Since January 2015 I have been writing a column in these pages on the social evolution of the honey bee. Social, in the sense that I have focused less on Darwinian forces that shape the individual and more on Darwinian forces that shape the group. This is why I have not, for example, talked about the evolution of insect anatomy, metamorphosis, or flight, as these are ancient features that were settled hundreds of millions of years ago by individual selection acting on honey bees’ solitary ancestors.
Along the way we studied the genetic peculiarities of the insect order Hymenoptera, the ants, the wasps, and the bees, and showed how the state of haploidy in males – possessing only one set of chromosomes – sets the stage for extreme relatedness in colonies.
Although this was no doubt a powerful driver toward sociality at first, we also showed how the subsequent evolution of queen multiple mating upset this tidy state of in-nest relatedness in favor of in-nest genetic diversity. Such a move can only be explained as an example of group, or social selection: the benefits of genetic diversity to the group outweighing the benefits of selfishness and nepotism to individuals. Put another way: a group of cooperative altruists probably out-competes a similar group of selfish competitors, even if the altruism is purchased at the cost of reduced individual fitness.
Early on we also established the three criteria of true sociality, or eusociality:1
1 Cooperative brood care in which individuals participate in the care of a common brood,
2 Reproductive division of labor in which reproductive demands and housekeeping demands are met by different cohorts of individuals, and
3 Overlapping generations in which at least some offspring remain at the nest to help their mother produce more siblings.
These three criteria are additive so that groups possessing only one or two of them are understood to be expressing presocial behaviors. Only when all three are present can we call a species eusocial, but even then, we can still talk about perennial versus annual eusociality on the basis of whether the species lives year-round in a eusocial state. Bumble bees fit this latter category, as it is only the newly-mated daughters who survive in isolated hibernation over winter, emerging in early spring to single-handedly found a nest, forage, and produce the first clutch of brood. Only when the first workers emerge is full eusociality restored. Honey bees, on the other hand, fit the description for perennial eusociality as they live as a social unit year-round.
We’ve also spent a lot of time talking about the distinction that occurs once a perennially eusocial species adopts fixed reproductive castes, as in the case of the honey bee. Over geologic time, as the mother bee abandoned foraging and nest duties, her worker-like behaviors and morphology atrophied until she was no longer able to perform work. The reverse was true of daughters who abandoned egg-laying to specialize on worker behaviors. Once castes had evolved into such states of hyper-specialization and mutual dependence, it was now the colony that was the true Darwinian unit of selection. Evolutionary biologists call this the “point of no return” because there are no known examples of a species returning to solitary life after these irreversibly divergent caste decisions were made.
Once reproductive conflicts between females was resolved by caste differentiation, the mother (we can now call her the queen) was free to practice multiple mating, leading to genetically diverse colonies in favor of genetically narrow families. It is no accident that this genetic diversity became associated with task specialization, increasing scales of efficiency leading to larger colony populations, emergent properties such as group thermoregulation and complex nest architecture, and every other measure of advanced eusociality.
Once fixed castes had rendered the colony an integrated whole, it became untenable to think of it anymore as a “society” which in biology implies an assembly of reproductively autonomous individuals. The group collectively achieved what organisms typically do, yet its constituent parts, the workers, were not cells but organisms themselves. It begged for a new name, and credit for illuminating the conundrum fell to William Morton Wheeler, who in a 1911 published lecture2 pointed out that an ant colony:
1 “…behaves as a unitary whole, maintaining its identity in space”
2 “…has its own peculiar idiosyncrasies of composition and behavior”
3 “…has a most interesting adaptive growth and orientation which may be regarded as a kind of tropism,” and
4 differentiates its cell types like an organism “in which the mother queen and the virgin males and females represent the germ-plasm …while the normally sterile females, or workers and soldiers, in all their developmental stages, represent the soma.”
All of which are things that describe organisms. It took Wheeler another 17 years before he coined the word “superorganism”3 to describe this situation that establishes when a group of organisms coalesce integrally and genetically into a higher level of biological organization. The “super” in superorganism expresses the idea of a stratum higher than organism, with the organism, not cells, making up the constituent parts.
The idea of the superorganism had its ups and downs in the 20th C, laying low while science went through decades of infatuation with reductionist approaches to biological questions. But recent years have seen a resuscitation of the term owing to a growing recognition of its usefulness as a context for understanding broad patterns of evolution. In short, the evolution of the superorganism recapitulates the evolution of organisms such as you and me, with, in the case of honey bees, the added benefit that one can “dissect” a superorganism and put it back together again. One of my reasons for writing this series of articles has been to let beekeepers know that they are wardens of a unique and privileged insight into reality, the honey bee superorganism – a window into ourselves and all organismal life on this planet.
Regardless of our labels and how we arrive at them, superorganismality has been a wildly successful life strategy. E.O. Wilson cites numerous examples.4 One third of all animal biomass, including vertebrates, in the Amazonian rainforest is composed of ants and termites. On the Ivory Coast savannah, the density of ants is 20 million per hectare. And in a demonstration of the mind-boggling populations possible in the most advanced eusocial species, one ant colony on the coast of Hokkaido, Japan was found to contain 306 million workers and 1,080,000 queens living in 45,000 interconnected nests spanning an area of 2.7 square kilometers (1 square mile).
The ecological success of eusociality can be explained as an interplay of at least three qualities:4 (1) coordinated groups can perform functions in parallel, rather than serial workflows; (2) groups can invest more effort, by energy or sheer numbers, on such priorities as …