The Uncertain Evolution of Social Immunity
We are continuing a short series on social immunity – individual behaviors and situations inside a bee nest that collectively discourage the entry, establishment, and proliferation of a parasite in the nest. The term “social immunity” is used in distinction to “innate” or “personal” or “individual” immunity of the kind that occurs in single organisms such as a worker bee. There are, however, parallels between the two that suggest how evolution has converged upon similar answers to similar problems. Both organisms and colonies, for example, show avoidance behavior toward parasites, rapid containment of parasites once they breach the border (the skin or nest wall), and high priority for protecting reproductive tissues (testes, ovaries, or queen).1 Moreover, in both organisms and colonies, immune strategies follow a predictable pattern of increasing engagement starting from outside and moving in2: (1) preventing parasite uptake, (2) preventing parasite intake, (3) preventing parasite establishment, (4) preventing parasite spread between tissues (or colony members), and lastly (5) preventing spread of parasite to offspring. Figure 1 shows what some of the mechanisms of social immunity look like in a bee colony.
It was these mechanisms that I talked about last month, and following the pattern of this monthly series I’d love to give you a well worked-out scenario on how social immunity arose, whether by natural selection acting on the group, by emergent properties of the physical nest, or by independent actions of the workers. But what this month offers instead is a glimpse into what a field of science looks like when it is young and ripe for development. The term “social immunity” has only been around for ten years. No such pathway has been worked out for its evolution. Basic questions remain, such as: Was social immunity a cause of social life or an effect of social life? We’ve barely settled on its definition. But we do have a lot of relevant material from which we can draw strong inferences. It is this uncertain state of affairs that I will try to summarize for you, an exercise, I believe, always worth doing because there’s benefit in understanding systems at their most base level. Only when we understand all the moving parts in a machine can we fix problems at their root. For a machine as complex as the honey bee colony, those “moving parts” are the selection forces that made the colony evolve the functions and behaviors we observe working so well today.
The term “social immunity” first showed up in 2007 in a landmark paper by Sylvia Cremer and her co-workers who defined social immunity as the “collective action or altruistic behaviours of infected individuals that benefit the colony.2” Three years later it was pointed out that such a term should be reserved for immune behaviors that are explicitly social – that is, the result of natural selection acting on groups.3 Self-grooming, small nest entrances, and removing waste, for example, could just as easily be expressed by a solitary mother in her simple earthen tunnel. Group responses of any kind, including holdovers from ancient solitary living, are better called “collective” responses, a safe term that makes no claims whether the trait is socially selected or solitary. In the most recent and refined definition of social immunity, Joël Meunier has taken into account solitary versus social origins and clarified that the term must be limited to a group: “any collective and personal mechanism that has emerged and/or is maintained at least partly due to the anti-parasite defence it provides to other group members.4” With this wording, an immune trait may be solitary in origin, but if it has been modified by group selection we may now include it under “social immunity.” The point of these clarifications is, What exactly is selected for; who benefits; who pays, and did it evolve in response to social or solitary living? Knowing this is useful for designing a honey bee breeding scheme that employs any of the features of social immunity detailed in Figure 1.
Now that we have the terms settled, we can begin considering the various immune mechanisms (Fig. 1) and their evolutionary histories. The questions and uncertainties are legion. First, we must determine if a trait is a product of group selection or a carry-over from solitary life. This is complicated by the fact that …