From the mid 1960s, evolutionary biologists such as John Maynard Smith argued that natural selection acted primarily at the level of the individual. They argued on the basis of mathematical models that individuals would not altruistically sacrifice fitness for the sake of a group. They persuaded the majority of biologists that group selection did not occur, other than in special situations such as the haplodiploid social insects like honeybees (in the Hymenoptera), where kin selection was possible.
In 1994 David Sloan Wilson and Elliott Sober argued for multi-level selection, including group selection, on the grounds that groups, like individuals, could compete. In 2010 three authors including E. O. Wilson, known for his work on ants, again revisited the arguments for group selection, provoking a strong rebuttal from a large group of evolutionary biologists. As of yet, there is no clear consensus among biologists regarding the importance of group selection.
- 1 Good of the species
- 2 Selfish selection
- 3 Group selection revisited
- 4 Criticism
- 5 References
- 6 Further reading
- 7 External links
Good of the species
Once Darwinism had been accepted, animal behavior was glibly explained with unsubstantiated hypotheses about survival value, which was largely taken for granted. The naturalist Konrad Lorenz had argued loosely in books like On Aggression (1966) that animal behavior patterns were "for the good of the species", without actually studying survival value in the field; the ethologist Niko Tinbergen praised Lorenz for his interest in the survival value of behavior, and naturalists enjoyed Lorenz's writings for the same reason. In 1962, group selection was used as a popular explanation for adaptation by the zoologist V. C. Wynne-Edwards.
From the mid 1960s, evolutionary biologists argued that natural selection acted primarily at the level of the individual. In 1964, John Maynard Smith, C.M. Perrins (1964), and George C. Williams in his 1966 book Adaptation and Natural Selection cast serious doubt on group selection as a major mechanism of evolution; Williams's 1971 book Group Selection assembled writings from many authors on the same theme.
The great majority of evolutionary biologists believe (2011) that selection above the level of the individual is a special case, probably limited to the unique inheritance system (involving haplodiploidy) of the eusocial Hymenoptera such as honeybees, which encourages kin selection.
Group selection revisited
Experiments from the late 1970s suggested that group selection involving altruism was possible. Early group selection models were flawed because they assumed that genes acted independently; but genetically-based interactions among individuals are ubiquitous in group formation because genes must cooperate for the benefit of association in groups to enhance the fitness of group members. On the other hand, kin selection is accepted as an explanation of altruistic behavior.
Since the 1990s, group selection models have seen a resurgence. Some biologists argue that kin selection and multilevel selection are both needed to "obtain a complete understanding of the evolution of a social behavior system".
In 2010 three authors including E. O. Wilson argued for multi-level selection, including group selection, to correct what they saw as deficits in the explanatory power of inclusive fitness. The response was a back-lash from 137 other evolutionary biologists who argued "that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature".
Multilevel selection theory
In 1994 David Sloan Wilson and Elliott Sober argued that the case against group selection had been overstated. They considered whether groups can have functional organization in the same way as individuals, and consequently whether groups can be "vehicles" for selection. Groups that cooperate better might survive and reproduce more than those that did not. Resurrected in this way, Wilson & Sober's new group selection is called multilevel selection theory.
Wilson compared the layers of competition and evolution to nested sets of Russian matryoshka dolls. The lowest level is the genes, next come the cells, then the organism level and finally the groups. The different levels function cohesively to maximize fitness, or reproductive success. The theory asserts that selection for the group level, involving competition between groups, must outweigh the individual level, involving individuals competing within a group, for a group-beneficiating trait to spread. Multilevel selection theory theory focuses on the phenotype because it looks at the levels that selection directly acts upon. For humans, social norms can be argued to reduce individual level variation and competition, thus shifting selection to the group level. Wilson ties the multilevel selection theory theory regarding humans to another theory, gene-culture coevolution, by acknowledging that culture seems to characterize a group-level mechanism for human groups to adapt to environmental changes.
MLS theory can be used to evaluate the balance between group selection and individual selection in specific cases. An experiment by William Muir compared egg productivity in hens, showing that a hyper-aggressive strain had been produced through individual selection, leading to many fatal attacks after only six generations; by implication,it could be argued that group selection must have been acting to prevent this in real life. Group selection has most often been postulated in humans and, notably, eusocial Hymenoptera that make cooperation a driving force of their adaptations over time and have a unique system of inheritance involving haplodiploidy that allows the colony to function as an individual while only the queen reproduces.
