Group selection

In evolutionary biology, group selection refers to the idea that alleles can become fixed or spread in a population because of the benefits they bestow on groups, regardless of the alleles' effect on the fitness of individuals within that group.

Group selection was used as a popular explanation for adaptations, especially by V. C. Wynne-Edwards.^[1][2] For several decades, however, critiques, particularly by George C. Williams,^[3] John Maynard Smith^[4] and C.M. Perrins (1964), cast serious doubt on group selection as a major mechanism of evolution, and though some scientists have pursued the idea over the last few decades, only recently have group selection models seen a resurgence.^[5][6][7]

Overview

Specific syndromes of selective factors can create situations where groups are selected because they display group properties that are selected-for. Some mosquito-transmitted rabbit viruses, for instance, are only transmitted to uninfected rabbits from infected rabbits that are still alive. This creates a selective pressure on every group of viruses already infecting a rabbit not to become too virulent and kill their host rabbit before enough mosquitoes have bitten it. In natural systems such viruses display much lower virulence levels than do mutants of the same viruses that in laboratory culture readily out-compete non-virulent variants (or than do tick-transmitted viruses—ticks, unlike mosquitoes, bite dead rabbits).

However, theoretical models of the 1960s seemed to imply that the effect of group selection was negligible. Alleles are likely to be held on a population-wide level, leaving nothing for group selection to select for. Additionally, generation time is much longer for groups than it is for individuals. Assuming conflicting selection pressures, individual selection will occur much faster, swamping any changes potentially favored by group selection. The Price equation can partition variance caused by natural selection at the individual level and the group level, and individual level selection generally causes greater effects.

Experimental results starting in the late 1970s demonstrated that group selection was far more effective than the then-current theoretical models had predicted.^[8] A review of this experimental work has shown that the early group selection models were flawed because they assumed that genes acted independently, whereas in the experimental work it was apparent that gene interaction, and more importantly, genetically based interactions among individuals, were an important source of the response to group selection (e.g.^[9]). As a result many are beginning to recognize that group selection, or more appropriately multilevel selection, is potentially an important force in evolution.

More recently, Yaneer Bar-Yam has claimed that the gene-centered view (and thus Ronald Fisher's treatment of evolution) relies upon a mathematical approximation that is not generally valid. Bar-Yam argues that the approximation is a dynamic form of the Mean Field approximation frequently used in physics and whose limitations are recognized there. In biology, the approximation breaks down when there are spatial populations resulting in inhomogeneous genetic types (called symmetry breaking in physics). Such symmetry breaking may also correspond to speciation.

Spatial populations of predators and prey have also been shown to show restraint of reproduction at equilibrium, both individually^[10] and through social communication,^[11] as originally proposed by Wynne-Edwards. While these spatial populations do not have well-defined groups for group selection, the local spatial interactions of organisms in transient groups are sufficient to lead to a kind of multi-level selection. There is however as yet no evidence that these processes operate in the situations where Wynne-Edwards posited them; Rauch et al.'s analysis,^[10] for example, is of a host-parasite situation, which was recognised as one where group selection was possible even by E. O. Wilson (1975), in a treatise broadly hostile to the whole idea of group selection.^[12] Specifically, the parasites do not individually moderate their transmission; rather, more transmissible variants "continually arise and grow rapidly for many generations but eventually go extinct before dominating the system."

The haystack model and trait groups

Maynard Smith can be credited with what has become known as the "haystack model" of group selection. As a non-mathematical introduction to the idea, imagine a group of animals that spend most of their time living and breeding in haystacks but that occasionally all come out of their haystacks simultaneously, mix together and then separate into equal groups, which once again go off to inhabit separate haystacks. We can then imagine a trait that benefits each haystack group, perhaps leading to behaviorally altruistic acts that cost an individual some fitness but enhance the fitness of its group even more, and a selfish trait that, for the purposes of this discussion, we can call the absence of the altruistic trait.

Each of these two traits works on a different level of selection. Within the individual haystacks the selfish organisms benefit in terms of evolutionary fitness. This is because the selfish organisms benefit from the actions of the altruistic organisms but do not pay any of the evolutionary costs for being altruistic (sacrificing some good for that of others). Thus, in each generation the number of altruists in the group would shrink compared to the number of selfish organisms. As a result one might first think that a group beneficial trait, especially an altruistic one, would be doomed to eventually die out. But we must remember the strange nature of these hypothetical organisms. Every so often, at the same time, all the members of all the haystacks form one large group, randomly assort into equal groups, and then move back into the haystacks. Because of this an altruistic behavior can take hold by the following reasoning. While the number of selfish organisms in each haystack increases in percentage every generation, the total population of haystacks that contain altruists produce more offspring over all than those that do not. This means that populations with altruists are going to be over-represented when all the haystacks are abandoned to form a larger group. So long as the number of generations spent in each haystack is not so long as to dramatically reduce the number of altruists, and so long as the group benefit of the altruistic trait is significant enough, the number of altruists in all the haystack populations can rise.

