My previous post on a potential problem for the selfish gene theory in explaining cooperative behavior resulted in a fair amount of heated discussion. However, there are quite a few misconceptions regarding the controversy surrounding the selfish gene, group selection, multilevel selection, generalized reciprocity, etc. that need to be clarified. When Richard Dawkins published The Selfish Gene in 1976 it was an instant classic and has been championed for the past three decades as the final answer on how natural selection operates. What has been tremendously useful about the theory, as in all scientific theories that explain so much about the natural world, is in directing scientific questions to the borderlands where the theory's explanatory power is weaker.
The best example of this outside of the life sciences would be Newton's theory of Universal Gravitation. Newtonian physics was a revelation to 17th century science and was immediately celebrated as the correct description of reality. The problem was that Newton wasn't able to describe what gravity actually was, just how the force acted on objects. To understand the frontiers of Newton's science the world had to wait for Albert Einstein and his theory of Special and General Relativity. With Einstein came the understanding that space-time was actually curved and that the force of gravity was the result of this curvature. Einstein didn't so much replace Newton as expand the borders of scientific understanding.
I would argue that the selfish gene theory also needs expanding.
One area of potentially fruitful research is in the area of multilevel selection theory. Multilevel selection is essentially the idea that natural selection can also operate at levels beyond just the individual. The difference between multilevel selection and group selection is mostly rhetorical, but is useful in that the name is more inclusive and doesn't restrict the level of selection. What the selfish gene theory did was expand the unit of selection from the individual organism to the gene itself. It is the gene's "goal" to replicate itself as widely as possible (it's hard to avoid ascribing intention in this discussion, but it's important to remember that a gene has no more conscious motivation than the force of gravity does). The individual organism is the means by which the gene passes copies of itself into subsequent generations. According to this view, humans (as well as pterodactyls and petunias) are merely ambulatory vehicles by which our genes pass from point A to point B. What multilevel selection theory proposes is that genes can also successfully pass on copies of themselves at the level of the social group.
There have been some fascinating findings in this area and one of the most well-known researchers into group/multilevel selection is David Sloan Wilson whose book Unto Others: The Evolution and Psychology of Unselfish Behavior is a must read. Wilson recently co-authored a paper in Quarterly Review of Biology (pdf here) with well-known Harvard entomologist Edward O. Wilson that reanalyzed sociobiology from a multilevel perspective.
Wilson has also been hosting regular updates on his research at The Huffington Post under the title Truth and Reconciliation for Group Selection. In his latest post he provides some examples of group selection in the laboratory. Initially, however, Wilson explains a classic experiment with hens demonstrating the importance that different levels of selection have for the evolution of sociality:
William Muir, an animal breeder at Purdue University, selected for egg productivity in hens in two different ways. Both involved housing hens in cages (groups), which is standard practice in the poultry industry. The first method involved selecting the most productive hen within each cage to breed the next generation of hens. The second method involved selecting the most productive cages and using all the hens from those cages to breed the next generation of hens. It might seem that this is a subtle difference, that the same trait (egg productivity) should be selected in both cases, and that the first method should be more efficacious. After all, eggs are produced by individual hens, so why not directly select the best? Why select at the group level, when even the best groups might have some individual duds?
The results told a completely different story. The first method caused egg productivity to perversely decline, even though the most productive hens were chosen each and every generation. The second method caused egg productivity to increase 160 percent in six generations, an astonishing response as artificial selection experiments go.
What happened? If you've been paying attention to my Truth and Reconciliation blogs, you'll recognize a classic case of multilevel selection. Natural selection within groups is sensitive only to relative fitness, relentlessly favoring hens who lay more eggs than their neighbors. The first method favored the nastiest hens who achieved their productivity by suppressing the productivity of other hens. After six generations, Muir had produced a nation of psychopaths, who plucked and murdered each other in their incessant attacks. No wonder egg productivity plummeted! It would be hard to imagine a more graphic example of what I have called "the original problem" throughout this series of blogs; traits that are "for the good of the group" are not always locally advantageous within the group and require a process of group-level selection to evolve.
That's why the second method worked. Selecting the most productive groups favored peaceful and cooperative hens, despite their selective disadvantage within groups. Moreover, group-level selection was sufficiently strong to successfully counteract selection within groups, which was taking place within cages for the second method, just as much as the first. Muir's experiment proves the efficacy of group selection, at least under the conditions of the experiment.
What's important to point out is that the hens in this case were siblings, but so were the hens in the study on individual selection. Amazingly, selection at the level of the individual eliminated the cooperative aspects between siblings that kin selection would normally provide and bred a generation of sororicidal maniacs! It also emphasizes that multilevel selection is not at odds with kin selection. As stated above it is an expansion upon the current understanding of how natural selection operates. While laying eggs may seem like a trait selected purely at the individual level, what this classic experiment revealed was how important the social network is. The most efficient outcome was not achieved by taking the most prolific egg layers and selecting their genes only. It was achieved by selecting the most prolific group of egg layers.
Wilson has also demonstrated this in an experiment conducted with William Swenson and published in Proceedings of the National Academy of Sciences. As he describes the research:
We grew a fast growing plant called Arabidopsis in small flowerpots. The soil was sterilized except for a slurry of six grams of unsterilized soil from a single well-mixed source. To be precise, to make the slurry, we placed unsterilized soil and sterilized water in a kitchen blender and blended it like crazy before delivering six grams of soil to each pot of sterilized soil. If you know anything about microbiology, you know that millions and millions of microbes comprising hundreds and hundreds of species are contained in a single gram of soil. Thus, the initial variation among pots in the genetic and species composition of the soil microbes was vanishingly small.
