Truth and Reconciliation for Group Selection XIV: Group Selection in the Laboratory

In the storybook portrayal of science, theories are tested by experiments, which are conducted in laboratories so that the conditions can be rigorously controlled.

How would group selection be tested in the laboratory? Let's begin with the thousands of selection experiments that have already been conducted in the laboratory at the individual level. A population of animals, such as fruit flies or chickens, is measured for a particular trait, such as bristle number or egg productivity. Individuals that score high or low (depending upon the desired direction of selection) for the trait are selected to breed the next generation. If the average value of the trait in the offspring generation shifts in the direction of selection, then the trait is heritable and there has been a response to selection. Over many generations, artificial selection can cause organisms to become completely different from their ancestors, as our domesticated plants and animals attest.

Group selection can be studied in the laboratory by a simple extension of the protocol outlined above. A population of groups is created, a particular trait is measured for the groups, and the highest (or lowest) scoring groups are used to breed the next generation. If the average value of the trait in the offspring generation shifts in the direction of selection, then group selection is proven to be efficacious, at least under the conditions of the laboratory experiment.

To make the procedure less abstract, consider my favorite group selection experiment, which I have written about in Evolution for Everyone. 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.

By the way, the groups of chickens were siblings. When some of my colleagues learn this fact, they shout "Aha! It's kin selection, not group selection!" Wrong. The groups were siblings in both methods, so their kinship cannot explain the difference between the methods. As I relate in T&R XIII, everything about kin selection theory can be understood in terms of the parameters of multilevel selection theory. Creating groups of siblings caused the psychopaths to cluster in some groups and the peaceniks to cluster in other groups, providing lots of variation to select upon at the group level. Psychopaths still beat peaceniks within each group; the fact that they were siblings is beside the point.

This experiment also raises important questions about what counts as an individual trait. Egg productivity seems like an individual trait because you can count the eggs coming out the hind end of a hen. The experiment reveals that egg productivity is in fact a highly social trait that depends upon the genetic composition of one's group, not just the individual's genetic composition. This example has profound consequences for how we think about human traits that seem individual but in fact are highly social.

This is only one of many experiments demonstrating the efficacy of group selection in the laboratory, for creatures as diverse as insects, plants, and vertebrates. In 1997, I organized a symposium on multilevel selection in my capacity as Vice President of the American Society of Naturalists, one of the premier evolution-oriented societies. The symposium took place at their annual meeting and was published as a special issue in the American Naturalist, arguably the premier journal for evolutionary research at the time. Among the speakers was John Maynard Smith, one of the premier evolutionists in the world and a chief critic of group selection, as I recount in T&R VIII and IX. I mention these credentials not to boast, but to emphasize how much the symposium occupied center stage in the world of evolutionary biology.

Another speaker at the symposium was Charles Goodnight, a student of Michael Wade, who conducted the first group selection experiments in the 1970's. Charles reviewed the literature and concluded that every group selection experiment conducted in the laboratory demonstrated an efficacious role for between-group selection, even when between-group selection was opposed by within-group selection. You can judge for yourself from the published version of Charles' talk (co-authored with Laurie Stevens) titled "Experimental Studies of Group Selection: What Do They Tell Us About Group Selection in Nature?", which is available on his website.

As Charles recently recounted to me, he was convinced that his talk would be a career-maker for himself and a turning point for acceptance of group selection. Why not, given the import of his conclusions for one of the most important controversies in evolutionary theory, the prominent forum, and the likes of John Maynard Smith in the audience? He was sorely disappointed. The laboratory evidence for group selection had virtually no impact on the acceptance of group selection by the evolutionary community at large. So much for the storybook portrayal of science.

The only legitimate reason to discount the results of a laboratory experiment is when the conditions are highly artificial, therefore irrelevant to real-world situations. But this is not the case for the group selection experiments, in which groups are formed much as they might form in nature. Moreover, the whole beauty of laboratory experiments is that conditions can be varied in a systematic fashion. If a critic thinks that the conditions of one experiment are artificial, the answer is to conduct another experiment, not to discount laboratory evidence entirely.

In fact, group selection is so efficacious in the laboratory that even the proponents of group selection were surprised. As often happens, the laboratory experiments revealed factors operating in real biological systems that were beyond the imagination of the theorists. In particular, the theorists had limited their models to traits with a simple genetic basis, such as selfish and altruistic genes that code directly for selfish and altruistic behaviors. Given this assumption, phenotypic variation among groups corresponds directly to genetic variation among groups, which in turn depends critically on the number of individuals initiating each group. The larger the initial group size, the less variation among groups for between-group selection to act upon. That is the entire import of kin selection and the early conclusion that group selection requires special conditions, such as small initial group size, to be efficacious.