However, though Maynard Smith gave a mathematical model by which group selection might work, he was skeptical that it would happen in nature often enough to be worth considering. His reasoning was that the specific conditions for group selection to take hold, namely the repeated isolation, mixture, and reisolation of organisms would be so rare and unlikely to occur in nature that it was almost certainly not a significant evolutionary force.

In their 1998 book Unto Others, and in various articles before this, Sober and David Sloan Wilson challenge this view. While one of their challenges takes the form of naming organisms, such as the so called "brain worm" (Dicrocoelium dendriticum), which has a life cycle much like that of the haystack organisms above, they present a more significant argument, based on the notion of trait groups.

Trait groups can occur within larger groups through the interaction of particular genetic traits, and need not interact for a generation to promote survival value. Sober and Wilson see kin selection, which is often considered an alternative to group selection, as a special case of a trait groups. To see how a trait group could be beneficial, let's imagine an altruist trait, such as cooperation with another organism even in such cases where it only benefits 40% as much as the organism it helps, and a selfish trait such as cooperating with another organism only when it will benefit more than the organism it helps. The first trait is considered altruistic in Sober and Wilson’s sense because the within-group fitness of the altruistic organism drops every time it cooperates compared with the other member of the group. Now imagine five organisms, one of which is altruistic in regards to this trait, and the rest of which are selfish. Assume that each case of cooperation increases the chance of survival and reproduction by 10 units, which is divided among the interacting pair (group of two). Now assume that member of the population groups/interacts with each other member of the population one time. After all the interactions have taken place, the selfish organisms have each acquired 6 units. This is because they all refuse to cooperation with other selfish members (since it is impossible for both members to benefit more than the other), but each takes advantage of the altruist benefits over that individual in a ratio of 60% to 40%. The altruist on the other hand has interacted with 4 selfish organisms and thus has earned 16 units (four for each encounter) and thus has a greater survival advantage than the selfish members of the population. The altruist ends up winning the survival "war" even though it came out behind in every survival "battle".

Because individuals can form hundreds or even thousands of trait groups within its life span, the trait group selection model does not have to rely on the unlikely situation of an entire population isolating into groups, merging, and then isolating into groups again. Likewise the rate at which trait groups can form and dissolve can be many times faster than the rate at which individuals reproduce, providing cumulative as opposed to all-or-nothing benefits. It is important to note that this argument has not settled the issue of group selection however. There is still heavy debate as to whether or not such formations count as “real” groups in the traditional biological sense of groups affected by group selection.

Multilevel selection theory

See also: Unit of selection

In recent years, the limitations of earlier models have been addressed, and newer models suggest that selection may sometimes act above the gene level. Recently David Sloan Wilson and Elliot Sober have argued that the case against group selection has been overstated. They focus their argument on whether groups can have functional organization in the same way individuals do and, consequently, whether groups can also be "vehicles" for selection. For example, groups that cooperate better may have out-reproduced those that did not. Resurrected in this way, Wilson & Sober's new group selection is usually called multilevel selection theory.^[13]

David Sloan Wilson, the developer of Multilevel Selection Theory (MLS) compares the many layers of competition and evolution to the “Russian Matryoska Dolls” within one another.^[7] The lowest level is the genes, next come the cells, and then the organism level and finally the groups. The different levels function cohesively to maximize fitness, or reproductive success. After establishing these levels, MLS goes further by saying that selection for the group level, which is competition between groups, must outweigh the individual level, which is individuals competing within a group, for a group-beneficiating trait to spread.^[14] MLS theory focuses on the phenotype this way because it looks at the levels that selection directly acts upon.^[7]

MLS theory does not lean towards individual or group selection but can be used to evaluate the balance between group selection and individual selection on a case-by-case scenario.^[14] Some experiments done imply that group selection can prevail, such as the experiment conducted by William Muir of Purdue University comparing egg productivity in hens. In the experiment, he demonstrates the existence of group selection by showing that in individual selection, a hyper-aggressive strain had been produced that led to many fatal attacks only after six generations.^[15] Group selection has been most often postulated in humans and, notably, social insects that make cooperation a driving force of their adaptations over time.^[16]

For humans, a highly pro-social, cognitive thinking species, social norms can be seen as a means of reducing the individual level variation and competition and shift selection in humans to the group level. Wilson ties the MLS theory regarding humans to another upcoming theory known as gene-culture evolution by acknowledging that culture seems to characterize a group-level mechanism for human groups to adapt to environmental changes.^[14] Methods of testing MLS include social psychological experimentation and multilevel modeling equations.