We grew the pots under constant environmental conditions until the plants were large enough to harvest. We weighed the biomass of the plants and performed a standard artificial selection experiment with a single twist. Instead of the selecting the largest or smallest plants to breed for the next generation, we selected the soil from under the largest and smallest plants (in separate treatments) to make into a slurry and inoculate the next generation of pots. In other words, we were selecting at the level of whole microbial ecosystems rather than at the level of individual plants. Plant biomass was being used as a phenotypic trait of the ecosystem.
Over many generations Wilson and Swenson continued to collect the bacteria laden soil from under the largest and smallest plants and grow more plants of the same species. What they found was that plants grown in the two soil ecosystems grew the same as previous (genetically unrelated) plants had. By selecting groups of bacteria, rather than the individual plants, Wilson and Swenson demonstrated how group selection could give rise to the most fit individuals. Since the network of soil bacteria thrive so long as their host plant thrives, the mutualistic relationship promotes each individual bacteria in the network, but they are only able to thrive because of the selection that occurred at the level of the group. This is how multilevel selection operates.
At this time, multilevel selection theory is in its infancy and it's currently unknown how widespread this kind of selection is in the natural world. However, I believe the research shows great promise and deserves to be taken seriously. It's unfortunate that Dawkins has often been as stridently against this line of research as he has been with religious conservatives. Referring to this research as the "group delusion" and Wilson's interest in it as a "weird infatuation" demeans his role as an advocate of cutting edge scientific research. Multilevel and group selection theory is not ideologically driven and the primary interest is to advance knowledge of evolutionary history not condemn it. Unfortunately, Dawkins has made the issue personal when the focus should be on the merits of the research itself.
However, all of this is commonplace in the history of science. Dawkins, like Newton before him, is passionate about his topic and will defend his perspective vociferously. I don't believe the life sciences equivalent of Einstein has entered the stage just yet, but I do think that such an arrival should be anticipated and welcomed as we continue to expand our knowledge about the natural world.
UPDATE: Bob O'Hara, blogger at Nature Network, has an in depth critique of my position. I respect the opinion of my former blog colleague and will be responding in the near future.
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Hey, having Dawkins dismissing your research is worth as much as having him praise it- more, maybe- in terms of profile-raising.
Dawkins is, of course, right that ultimately it's gene frequencies that vary in evolution. You are right that _how this happens_ can invole many levels.
I don't see that Bill Muir's work is a problem for the Selfish gene: it's nothing more than an application of the Price equations, which are just gene-centric.
My impression as an outsider has been that the inclusive-fitness people can turn any multi-level selection model into an inclusive fitness model with the appropriate Price-jitsu, and vice versa. A similar phenomenon seems to occur with regard to game-theoretic descriptions of evolution: Nowak et al. publish a criterion for when cooperation is stable in such-and-such a scenario, and then somebody comes along with another paper saying, "What they did with game theory, we can do with inclusive fitness, too! ZOMG!!eleven!"
Assuming that there is this great big fuzzy equivalence class of evolutionary models, the question is not, "Which tool is Correct-with-a-capital-C?", but rather, "Which tool is most useful in which circumstances?" In addition, I suppose it's possible that evolutionary phenomena exist which are outside this equivalence class, and thus for which no model currently on the shelf is fully adequate. Then the question would become, "Which of these perspectives currently in our toolbox best generalizes to cover the new situation?"
Blake - I wrote a longer reply that's caught in moderation (too many links!). There was a too and fro in the Journal of Evolutionary Biology on precisely this.
It's strange that I really don't think there's a controversy amongst people actively working on the models for social evolution: we're beyond that. But the old names keep on getting dragged up as if nothing has happened.
It appears to me that the first described experiment with the groups of chickens very nicely demonstrates a regression to the mean phenomenon when the individual chickens are selected.
If you always take the highest producer,it will tend to lay closer to the centre of the distribution of possible number laid next time. So fewer eggs.
Feel free to prove me wrong.
The chicken experiment need not support group selection. For the individual (psycho) group the experiment changes their environment so much that they are suddenly surrounded by like minded individuals instead of a heterogeneous group. Each chicken will perform badly (because natural selection has not equipped them to be fittest in these new conditions) until the gene pool has time to adjust by allowing those more successful variants, selected individually, to provide more of their genes the the future gene pool.
The effectiveness of any gene is a function of the environment in which it operates.
The expression of the gene in other carriers of the gene is part of the environment.
Seems really simple to me. (To express; it's a non-linear feedback, and consequences of those are endlessly hairy to deal with computationally.)
Could you please provide an explicit statement of this "selfish gene theory" that you keep talking about? Preferably with citations from Dawkins himself, since I can't recall reading this expression in his work?
You mean like the book The Selfish Gene, published in 1976?
. . . which uses the exact expression "selfish gene theory" on pp. xv, 67, 68, 101, 112, 115, 116, 118, 119, 120, 143, 155, 168, 170, 172, 174, 234 and 295.
If I recall correctly, Gould's response to Dawkin's approach was that he was "mistaking bookkeeping for causality".
I've commented on this post, now. I avoided spam traps too. :-)