Adaptive radiation Evolution of individuality Evolutionary genetics Ecological genetics Infectious disease

Evolution of individuality

Team members: Dr. Katrin Hammerschmidt, Dr. Sylke Nestmann, Caroline Rose, Yuriy Pichugin
Collaborators: Dr. Silvia De Monte, Dr. Ben Kerr, Dr. Eric Libby
Key publications: Rainey 2007 Nature, Rainey & Kerr 2010 Bioessays, Libby & Rainey 2013 Phys Biol, De Monte & Rainey 2014 J Biosci, Rainey & De Monte 2014 Annu Rev Ecol Evol Syst, Hammerschmidt et al 2014 Nature

In the early 1990s I completed a set of studies (aided by Katrina) on the evolution of cooperation and conflict: I finally got round to writing this up about 10 years later thanks to a welcome prod from Greg Velicer (see Rainey & Rainey 2003 Nature).

The focus of attention was the wrinkly spreader (WS) genotypes that emerge from the ancestral genotype when it is propagated in spatially structured (unshaken) microcosms. The success of WS is attributable to cooperation among individual cells: by linking to each other (via the over production of adhesive polymers) and ultimately to the edge of the glass vial the group of cells forms a self-supporting mat. Belonging to the group is costly to individual cells, but these costs are out-weighed by the benefits of group membership (group membership ensures access to the oxygen replete air-liquid boundary (there is no oxygen under the mat)).

wrinkly spreader mats

The picture above shows an intact mat (the cumulative product of the cooperative interactions of millions of cells). When the mat becomes too heavy (or too weak) it collapses into the broth (it is not buoyant) as seen in the middle microcosm. It is important to note that a WS mat is far more than the sum of the individual parts.  The photo of the microcosm on the right was taken immediately after disturbing (with a brief shake) a vial with an intact mat.  The mat breaks into many pieces (just visible on the bottom) and does not spontaneously reform.  While a mat will eventually re-emerge it will do so by a process of growth and development from just a single cell.

Although the evolutionary emergence of WS mats is a profound event, such mats are short-lived.  Selection continues to act at the level of individual cells and in so doing, favours mutant types that cheat; i.e., cells that no longer produce the adhesive polymers, but nonetheless take advantage of the benefit that accrues from being part of the mat. In the absence of any mechanism to repress them, cheaters prosper (they are in effect a cancer) -– ultimately weakening the fabric of the mat to the point where it collapses.

Having witnessed the evolution of groups I naturally began to think of the possibilities for the further evolution of these groups. At this point things became interesting. The typical group selection experiment would involve imposing selection for some group property, for example, mat strength, which is readily done by placing glass beads on the mats to find the strongest mat. The strongest mat (if that is the group trait of interest) is then allowed to reproduce (the experimenter takes that group and places some cells in a new microcosm. Some interesting things can arise in response to these types of experiments (Mike McDonald has even witnessed the evolution of a division of labour), but to me these kinds of group selection experiments fail to hit spot.

The reason for disatisfaction stems from my desire to observe the evolution of mats and this requires mats to participate in the process of evolution by natural selection. For this to occur the mats must have variation and be capable of reproducing copies of mats where the off-spring mats resemble the parent mats. While mats show substantiall genetic variation, mats lack the capacity to leave off-spring mats. As a consequence, mats are an evolutionary dead-end.

Many would not see it this way, pointing to bits breaking off mats as a means for mats to leave off-spring copies. While it would be imprudent to ignore this possibility, I think this is unlikely, because pieces of mat that break off fall to the bottom of the vial and the cells die. Others would point to the trait group models of David Sloan Wilson and say this provides a way around the problem, to which I would reply, no it doesn't! The trait group models require the entities that comprise the mat (the coooperators and the cheats) periodically disperse and then re-group (otherwise cheats take over). This might be possible in populations of organisms that have already evolved the capacity to decide when to interact and when not to interact, but in the context of these primordial groups the cells are unable to simply turn off production of the adhesive polymer, swim away, and then reform groups with different frequencies of cooperators and cheats. Such models simply do not reflect biological reality. Moreover, it is very difficult to see how selection can act with potency given the very limited heritibility that operates in such models.

I would arge then, that if simple undifferentiated groups (such as the WS mats) are a raw material for the evolution of more fit groups, then it is necessary to face up to a paradox of quite major proportions: for WS groups to become more complex they must be able to participate in the process of evolution by natural selection, but to participate in the process of evolution by natural selection they must be more complex.

Is there a way forward? I think there is. Careful observation of the dynamic of WS evolution reveals the WS mats (which appear to be evoltuionary dead-ends) and cheating genotypes. Cheating genotypes arise readily by mutation and can leave the group. Moreover, cheating genotypes can give rise to mat-forming WS genotypes by compensatory mutation. Remarkably this process can go on for some considerable time, as has been shown in spectacular fashion by Bertus Beaumont. If we pause for a moment and look at this dyamic from a different perspective we see a life cycle emerge, where the WS mat approximates the soma and the cheat approximates a germ-line. Admitedly this is a clumsy life cycle, relying to being with on mutation to switch between the different stages, but this life cycle does get us out of the paradox. WS mats, thanks to the production of cheats, can leave collective copies. They can therefore participate in the process of evolution by natural selection.

This simple idea has a number of interesting implications. One being a possible route for the evolution a soma / germ-line distinction; another being a mechanism for the control of cheats (we should no longer call them cheats they are not all bad). This arises from the mutual dependency of germ-line on soma and soma on germ-line.

In terms of multi level selection theory, recognition that the cooperater / cheat distinction might, under some circumstances, be viewed as a development cycle allows us to disband the naive assignment of fixed fitnesses to cheats and cooperaters. More importantly though, we assign fitness to the developmental programme. Our cautious suggestion is that this provides a means of moving naturally between MLS1 and MLS2 frameworks.

The germ of this idea was published in 2007 as a short essay inNature (446, 616). Ben Kerr and I published a fuller account inBioEssays (32, 872) in which the ideas are more thoroughly developed and mathematically realized (an expanded essay will appear in The Major Transitions Revisited: The Evolution of Individuality. (eds Calcott, B. & Sterelny K.) MIT Press). Caroline Rose and Katrin Hammerschmidt are currently in the midst of extraordinarily exciting and challenging experiments to explore these ideas in a large-scale experimental setting.