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Helpful cheaters?

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.

Comments

There are a number of points at which the line between multicellular life and single-celled life become blurred. The social amoeba is one that is well known. When nutrients become scarce, normally solitary amoeba gather together to form what looks and acts like a slug of perhaps 100,000 cells. It will move some distance, then take on the form of a puddle giving way to a stalk - where only the cells at the top have the chance to create spores.

Then there is cancer, where the normal regulation of the life and death of a cell is broken. The genome becomes destabilized since cells which have mutated no longer undergo programmed cell death, and their mutations facilitate more. At this point, natural selection selects for those cells which reproduce the most quickly and have the variability necessary to evade whatever is thrown at them. In essence, they are no longer evolving according to the rules required of multicellular life but more closely to those of single-celled life - at the expense of the multicelled organism their line depends on - usually.

However, one wolf took this to the extreme:

A Dead Dog Lives On (Inside New Dogs)
Category: Evolution
Posted on: August 9, 2006 12:02 PM, by Carl Zimmer
http://scienceblogs.com/loom/2006/08/09/an_old_dog_lives_on_inside_new.php

In any case, bacterial mats occupy different points along what is essentially a continuem between multicelled life and single celled. From what I understand, some communities will even have lifespans which are internally determined rather than a function of external conditions. Moreover, we know that there exists complicated signaling systems between different species of bacteria within a given community or between different members of the same species. Moreover, they are now investigating the phylogenetic relationships between intercellular signaling within multicelled organisms and signaling between bacteria.

One point which I myself have wondered about is whether, in adapting to a variable environment in which a species of bacteria may be required to form communities in combination with varying species of other bacteria, this may have resulted in the evolution of an adaptability through the emergence of pre-eukaryotic gene regulation, leading eventually to us. Obviously there will have to be a point at which the primary community consists of clonal cells, but cells which are capable of intercellular regulation and specialization. In essence, variable multispecies bacteria mats would have been a kind of training ground for that sort of plasticity.

In any case, I will be looking forward to reading this article. Obviously the evolution of multicellular life is an interest of mine. (My apologies if I seemed to ramble.)

Thank you for pointing this out!

"Evolutionists are increasingly aware of the importance of a multilevel-selection perspective — a way of making sense of the effects of selection at different levels of biological organization. Integral to this perspective is the recognition that processes occurring at different levels (for example at the level of the cell or of the organism), and at different times, are connected: selection at the higher level has consequences for the lower level and vice versa."

Unity from conflict
Paul B. Rainey
NATURE|Vol 446|5 April 2007

This is one of the insights which I regard as being of considerable interest. What is the unit of selection? The gene, a gene complex, a cell, an organism or a society? What about an ecological system?

Selection requires variation and more than one unit to select from - therefore it would appear that the biosphere as a whole cannot be a unit of selection, but anything below this presumably could be, but forming looser and looser confederations as one moves to the next "higher" level. However, to move to the next level would itself presumably require slightly detrimental mutations or variation, otherwise selection at a given level would prevent movement to the next level. Smaller populations, hower, have a wider range of mutations to which the phrase "slightly detrimental" applies. Then perhaps as the population expands, selection can once again tighten the reins, but at a higher level of complexity.

Another aspect of "selection" which people are taking more of an interest in (at least in molecular biology) is "indirect selection" where selection selects for variation or variability. If a given organism is incapable of producing such variation, then in a variable environment, as soon as that environment is no longer conducive to the survival one of its descendants, it will no longer be conducive to the survival of all of its descendants. Therefore, one strategy that evolution may give rise to is variability where fidelity is weakened - at least in the areas where such variation would be of value. Thus for example hypervariable regions of the genome may be selected for - if they produce the sort of variation which increases the chances that at least some of your descendants will survive. This approach is explored in a number of essays in "The Implicit Genome" edited by Lynn Caporale. (I highly recommend it.)

But there are other ways of varying the phenotype, that is, other than by means of mutations. Much earlier, Bruce Wallace focused on the variability of a population (e.g., "Fifty Years of Genetic Load"), in some cases as the result of its life-cycle. If all organisms were equally fit, then in an environment where only a certain fraction could be supported, it would be more likely that all would die or be seriously injured before there would be enough culling of the herd for those remaining to survive. Therefore we could expect evolution to select for those organisms which have varying degrees of fitness - at least under what he termed "soft selection."

Timothy,
Thanks for your comments and the link on transmissible cancers in dogs. I'd read about the one in Tasmanian devils.

You wrote: "complicated signaling systems between different species of bacteria within a given community or between different members of the same species."

I agree with a recent review: "From an evolutionary perspective, intraspecies signalling can be explained using models such as kin selection, but when communication is described between species, it is more difficult to
explain. It is probable that in many cases this involves QS [quorum sensing] molecules being used as ‘cues’ by other
species as a guide to future action or as manipulating molecules whereby one species will ‘coerce’ a
response from another."
Diggle SP, Gardner A, West SA, Griffin AS. (2007) Evolutionary theory of bacterial quorum sensing: When is a signal not a signal? Philosophical Transactions of the Royal Society

For an analogous analysis of "signals" among insects and plants, see:
Stowe MK, Turlings TCJ, Loughrin JH, Lewis WJ, Tumlinson JH. (1995) The chemistry of eavesdropping, alarm, and deceit. Proc Natl Acad Sci USA 92: 23-28.
One of the many cool examples in this paper is bola spiders, which release a volatile that mimics moth pheremone, and feed mostly on male moths they lure!

The Selfish Gene and The Extended Phenotype (both by Dawkins) are still most useful to me in making sense of these complex interactions.

Dawkins is brilliant. In addition to the books already mentioned, pick up "The God Delusion" - he applies evolutionary theory to faith.

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