Wilson & Sober's work revived interest in multilevel selection. In a 2005 article, E. O. Wilson argued that kin selection could no longer be thought of as underlying the evolution of extreme sociality, for two reasons. First, he suggested, the argument that haplodiploid inheritance (as in the Hymenoptera) creates a strong selection pressure towards nonreproductive castes is mathematically flawed. 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, including a variety of insect species, as well as two rodent species (the naked mole-rat and the Damaraland mole rat). Wilson suggests the equation for Hamilton's rule:
- 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
- rbk + be > c
in which bk is the benefit to kin (b in the original equation) and be 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 be>rbk, so that altruism needs to be explained in terms of selection at the colony level rather than at the kin level. However, kin selection and group selection are not distinct processes, and the effects of multi-level selection are already accounted for in Hamilton's rule, rb>c, provided that an expanded definition of r, not requiring Hamilton's original assumption of direct genealogical relatedness, is used, as proposed by E. O. Wilson himself.
Spatial populations of predators and prey show restraint of reproduction at equilibrium, both individually and through social communication, 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, 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. 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."
A variant of group selection theory rooted in the idea of population viscosity (limited offspring dispersal), first proposed by Hamilton (1964), is widely present in natural populations. This population structure builds a continuum between individual selection, kin selection, kin group selection and group selection without a clear boundary for each level. However, early theoretical models by D.S. Wilson et al. (1992) and Taylor (1992) showed that pure population viscosity cannot lead to cooperation and altruism. This is because any benefit generated by kin cooperation is exactly cancelled out by kin competition; additional offspring from cooperation are eliminated by local competition. However, this exact cancelling out also suggests that any additional benefit of local cooperation would be sufficient to allow cooperation to evolve. Mitteldorf and D.S. Wilson (2000) later showed that if the population is allowed to fluctuate, then local populations can temporarily store the benefit of local cooperation and promote the evolution of cooperation and altruism. By assuming individual differences in adaptations, Yang (2013) further showed that the benefit of local altruism can be stored in the form of offspring quality and thus promote the evolution of altruism even if the population does not fluctuate. This is because local competition among more individuals resulting from local altruism increases the average local fitness of the individuals that survive.
Gene-culture coevolution in humans
Gene-culture coevolution (also called dual inheritance theory) is a modern hypothesis (applicable mostly to humans) that combines evolutionary biology and modern sociobiology to indicate group selection. 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.
Gene-culture coevolution allows humans to develop highly distinct adaptations to the local pressures and environments more quickly 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. This leads to cultural evolution of behaviors and technology alongside genetic evolution. Boyd and Richerson believe that the ability to collaborate evolved during the Middle Pleistocene, a million years ago, in response to a rapidly changing climate.
Differing evolutionarily stable strategies (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. For example, a group where altruism was universal would outcompete a group where every creature acted in its own interest, but the group of altruists would be vulnerable to cheating by non-altruists.
Implications in population biology
Social behaviors such as altruism and group relationships can impact many aspects of population dynamics, such as intraspecific competition and interspecific interactions. In 1871, Darwin argued that group selection occurs when the benefits of cooperation or altruism between subpopulations are greater than the individual benefits of egotism within a subpopulation. This supports the idea of multilevel selection, but kinship also plays an integral role because many subpopulations are composed of closely related individuals. An example of this can be found in lions, which are simultaneously cooperative and territorial. Within a pride, males protect the pride from outside males, and females, who are commonly sisters, communally raise cubs and hunt. However, this cooperation seems to be density dependent. When resources are limited, group selection favors prides that work together to hunt. When prey is abundant, cooperation is no longer beneficial enough to outweigh the disadvantages of altruism, and hunting is no longer cooperative.
Interactions between different species can also be affected by multilevel selection. The previously mentioned example of how group selection works on mosquito-borne viruses in rabbits demonstrates how parasite-host interactions are impacted. Predator-prey relationships can also be affected. Individuals of certain monkey species howl to warn the group of the approach of a predator. The evolution of this trait benefits the group by providing protection, but could be disadvantageous to the individual if the howling draws the predator's attention to them. By affecting these interspecific interactions, multilevel and kinship selection can change the population dynamics of an ecosystem.
Multilevel selection attempts to explain the evolution of altruistic behavior in terms of quantitative genetics. Increased frequency or fixation of altruistic alleles can be accomplished through kin selection, in which individuals engage in altruistic behavior to promote the fitness of genetically similar individuals such as siblings. However, this can lead to inbreeding depression, which typically lowers the overall fitness of a population. However, if altruism were to be selected for through an emphasis on benefit to the group as opposed to relatedness and benefit to kin, both the altruistic trait and genetic diversity could be preserved. However, relatedness should still remain a key consideration in studies of multilevel selection. Experimentally imposed multilevel selection on Japanese quail was more effective by an order of magnitude on closely related kin groups than on randomized groups of individuals.
