jeff smith

Abstract: Hamilton’s rule states that cooperation will evolve if the fitness cost to actors is less than the benefit to recipients multiplied by their genetic relatedness. This rule makes many simplifying assumptions, however, and does not accurately describe social evolution in organisms such as microbes where selection is both strong and nonadditive. We derived a generalization of Hamilton’s rule and measured its parameters in Myxococcus xanthus bacteria. Nonadditivity made cooperative sporulation remarkably resistant to exploitation by cheater strains. Selection was driven by higher-order moments of population structure, not relatedness. These results provide an empirically testable cooperation principle applicable to both microbes and multicellular organisms and show how nonlinear interactions among cells insulate bacteria against cheaters.

jeff smith, J. David Van Dyken, & Peter C. Zee (2010) “A generalization of Hamilton’s rule for the evolution of microbial cooperation” Science 328: 1700-1703. [Link]

While putting my Myxo work together into a talk, and trying to present it all with some semblance of coherence, I had the opportunity to think about where the evolution of microbial cooperation is as a field and where I think it should go.  The way I see it, the most important open are these:

Is shared genes the primary evolutionary mechanism maintaining cooperation in microbes? By shared genes I mean that the benefits of cooperation are preferentialy experienced by individuals who also share the alleles for expressing the cooperative trait.  This process can be described as kin selection or group selection.  Shared genes is widely thought to be the primary mechanism for the evolution of cooperation in animals—is it true for microbes, too?  And what role do other mechanisms like enforcement, direct benefits, or pleiotropic constraint play?

What is the primary cause of genetic correlations among individuals? Limited dispersal, kin recognition, green-beard genes, infectious gene transfer, or something else?  Do cooperative traits themselves create genetic correlations through their effect on migration and motility?  The important part of these questions is getting at what IS happening, not just what CAN happen.

How does social evolution shape microbial traits? Many traits seem to involve interactions between individuals (quorum sensing, biofilms, and so on), but are these traits cooperative in the evolutionary sense of increasing the fitness of other individuals?  How does the magnitude, regulation, or form of these traits differ from that what they would evolve to be if they did not have social effects?  To what extent do microbes actively alter their behavior in response to social conditions?  Which traits are adaptations and which are only side-effects of some other function?

How do social traits change over evolutionary time? Are social traits under stabilizing selection or do they evolve in evolutionary arms races?  How often are they lost?  If cheaters occur in natural habitats, do they persist because of selection or recurrent mutation?

What are the origins of microbial cooperation? What traits were co-opted into becoming the building blocks of cooperation?  Worker behavior in social insects, for example, is a modified form of maternal behavior.  Are the benefits of cooperative traits the same now as they were originally?  How many times have similar cooperative traits originated?  Are cooperative traits usually acquired by horizontal gene transfer or invented de novo?