In the laboratory, groups vary substantially at the phenotypic level, even when they are initiated by large numbers of individuals -- because the relationship between the genetic composition of a group and its phenotype is complex rather than simple. Even when groups initially vary by only a small amount, complex interactions within groups causes them to become more variable over time, a kind of "butterfly effect" that also accounts for why complex physical systems, such as the weather, are so variable.

An experiment that I performed my former student, William Swenson, will make this idea less abstract. 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.

Even though the initial variation among pots was miniscule based on the large number of microbes colonizing each pot, variation did not stay miniscule because each pot was a complex biological system. Just as a butterfly flapping its wings can change the trajectory of a complex physical system such as the weather, each pot embarked upon a separate trajectory during the course of the first plant generation. This was apparent even to the naked eye; for example, some pots but not others developed a mat of algae over the surface of the soil. These differences made a difference for plant growth, so that by selecting the soil from beneath the largest and smallest plants, we were selecting microbial ecosystems that caused the plants to become large or small. Over a number of ecosystem "generations" (each comprising many microbial generations), the high and low selected lines diverged from each other -- proof that variation among ecosystems was heritable. This work was published in one of the nation's premier science journals, the Proceedings of the National Academy of Sciences. Once again, I say this not to boast, but to demonstrate that if multilevel selection experiments in the laboratory have failed to have an impact, it is not for lack of legitimacy or exposure. As with Goodnight's review of the literature, however, our experiment had virtually no impact on attitudes about group selection by the evolutionary community at large.

Muir's chicken experiment and our soil ecosystem experiment show that multilevel selection is not just an arcane scientific subject; it can be put to practical use. The eggs in your refrigerator come from group selected hens, regardless of what you might think of group selection. In a second set of experiments, Bill Swenson and I selected microbial ecosystems to degrade a toxic compound. In his current research, Bill Muir and his colleagues are using group selection to create strains of livestock that have not been inadvertently selected to make each other miserable. What else might we select groups and ecosystems to do?

Multilevel selection experiments in the laboratory vividly illustrate why a truth and reconciliation process is needed for the subject of group selection. The experiments are published in the best journals because a core group of evolutionists does understand their import. For them, the storybook portrayal of science actually takes place. For the evolutionary community at large, however, the rules governing the acceptance and rejection of group selection are a different story.

Comments

[whitecap]

Dr, Wilson, in a commentary on a paper by Henrich you suggest that some of what Henrich attributes to the action of culture – behavioural conformity among groups of genetically diverse individuals – can be more generally attributed to complex genotype–phenotype relationships, concluding that “this does not diminish the importance of the cultural mechanisms discussed in the target article but it does encourage us to look for additional possibilities in human and nonhuman complex systems alike”. In “A Farewell to Alms” Gregory Clark tries to overturn cultural institutional explanations for why the Industrial Revolution began in Britain in favor of a “survival of the richest” thesis that contends downward social mobility and high urban mortality among the poor caused the spread of traits favorable to industrialization through British society. I’m not too sure of the aptness of this example but it seems to be getting at this idea of the magnification of small initial genetic differences by complex interactions. At any rate, the historical and ethnographic record doesn’t appear sufficient to definitively settle the argument, so I’m wondering if you think modeling and other analytical tools are able to shed much light on ambitious questions of this kind yet?

[whitecap]

I forgot to add the link to Joseph Henrich's (2004) paper (which includes Dr. Wilson's commentary), "Cultural group selection, coevolutionary processes and large-scale cooperation" in Journal of Economic Behavior & Organization, a manuscript copy of which is available here:
http://www.psych.ubc.ca/~henrich/Website/Papers/HenrichplusCommentsJebo2003.pdf

[biogxh]

The number of the offspring in a group is significant index of the group selection. But in some degree, it is different from Wynne-Edwards' thoughts. He thought group selection also has ability to regulate the population. Therefore, in my opinion, it seems to be a controversy how to define the index of the group selection.

[markus7]

Dr Wilson,

The chicken and the soil microbe group selection experiments are charming, practical examples of the reality and underexploited power of group selection.

But even so, group selection’s responsibility for the natural evolution of traits like human unselfishness and cooperation seems to me to have sometimes been overstated. Game theory shows that, in environments where specific levels of benefits from cooperation exist, good cooperators (individuals who are unselfish but provokable to retaliation when treated unfairly) can individually receive, on average and in the long term, more benefits than poor cooperators provided selfish individuals (unfair cooperators) are identified and punished. Clearly defining when a trait like unselfishness (as part of being a good cooperator) can be an evolutionarily successful strategy without reference to group selection should help the case for acceptance of group selection by limiting the claims for group selection.