Wilson & Sober's work has been part of a revival of interest in multilevel selection as an explanation for evolutionary phenomena. Indeed, in a 2005 article,^[17] E. O. Wilson argued that kin selection could no longer be thought of as underlying the evolution of extreme sociality, for two reasons. First, some authors have shown that the argument that haplodiploid inheritance, characteristic of the Hymenoptera, creates a strong selection pressure towards nonreproductive castes is mathematically flawed.^[18] Second, eusociality no longer seems to be confined to the hymenopterans; increasing numbers of highly social taxa have been found in the years since Wilson's foundational text on sociobiology was published in 1975,^[12] including a variety of insect species, as well as a rodent species (the naked mole rat). Wilson suggests the equation for Hamilton's rule:^[19]

rb > c

(where b represents the benefit to the recipient of altruism, c the cost to the altruist, and r their degree of relatedness) should be replaced by the more general equation

(rb_k + b_e) > c

in which b_k is the benefit to kin (b in the original equation) and b_e is the benefit accruing to the group as a whole. He then argues that, in the present state of the evidence in relation to social insects, it appears that b_e>rb_k, so that altruism needs to be explained in terms of selection at the colony level rather than at the kin level. However, it is well understood in social evolution theory that kin selection and group selection are not distinct processes, and that the effects of multi-level selection are already fully accounted for in Hamilton's original rule, rb>c.^[20]

Group selection indicated by gene-culture coevolution

Gene-culture coevolution is a modern hypothesis (applicable mostly to humans) that combines evolutionary biology and modern sociobiology to indicate group selection.^[21] It treats culture as a separate evolutionary system that acts in parallel to the usual genetic evolution to transform human traits. It is believed that this approach of combining genetic influence with cultural influence over several generations is not present in the other hypotheses such as reciprocal altruism and kin selection, making gene-culture evolution one of the strongest realistic hypotheses for group selection. Fehr provides evidence of group selection taking place in humans presently with experimentation through logic games such as prisoner’s dilemma, the type of thinking that humans have developed many generations ago.^[22]

Gene-culture coevolution, or cumulative cultural evolution, allows humans to culturally evolve highly distinct adaptations to the local pressures and environments much quicker than with genetic evolution alone. Robert Boyd and Peter J. Richerson, two strong proponents of cultural evolution, postulate that the act of social learning, or learning in a group as done in group selection, allows human populations to accrue information over many generations.^[23] This leads to the cultural evolution of highly adaptive behaviors and technology alongside genetic evolution. Specifically, they believe that the ability to collaborate with each other evolved during the Middle Pleistocene, a million years ago, in response to a rapidly-changing climate.^[23]

Herbert Gintis approaches cultural evolution of group selection in a much more statistical approach to prove that societies that promote pro-social norms, as in group selection, have higher survival rates than societies that do not.^[24] He does so by developing a multilevel gene-culture coevolutionary model that explains the process whereby altruistic social norms will hinder socially harmful and fitness reducing norms and consequently will be internalized. In his equations, he differentiates between a genetic group selection model that is sensitive to group size and migration rates versus his own model that is much less affected by these constraints and therefore more accurate.^[25]

Group selection due to differing ESSs

The problem with group selection is that for a whole group to get a single trait, it must spread through the whole group first by regular evolution. But, as J. L. Mackie suggested, when there are many different groups, each with a different Evolutionarily Stable Strategy (ESS), there is selection between the different ESSs, since some are worse than others.^[26] For example, a group where altruism arose would outcompete a group where every creature acted in its own interest.

