occurs when a forager enters another colony by accident, something that is largely a byproduct of modern apiary management since the wide spacing of wild colonies largely precludes drifting (Seeley 2017b; Seeley and Smith 2015). Robbing occurs primarily during periods of a nectar dearth, when strong colonies attempt rob honey from weak ones. In this case, pathogen transfer is most likely to occur from the weak colony to the strong colony, though the opposite is also possible. The transfer of pathogens during contact while foraging has been described in both natural and experimental models, including video documentation of a Varroa mite jumping onto a foraging honey bee the instant the bee lands on a flower (Peck et al. 2016). Finally, diseases can be spread from one colony to another through sharing of contaminated water, as has been observed with infections of the microsporidium Nosema apis (L'Arrivée 1965).
Honey Bee Demographic Turnover
In the article entitled, What epidemiology can teach us about honey bee health management, Delaplane (2017) reviewed the ecological and evolutionary impacts of the host–parasite relationship and proposed that an important driver of virulence is the high rate of introduction of susceptible colonies into apiaries (i.e. the introduction of new individuals into existing populations). Epidemiologists recognize three distinct “compartments” for individuals in a population exposed to a disease: Susceptible (S), Infected (I), and Recovered (R) individuals. In the simplest SIR (Susceptible, Infected, and Recovered) model, once susceptible animals catch the disease they become members of the infected “compartment” and can spread the disease to susceptible individuals. The infected animals that survive then move into the recovered “compartment” and are considered immune for life (Kermack and McKendrick 1927). Delaplane argues that the beekeeping practice of restocking “dead‐out” hives with nucleus colonies prolongs the epidemic by introducing new “S” individuals into the population of colonies in an apiary, a process that fosters the evolution of virulence (Fries and Camazine 2001). In a closed population, however, a disease epidemic is not artificially prolonged and the surviving individuals tend to have resistance, so there tends to be coevolution of the host–parasite or host–pathogen relationship. Given the high levels of colony losses experienced by beekeepers each year, the restocking of colonies with “nuc” replacements – thereby introducing a fresh batch of susceptible individuals to the apiary population – may represent one of the most noteworthy (and easy to address) management practices contributing to the collapse of honey bee colonies (Cornman et al. 2012).
Now let us return to those curious observations of populations of mite‐surviving honey bee colonies in various places around the world. A common thread among these reports of populations of honey bee colonies surviving Varroa infestation for long periods without the use of miticides is the isolation of these populations of colonies from managed colonies. The colonies live on islands (Gotland Island in Sweden or the island of Fernando de Noronha off the coast of Brazil), in remote inaccessible regions (far‐eastern Russia), or in an intact forest ecosystem (the Arnot Forest in the northeastern United States). The isolation from managed colonies found in all three of these scenarios must have favored the evolution of avirulence of Varroa and the multitude of viral diseases vectored by this mite. In essence, these populations all lack an important feature that drives virulence of infectious disease – a steady introduction of “S” individuals. With no new “Susceptible” colonies coming into these populations, in each case the mites and the bees have co‐evolved a stable host–parasite relationship. In the case of the Arnot Forest bees, we know the Varroa invasion was associated with significant loss of genetic diversity in the bees (an indicator of heavy colony mortality caused by Varroa), but at the same time the surviving colonies of this population possessed effective defenses against the mites (Mikheyev et al. 2015; Seeley 2017b).
It is here that the “good lifestyle” of colonies occupying small nest cavities, living widely spaced, and swarming frequently meets the “good genes” of colonies that are living as an isolated “island” of colonies. Now that we have married the good genes and the good lifestyle aspects of health in our examination of honey bee management, where does the bee doctor fit into this picture? In the final section of our chapter, we will explore how we can use the knowledge garnered from a deep understanding of wild colonies to develop a new way of keeping healthy colonies in managed apiaries, an approach recently named Darwinian beekeeping (Seeley 2017a).
Lessons from the Wild Bees
Modern apiarists practice pest/disease control, close colony spacing, swarm control, queen rearing, mating control (sometimes),