Have you already done this and I missed it, or perhaps you interpret the above results from game theory as only revealing strategies about how to split an existing group into cooperative and non-cooperative subgroups for group selection to act on?

Mark

[royniles]

My first attempt to post a reply here has been either moderated out or lost in cyberspace. I thought it was quite civil, even though critical, but in any case I won't repeat it.
Instead I'd just like to ask, Is there a gene for psychopathy in chickens?

[royniles]

Aha, the critical post was refused, but the non-critical has been accepted. Well, I've had my say earlier and these examples of real life test subjects instead of some computer models have supported my contentions about strategies - as opposed to Dr. Wilson's about selfishness or altruism being simply genetically determined. Because perhaps he hasn't discovered the mechanism for the adaptation of strategic algorithms. But in any case, my work here has been done in.

[markus7]

Hi Royniles, I’ll put in my 2 cents worth of opinion.

It seems sensible there are genes that increase aggression and an urge to dominate other chickens (to be on the top of the pecking order). Selecting for these genes based on the dominant chicken easily laying the most eggs due to her aggression suppressing egg laying in the other chickens probably accounts for the experimental results. If genes for psychopathy in people exist and are the source of a pyschopath’s lack of conscience, then a corresponding mental illness in chickens might be closer to a mother chicken who does not take care of her chicks (and feels no motivation to do so) rather than a chicken who tries to dominate all the others as in the example which is just intensifying a normal urge.

[royniles]

markus7,
Choices of strategies that exist in chickens are different from the choices available to humans.
Humans are socialized differently than chickens, and the type of conscience that a human may or may not have been born with, or failed to have developed later, will arguably not be found in chickens. And I believe I can explain how the differences in pecking orders, either among chickens, among humans, or between chickens and humans, are strategic, although the ranges of strategic options are of course genetic.
But I'm not about to offer such an explanation to a site that reserves the right to omit any presentation that makes its censors uncomfortable.
In any case, the subject of the comment that was apparently banned was the significance I found in the differences noted in the results of the modeling research previously presented and those of the present efforts that involved actual chickens and microbial systems.

[royniles]

As to specific genes that .increase aggression, they are no more likely than genes for altruism of selfishness. Here's a clue as to why:
From Wilson's paper, EVOLUTIONARY SOCIAL CONSTRUCTIVISM:
"The key concept -- is behavioral flexibility, also called phenotypic plasticity. No organism is so simple that it is instructed by its genes to “do x”. Even bacteria and protozoa are genetically endowed with a set of if-then rules of the form “do x in situation 1”, “do y in situation 2” and so on. These rules enable organisms to do the right thing at the right time, not only behaviorally but physiologically and morphologically. ---"

But I'd ague that it’s more like “do x strategy in response to y strategy, and y strategy in response to z strategy,” etc. Each species may have particular scenarios with symbols of strategic entities to be wary of, such as snakes, etc. And these could carry over when species adapt or branch off, but more importantly, the STRATEGIES THEMSELVES will evolve to encompass new varieties of strategic entities.
Hence we don't need the many thousands of alleged "if-then" rules that we supposedly inherited from primitive man, etc. Strategies are "intelligent" in that they are optional systems in and of themselves. They are the essence of the brain's apparent plasticity - they are "option wiring" instead of hard wiring. They are central to the brain's "experiential learning" apparatus.

[royniles]

However, rather than give examples of biological strategies, which won't be welcome on this blog, let me add commentary to these excerpts from the initial post:

"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.­"
(Comment: Misstating first that this "human directed" selection was a definitive form of natural selection, and second, that fitness is relative only to laying more eggs, since again it's a fitness index selected by other than chicken "societies" themselves - hatchable quality of eggs may be more important, and "character" of the resultant chicks may be as well.)
"The first method favored the nastiest hens who achieved their productivity by suppressing the productivity of other hens."
(Stacking the deck already?)
"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."
(This doesn't show that exceptional egg laying was ever thought good for the group by even chickens themselves­.)

[royniles]

"That's why the second method worked. Selecting the most productive groups favored peaceful and cooperative hens, despite their selective disadvantage within groups."
(False - they had no such selective advantage.­)
"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."
(Proving my point, that chickens didn't see cooperative hens as being at a disadvantage compared to extra egg layers. They didn't give the chicken's futures any advantage even if chickens don't knowingly plan their own futures.)
"Muir's experiment proves the efficacy of group selection, at least under the conditions of the experiment­."
(But of course it "proves" nothing of the sort, since if anything it demonstrates the opposite.)

[dynwit]

"...caused the psychopaths to cluster in some groups and the peaceniks to cluster in other groups."

Doesn't that just say it all?

[JohnFromCensornati]

Birthers in just six generations!

[HeevenSteven]

Lol!