Criticism

The evolutionary biologist Jerry Coyne noted:^[27]

Group selection isn’t widely accepted by evolutionists for several reasons. First, it’s not an efficient way to select for traits, like altruistic behavior, that are supposed to be detrimental to the individual but good for the group. Groups divide to form other groups much less often than organisms reproduce to form other organisms, so group selection for altruism would be unlikely to override the tendency of each group to quickly lose its altruists through natural selection favoring cheaters. Further, we simply have little evidence that selection on groups has promoted the evolution of any trait. Finally, other, more plausible evolutionary forces, like direct selection on individuals for reciprocal support, could have made us prosocial. These reasons explain why only a few biologists, like Wilson and E. O. Wilson (no relation), advocate group selection as the evolutionary source of cooperation.

Richard Dawkins and fellow advocates of the gene-centered view of evolution remain unconvinced about group selection.^[28][29][30] In particular, Dawkins suggests that group selection fails to make an appropriate distinction between replicators and vehicles.^[31]

See also

• Eva Jablonka
• Group Selection, a 1971 book, by G. C. Williams, arguing against group selection
• Collective identity
• Battle trance

References

• Sober, Elliott and Wilson, David Sloan (1998). Unto Others: The Evolution and Psychology of Unselfish Behavior. Harvard University Press.

1. ^ Wynne-Edwards, V.C. (1962). Animal Dispersion in Relation to Social Behaviour. Edinburgh: Oliver & Boyd.
2. ^ Wynne-Edwards, V. C. (1986) Evolution Through Group Selection, Blackwell. ISBN 0-632-01541-1
3. ^ Williams, G.C. (1972) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press.ISBN 0-691-02357-3
4. ^ Maynard Smith, J. (1964). "Group selection and kin selection". Nature 201 (4924): 1145–1147. doi:10.1038/2011145a0. 
5. ^ Koeslag, J.H. (1997). Sex, the prisoner's dilemma game, and the evolutionary inevitability of cooperation. J. theor. Biol. 189, 53--61
6. ^ Koeslag, J.H. (2003). Evolution of cooperation: cooperation defeats defection in the cornfield model. J. theor. Biol. 224, 399-410
7. ^ ^{a b c} Wilson, D. S., & Wilson, E. O. (2008). Evolution "for the good of the group". [Article]. American Scientist, 96(5), 380-389.
8. ^ Wade, M. J. (1977). "An experimental study of group selection". Evolution 31 (1): 134–153. doi:10.2307/2407552. JSTOR 2407552. 
9. ^ Goodnight, C. J. and L. Stevens. 1997. Experimental studies of group selection: What do they tell us about group selection in nature. American Naturalist 150:S59–S79.
10. ^ ^{a b} Rauch, E. M., Sayama, H., & Bar-Yam, Y. (2003). Dynamics and genealogy of strains in spatially extended host-pathogen models. Journal of Theoretical Biology, 221, 655–664 [1].
11. ^ Werfel, J.; Bar-Yam, Y. (2004). "The evolution of reproductive restraint through social communication". Proceedings of the National Academy of Sciences of the United States of America 101 (30): 11019–11020. doi:10.1073/pnas.0305059101. 
12. ^ ^{a b} Wilson, E.O. 1975. Sociobiology: The New Synthesis Belknap Press, ISBN 0-674-81621-8.
13. ^ link Wilson, D.S. & Sober, E. 1994. Reintroducing group selection to the human behavioral sciences. Behavioral and Brain Sciences 17 (4): 585–654.
14. ^ ^{a b c} O'Gorman, R., Wilson, D. S., & Sheldon, K. M. (2008). For the good of the group? Exploring group-level evolutionary adaptations using multilevel selection theory. [Article]. Group Dynamics-Theory Research and Practice, 12(1), 17-26. doi: 10.1037/1089-2699.12.1.17
15. ^ Muir, W. M. (2009). Genetic selection and behaviour. [Meeting Abstract]. Canadian Journal of Animal Science, 89(1), 182-182.
16. ^ Boyd, R., & Richerson, P. J. (2009). Culture and the evolution of human cooperation.
17. ^ Wilson, E. O. (2005). Kin Selection as the Key to Altruism: its Rise and Fall. "Social Research" 72 (1): 159–166.
18. ^ Trivers, R. (1976) Science 191(4224), 250-263
19. ^ Hamilton, W.D. (1964). "The evolution of social behavior". Journal of Theoretical Biology 1: 295–311. 
20. ^ linkWest, S.A., Griffin, A.S. & Gardner, A. (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection Journal of Evolutionary Biology 20:415-432.
21. ^ Mesoudi, A., & Danielson, P.(2008). Ethics, evolution and culture. [Review]. Theory in Biosciences, 127(3), 229-240. doi: 10.1007/s12064-008-0027-y
22. ^ Fehr, E.; Fischbacher, Urs (2003). "The nature of human altruism. [Review]". Nature 425 (6960): 785–791. doi:10.1038/nature02043. PMID 14574401. 
23. ^ ^{a b} Boyd, R., & Richerson, P. J. (2009). Culture and the evolution of human cooperation.
24. ^ Gintis, H. (2003). "The hitchhiker's guide to altruism: Gene-culture coevolution, and the internalization of norms". Journal of Theoretical Biology 220 (4): 407–418. doi:10.1006/jtbi.2003.3104. PMID 12623279. 
25. ^ Gintis, H. (2003). The hitchhiker's guide to altruism: Gene-culture coevolution, and the internalization of norms. Journal of Theoretical Biology, 220(4), 407-418. doi: 10.1006/jtbi.2003.3104
26. ^ The selfish Gene (Richard Dawkins)
27. ^ Coyne, J. A. (2011). Can Darwinism Improve Binghamton? New York Review of Books, September 9, 2011. http://www.nytimes.com/2011/09/11/books/review/the-neighborhood-project-by-david-sloan-wilson-book-review.html?_r=2&pagewanted=all
28. ^ See the chapter God's utility function in Dawkins, Richard (1995). River Out of Eden. New York: Basic Books. ISBN 0-465-06990-8. 
29. ^ link Dawkins, R. (1994). Burying the Vehicle. Commentary on Wilson & Sober: Group Selection. Behavioural and Brain Sciences. 17 (4): 616–617.
30. ^ link Dennett, D.C. (1994). E Pluribus Unum? Commentary on Wilson & Sober: Group Selection. Behavioural and Brain Sciences. 17 (4): 617–618.
31. ^ Richard Dawkins, "Replicators and Vehicles," King's College Sociobiology Group, eds., Current Problems in Sociobiology, Cambridge, Cambridge University Press, (1982), pp. 45-64

