The Evolution of Swarming
This month we finish a three-part series on swarming, the pivotal event around which the 12-month life cycle of Apis mellifera revolves. Since May we have established that (1) swarming is reproduction at the level of superorganism – the fission, or budding of a new colony off of a parent colony; (2) swarming involves a primer phase operating at a timescale of months during which the colony rears replacement queens and is demographically and physiologically readied for the swarm event; (3) the swarm event is triggered by cues operating at a timescale of hours or even minutes – chief of which are the presence of viable queen cells, a large worker population, a steady nectar flow, and good weather; and (4) the behaviors by which the swarm decides on a new nest site are under selection pressure to ensure that bees choose the optimum site as soon as possible, and this is accomplished by an evolved emphasis on scout quorum over consensus, by the voluntary retirement of scouts who rapidly and successively cede decision-making to “fresh eyes and opinions,” by the active discouragement of dissenting scouts who are dancing (advertising) for inferior nest sites, and by voting by direct participation – recruited workers flying to one site and not another. Included in that summary is a bevy of associated behaviors such as the vibration dances delivered to a queen to encourage her to move and lose weight so she can fly again, the “piping” signals and “buzz runs” scouts do to whip up their nestmates into a flying frenzy, the chaotic and collective flight exodus, and the cloud’s consolidation around the queen on some branch or object into a temporary cluster, or bivouac. All of this is the crux of the bees’ “Darwinian moment.” If there were ever a behavioral cascade we would lay at the feet of natural selection, this is it: the superorganism’s mechanisms for reproducing itself.
To propose an evolutionary roadmap for swarming, we will follow a pattern common to all such analyses: we look for behaviors that are common across the biological family (called conserved characters) then zero-in on variants of that behavior that are particular to the species we’re studying. We presume that the common behavior is the more ancient, or basal, and the variant more modern, or derived. In the case of the honey bees, genus Apis, there are two primitive behaviors that appear very similar to reproductive swarming – absconding and migratory behavior. And with A. mellifera we are advantaged by the knowledge that it is a relatively derived member of the genus, being among the “cavity-nesting” Apis that branched off of the more primitive single-comb open-nesters. These are the starting points for our discussion on the evolution of reproductive swarming.
To begin, let’s remind ourselves that the bulk of evidence supports a tropical origin for the genus Apis in Southeast Asia. There is an argument for a European origin1, but this claim is too recent to have a significant base of support in the literature. Moreover, there are many compelling arguments for the traditional narrative, some of which we will touch upon here.
There are three behaviors known across Apis that involve all or a part of the adult bees leaving the nest and moving to a new site: (1) migration, (2) absconding, and (3) reproductive swarming (Fig. 1). The last one, reproductive swarming, has been the subject of this series for the last two months. The second, absconding, happens when the entire colony’s adult population uproots from the parent nest, usually in response to some disturbance, and relocates to a nest site. The first, migration, is a pattern known only in tropical Apis, including tropical Apis mellifera in Africa, and involves the regular movement of a colony in response to seasonal availability of foraging resources. Migration and absconding are functionally the same thing in that each is a response to changing environmental conditions. Migration can be called “prepared absconding” because it is closely tied to seasonal floral changes, and bees often prepare for it weeks in advance by slowing down foraging and brood production. In contrast to migration, true absconding, sometimes called “simple” absconding, is a response to disaster – the colony relocating because of flood, predation, or some other acute crisis. North American beekeepers may see this behavior in our own A. mellifera. More than once I’ve had a new swarm immediately reject and fly away from a hive I had given it – usually a brand new one of fresh wood and plastic foundation with not a trace of natural bee hive odor. In contrast to these first two modes of adult emigration is reproductive swarming. It is distinguished from the other two by the fact that it is always accompanied by the production of new queens, and only a portion, not the whole, adult population departs for a new nest site.
Next, let’s reflect on the fact that true migratory behavior – regular colony relocation in response to seasonal fluxes in foraging quality – is predicted to evolve under tropical conditions in which floral resources are patchy in space, but seasonality is low.2 In other words, something is always blooming, but a colony may need to move to find it. And it is precisely and exclusively in tropical Apis today that we find migratory behavior. The primitive open-air, single-comb nesting species Apis dorsata and A. florea are famous for their regular colony relocations in response to declining local resources. In the case of A. florea the migration may occur laterally for distances of up to 25 kilometers3, and in the African races A. mellifera scutellata (ancestral stock of the Africanized bees of the Americas) and A. m. adansonii, migrations can occur at elevation gradients up and down mountainsides.4,5
Temperate environments, on the other hand, are more spatially uniform in their distribution of forage plants6, but those forage plants are highly seasonal in their nectar output. Nectar availability based on time rather than space, and the overwhelming advantages of a stationary nest heavily invested with food for winter are strong selective discouragements against a migratory lifestyle. In short, temperate A. mellifera lost the ability to migrate as they settled into Europe. Today, no modern temperate-evolved European A. mellifera has retained its ancestral ability to migrate.
Migration, absconding, and reproductive swarming all share striking similarities in mechanisms and outcomes across the genus Apis. Each involves scout bees who seek new nest sites and recruit …