Back in March I described a superorganism as a group of individuals that together “does the kinds of things that only organisms do,” and I continued in that issue to describe one of those organism-like things – possession of a “brain” – that is, the capacity for group decision-making. Further back in November 2015 I offered a table of other metaphorical comparisons between organisms and superorganisms and suggested such comparisons as mammalian mammary glands with nurse bee hypopharyngeal glands, mammalian ovaries with the queen, mammalian testes with the drones, and mammalian wound healing with the bees’ aptitude for killing and propolizing the bodies of nest invaders. It is time to treat the subject of a superorganism’s “tissues and organs” more generally and to give an account of how such things can evolve or emerge in a group-living species like the honey bee.
First, we must make clear that when I speak tongue-in-cheek about a superorganism’s organs I’m really talking about the different functions happening in the honey bee nest that correspond to functions performed by specialized tissues or organs in an animal like you or me. There is nothing that looks like a real colony-level brain or muscles or mammary glands or ovaries or testes in a honey bee nest. But what does happen is different groups of bees performing either permanently or temporarily a specific function necessary to the group. The point here is specialization: some individuals concentrating on a particular task while others concentrate on another. Even non-beekeepers are familiar with one of these specializations – the reproductive division of labor which results in two strikingly different female castes – the fertile queen who lays the eggs and the (mostly infertile) workers who labor on behalf of the colony. Within the behaviorally rich workers we can identify even more castes if we broaden the word to include groups of individuals engaged in a particular specialty. Worker honey bees go through a series of predictable tasks as they age, a phenomenon called age polyethism, and the biological literature is rife with such terms as behavioral castes or temporal castes to describe these transient stages in the lives of workers. Newly-emerged bees concentrate on center-of-brood-nest activities like cell cleaning and feeding brood. After about one week they transition to edge-of-brood-nest activities like comb building, and around the third week they transition to outside duties like foraging1. To the extent we find metaphors useful, any of these duty categories and the workers performing them at any point in time can be considered a functional “organ” for the superorganism.
How did such task specializations / divisions of labor / behavioral castes / organs evolve in our ancestral honey bee superorganism? Well, some of it doesn’t require evolution at all. It seems that division of labor can be understood partly as another one of those emergent properties of social insect nests – order that spontaneously emerges from the collective actions of independent individuals, examples I’ve talked about in recent months including winter thermoregulation (November 2015), comb construction (December 2015), cell construction (January 2016), pattern of resource storage on a comb (February 2016), and group decision-making behavior (March 2016). Rob Page writes that “at least the rudiments of division of labour are inescapable properties of groups. There never was a time in the history of the evolution of social insects where individuals shared nests and did not have a division of labor2.” Page illustrates this point with an experimental example. Researchers in Japan studied a solitary bee species that nests singly in hollowed-out reeds. They coerced five pairs of this species to nest together by housing each pair in one container but providing only one nest site. In every case a reproductive division of labor spontaneously emerged: only one of the pair laid eggs while the other did all the foraging. It’s important to note here that this effect was immediate, not a product of time or selection, which suggests that pre-existing variation in individuals is sufficient to explain division of labor at the earliest stages of sociality. From a human viewpoint this makes intuitive sense: put together a committee, a parent-teacher association, or a beekeeping club, and it doesn’t take long to figure out who are the leaders, the followers, the workers, and the hangers-on.
In the case of honey bees there’s additional insight into some of that “pre-existing variation” that inclines an individual toward one type of task over another. To begin, we recall that the ancestral state of all bees was a solitary life with one female founding one nest and performing all the functions of reproduction, maternal care, nest defense, and foraging, with pollen foraging emphasized in females in the reproductive phase of their lives (pollen ball formation, egg deposition) and nectar foraging emphasized in the non-reproductive phases (foraging for self, nest construction)3. It is still true in modern honey bees that those workers with comparatively high numbers of ovarioles are more likely to preferentially forage for pollen. The reverse is also true, with those workers with fewer ovarioles being more likely to forage for nectar4. Thus it appears that ghosts of ancient solitary bee DNA still linger to affect task choices in social bees. Modern pollen forager honey bees are expressing an ancient maternal type behavior while nectar foragers are expressing non-reproductive behavior.
Insight to this genetic link from modern division of labor to ancient reproductive state came about through a series of studies showing that a colony-level preference for pollen hoarding could be easily selected for, sometimes in as few as three generations5,6 (Fig. 1). Compared to low pollen-hoarding bees, high-hoarding bees initiate foraging…
Compared to bees from low pollen-hoarding strains, individual bees from high-hoarding strains have higher levels of juvenile hormone and the yolk protein vitellogenin, begin foraging earlier, preferentially collect pollen over nectar, and collect larger pollen loads. All these are expressions of maternal-like behavior that harkens back to their solitary bee ancestry. Pre-existing variation in an individual’s expression of maternal versus non-reproductive behavior may affect that individual’s choice of task specialization in a modern social colony.