Further reading

• Bergstrom, T.C. (2002). "Evolution of Social Behavior: Individual and Group Selection" (PDF). Journal of Economic Perspectives 16 (2): 67–88. doi:10.1257/0895330027265. http://www.econ.ucsb.edu/~tedb/Evolution/groupselection.pdf. 
• Bijma, P.; Muir, W.M.; Van Arendonk, J.A.M. (2007). "Multilevel Selection 1: Quantitative Genetics of Inheritance and Response to Selection". Genetics 175 (1): 277–288. doi:10.1534/genetics.106.062711. PMC 1775021. PMID 17110494. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1775021. 
• Bijma, P.; Muir, W.M.; Ellen, E. D.; Wolf, Jason B.; Van Arendonk, J.A.M. (2007). "Multilevel Selection 2: Estimating the Genetic Parameters Determining Inheritance and Response to Selection". Genetics 175 (1): 289–299. doi:10.1534/genetics.106.062729. PMC 1775010. PMID 17110493. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1775010. 
• Boyd, R.; Richerson, P.J. (2002). "Group Beneficial Norms Spread Rapidly in a Structured Population" (PDF). Journal of Theoretical Biology 215 (3): 287–296. doi:10.1006/jtbi.2001.2515. http://www.sscnet.ucla.edu/anthro/faculty/boyd/BoydRichersonJTB2002_Clean.pdf. 
• West, S.A.; Griffin, A.S.; Gardner, A. (2008). "Social semantics: how useful has group selection been?". Journal of Evolutionary Biology 21: 374–385. http://www3.interscience.wiley.com/cgi-bin/fulltext/119412422/PDFSTART. 
• Soltis, J.; Boyd, R.; Richerson, P.J. (1995). "Can Group-functional Behaviors Evolve by Cultural Group Selection? An Empirical Test" (PDF). Current Anthropology 63: 473–494. http://www.des.ucdavis.edu/faculty/richerson/SoltisBoydRichersonCA95.pdf. 
• Wilson, D. S. (1987). "Altruism in Mendelian populations derived from sibling groups: The haystack model revisited". Evolution 41 (5): 1059–1070. doi:10.2307/2409191. JSTOR 2409191. 
• Wilson, D.S. (2006). Human groups as adaptive units: toward a permanent consensus. In P. Carruthers, S. Laurence & S. Stich (Eds.), The Innate Mind: Culture and Cognition. Oxford: Oxford University Press. Full text

External links

• The Controversy of the Group Selection Theory - a review from the "Science Creative Quarterly" (a blog)
• Link to publications by D.S. Wilson