Paul Rainey has a very interesting essay in the April 5 issue of Nature. Much of what we know about "cheating" in bacteria that form floating mats comes from his research, including collaboration with Michael Travisano, recently hired here at University of Minnesota. See my earlier post, "how disturbed are cheaters", for background on this system. Although cheaters that don't invest in the goop that holds floating mats together can result in mats breaking up and sinking, Rainey's new essay suggests that a similar form of cheating may have contributed to the evolution of multicellular life.
Here's the problem. As long as cells reproduce independently, natural selection will favor anything that helps individuals reproduce more in a given generation, even if all the cells would have more descendants, over the long term, if they all cooperated. It's a tragedy of the microbial commons.
If selection operated on groups, rather than individual cells, that would favor mechanisms to suppress cheating. Humans can and do impose group selection (see Darwinian Agriculture), but group selection strong enough to overcome individual selection is thought to be rare in nature.
However, Rainey points out that cheaters don't just disrupt groups of floating cells. They also tend to swim away, where they could potentially found new groups. For the new groups to be most successful, they would need to float, so most individuals in a group would need to produce goop. Therefore, cheaters that have lost the goop gene, thought mutation, wouldn't form successful groups.
But what if, instead of losing the gene altogether, they just turn it off long enough to swim away? If they then turn it back on again before reproducing (by dividing), they could form a new floating group. Therefore, a genotype that keeps most cells in the goop-producing mode (keeping mats floating), but with a few cells not making goop (swimming away and founding new groups), might out-compete genotypes with no cheaters at all. Rainey suggests that the swimming cheaters are analogous to germ cells (sperm or eggs), whereas the cooperative goop-producers are more like somatic (nonreproductive) cells.
Could the division of labor between reproductive and nonreproductive cells, a key to multicellular life, really have arisen by a similar process? I have no idea. I look forward to reading responses to Rainey's essay from other scientists.
I will point out that nothing in the essay suggests that most forms of "cheating" are beneficial. What about rhizobium bacteria that infect bean roots but don't provide their host with nitrogen (my specialty), bees that cut through the base of a flower to take nectar without pollinating, or people who cheat on taxes? If any of these forms of cheating are beneficial to anyone other than the cheater, the reasons would have to be very different from those proposed for Rainey's floating bacteria.
P.B. Rainey 2007. Unity from conflict. Nature 446:616.
P.B. Rainey and M. Travisano. 1998. Adaptive radiation in a heterogeneous environment. Nature 394:69-72.
Rainey PB, Rainey K. (2003) Evolution of cooperation and conflict in experimental bacterial populations. Nature 425: 72-74.