The use of the Price equation to support group selection was challenged by van Veelen in 2012, arguing that it is based on invalid mathematical assumptions. Richard Dawkins and other advocates of the gene-centered view of evolution remain unconvinced about group selection. In particular, Dawkins suggests that group selection fails to make an appropriate distinction between replicators and vehicles. Psychologist Steven Pinker concluded that "Group Selection has no useful role to play in psychology or social science."  The evolutionary biologist Jerry Coyne summarized the arguments in the New York Review of Books in non-technical terms as follows:
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, little evidence exists 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 humans prosocial. These reasons explain why only a few biologists, like [David Sloan] Wilson and E. O. Wilson (no relation), advocate group selection as the evolutionary source of cooperation.
- Tudge, Colin (31 March 2011). Engineer In The Garden. Random House. p. 115. ISBN 978-1-4464-6698-8.
- Burkhardt, Richard W. (2005). Patterns of Behavior: Konrad Lorenz, Niko Tinbergen, and the Founding of Ethology. University of Chicago Press. p. 432. ISBN 978-0-226-08090-1.
- Wynne-Edwards, V.C. (1962). Animal Dispersion in Relation to Social Behaviour. Edinburgh: Oliver & Boyd.
- Wynne-Edwards, V. C. (1986) Evolution Through Group Selection, Blackwell. ISBN 0-632-01541-1
- Maynard Smith, J. (1964). "Group selection and kin selection". Nature 201 (4924): 1145–1147. doi:10.1038/2011145a0.
- Williams, G.C. (1972) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press.ISBN 0-691-02357-3
- Williams, G.C. (editor) (2008)  Group Selection, Transaction Publishers. ISBN 0-202-36222-1
- Nature 471, E1–E4 (24 March 2011) doi:10.1038/nature09831
- Wade, M. J. (1977). "An experimental study of group selection". Evolution 31 (1): 134–153. doi:10.2307/2407552. JSTOR 2407552.
- Goodnight, C. J.; Stevens, L. (1997). "Experimental studies of group selection: What do they tell us about group selection in nature". American Naturalist 150: S59–S79. doi:10.1086/286050.
- Wade, MJ; Wilson, DS; Goodnight, C; Taylor, D; Bar-Yam, Y; de Aguiar, MA; Stacey, B; Werfel, J; Hoelzer, GA; Brodie ED, 3rd; Fields, P; Breden, F; Linksvayer, TA; Fletcher, JA; Richerson, PJ; Bever, JD; Van Dyken, JD; Zee, P (Feb 18, 2010). "Multilevel and kin selection in a connected world.". Nature 463 (7283): E8–9; discussion E9–10. doi:10.1038/nature08809. PMC 3151728. PMID 20164866.
- Koeslag, J.H. (1997). "Sex, the prisoner's dilemma game, and the evolutionary inevitability of cooperation". Journal of Theoretical Biology 189: 53–61.
- Koeslag, J.H. (2003). "Evolution of cooperation: cooperation defeats defection in the cornfield model". Journal of Theoretical Biology 224: 399–410.
- Wilson, D. S.; Wilson, E. O. (2008). "Evolution 'for the good of the group'.". American Scientist 96 (5): 380–389. doi:10.1511/2008.74.1.
- Yang, Jiang-Nan (2013). "Viscous populations evolve altruistic programmed aging in ability conflict in a changing environment". Evolutionary Ecology Research 15: 527–543.
- Wilson, David Sloan (2010). "open letter to Richard Dawkins". scienceblogs.com. Self-published. Retrieved 12 January 2015.
- Goodnight, Charles (June 2013). "On multilevel selection and kin selection: Contextual analysis meets direct fitness". Evolution 67 (6): 1539–1548.
- Nature 466, 1057–1062 (26 August 2010) doi:10.1038/nature09205
- Wilson, D.S.; Sober, E. (1994). "Reintroducing group selection to the human behavioral sciences". Behavioral and Brain Sciences 17 (4): 585–654. doi:10.1017/s0140525x00036104.
- 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". Group Dynamics-Theory Research and Practice 12 (1): 17–26. doi:10.1037/1089-2622.214.171.124.
- Muir, W. M. (2009). "Genetic selection and behaviour". Canadian Journal of Animal Science 89 (1): 182–182.
- Boyd, R.; Richerson, P.J. (2009). "Culture and the evolution of human cooperation". Phil. Trans. R. Soc. B 364 (1533): 3281–3288.
- Wilson, E. O. (2005). "Kin Selection as the Key to Altruism: its Rise and Fall". Social Research 72 (1): 159–166.
- Trivers, R. (1976). "Haploidploidy and the evolution of the social insect". Science 191 (4224): 250–263. doi:10.1126/science.1108197. PMID 1108197.
- Wilson, E.O. (1975). Sociobiology: The New Synthesis. Belknap Press. ISBN 0-674-81621-8.
- Hamilton, W.D. (1964). "The evolution of social behaviour". Journal of Theoretical Biology 7 (1): 1–16. doi:10.1016/0022-5193(64)90038-4. PMID 5875341.
- West, 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.
- Wilson, David Sloan. "Rethinking the Theoretical Foundation of Sociobiology" (PDF). Retrieved 10 September 2013.
- 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. doi:10.1006/jtbi.2003.3127.
- 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.
- Wilson, D.S.; Pollock, G.B.; Dugatkin, L.A (1992). "Can altruism evolve in purely viscous populations?". Evol. Ecol. 6: 331–341. doi:10.1007/bf02270969.
- Taylor, P.D. (1992). "Altruism in viscous populations – an inclusive fitness model.". Evol. Ecol. 6: 352–356. doi:10.1007/bf02270971.
- Mitteldorf, Joshua; Wilson, D.S. (2000). "Population viscosity and the evolution of altruism" (PDF). J. Theor. Biol. 204: 481–496. doi:10.1006/jtbi.2000.2007.
- Mesoudi, A.; Danielson, P. (2008). "Ethics, evolution and culture". Theory in Biosciences 127 (3): 229–240. doi:10.1007/s12064-008-0027-y. PMID 18357481.
- Fehr, E.; Fischbacher, Urs (2003). "The nature of human altruism. [Review]". Nature 425 (6960): 785–791. doi:10.1038/nature02043. PMID 14574401.
- Boyd, R., & Richerson, P. J. (2009) Culture and the evolution of human cooperation.
- 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.
- 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.
- The selfish Gene (Richard Dawkins)
- Axelrod, Robert (1984). The Evolution of Cooperation. Basic Books. p. 98. ISBN 978-0465005642.
- Darwin,C.: 1871, The Descent of Man, The Heritage Press, New York, 1972.
- Heinsohn, R.; Packer, C. (1995). "Complex cooperative strategies in group-territorialAfrican lions". Science 269 (5228): 1260–1262. doi:10.1126/science.7652573. PMID 7652573.
- Cheney,D. L. & Seyfarth, R. M. (1990). How monkeys see the world: Inside the mind of another species. University of Chicago Press. ISBN 978-0-226-10246-7.
- Wade,M. J. and F. Breden. Sept. 1981. Effect of Inbreeding on the Evolution of Altruistic Behavior by Kin Selection. Evolution 35.5: 844-858.
- Muir,W. M., et al. June 2013. Multilevel selection with kin and non-kin groups,Experimental results with Japanese quail. Evolution 67.6: 1598-1606.
- "Group selection and inclusive fitness are not equivalent; the Price equation vs. models and statistics". Journal of Theoretical Biology 299: 64–80. doi:10.1016/j.jtbi.2011.07.025.
- See the chapter God's utility function in Dawkins, Richard (1995). River Out of Eden. New York: Basic Books. ISBN 0-465-06990-8.
- Dawkins, R. (1994). "Burying the Vehicle Commentary on Wilson & Sober: Group Selection". Behavioural and Brain Sciences 17 (4): 616–617. Archived from the original on 2006-09-15.
- Dennett, D.C. (1994). "E Pluribus Unum? Commentary on Wilson & Sober: Group Selection". Behavioural and Brain Sciences 17 (4): 617–618. Archived from the original on 2007-12-27.
- Richard Dawkins, "Replicators and Vehicles", King's College Sociobiology Group, eds., Current Problems in Sociobiology, Cambridge, Cambridge University Press, (1982), pp. 45-64
- Pinker, S. (2012). The False Allue of Group Selection. Edge, Jun 19, 2012. http://edge.org/conversation/the-false-allure-of-group-selection
- Coyne, J. A. (2011). Can Darwinism Improve Binghamton?, New York Review of Books, September 9, 2011.
- 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.
- 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.
- 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.
- 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.
- West, S.A.; Griffin, A.S.; Gardner, A. (2008). "Social semantics: how useful has group selection been?". Journal of Evolutionary Biology 21: 374–385. doi:10.1111/j.1420-9101.2007.01458.x.
- Sober, Elliott and Wilson, David Sloan (1998). Unto Others: The Evolution and Psychology of Unselfish Behavior. Cambridge, MA: Harvard University Press.
- 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.
- 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, David Sloan (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 (archived from the original on 2009-02-26)
- altr-grp Altruism and Group Selection entry in the Internet Encyclopedia of Philosophy
- Lloyd, Elisabeth, "Units and Levels of Selection." The Stanford Encyclopedia of Philosophy, (Fall 2005 Edition), Edward N. Zalta (ed.)
- The Controversy of the Group Selection Theory - a review from the "Science Creative Quarterly" (a blog)
- Binghamton: D.S. Wilson