Evolutionary Explanations for Cooperation
2007; Elsevier BV; Volume: 17; Issue: 16 Linguagem: Inglês
10.1016/j.cub.2007.06.004
ISSN1879-0445
AutoresStuart A. West, Ashleigh S. Griffin, Andy Gardner,
Tópico(s)Experimental Behavioral Economics Studies
ResumoNatural selection favours genes that increase an organism's ability to survive and reproduce. This would appear to lead to a world dominated by selfish behaviour. However, cooperation can be found at all levels of biological organisation: genes cooperate in genomes, organelles cooperate to form eukaryotic cells, cells cooperate to make multicellular organisms, bacterial parasites cooperate to overcome host defences, animals breed cooperatively, and humans and insects cooperate to build societies. Over the last 40 years, biologists have developed a theoretical framework that can explain cooperation at all these levels. Here, we summarise this theory, illustrate how it may be applied to real organisms and discuss future directions. Natural selection favours genes that increase an organism's ability to survive and reproduce. This would appear to lead to a world dominated by selfish behaviour. However, cooperation can be found at all levels of biological organisation: genes cooperate in genomes, organelles cooperate to form eukaryotic cells, cells cooperate to make multicellular organisms, bacterial parasites cooperate to overcome host defences, animals breed cooperatively, and humans and insects cooperate to build societies. Over the last 40 years, biologists have developed a theoretical framework that can explain cooperation at all these levels. Here, we summarise this theory, illustrate how it may be applied to real organisms and discuss future directions. Box 1Glossary.Actor: the focal individual performing a behaviour.Altruism: a behaviour that is costly to the actor and beneficial to the recipient. Cost and benefit are defined on the basis of the lifetime direct fitness consequences of a behaviour.Cheaters: individuals who do not cooperate or who cooperate less than their fair share, but are potentially able to gain the benefit of others cooperating.Cooperation: a behaviour that provides a benefit to another individual (recipient), and the evolution of which has been dependent on its beneficial effect for the recipient.Direct fitness: the component of fitness gained from producing offspring; the component of personal fitness due to one's own behaviour.Greenbeard: a hypothetical gene that causes in carriers both a phenotype that can be recognised by conspecifics (a 'green beard') and a cooperative behaviour towards conspecifics who show a green beard.Inclusive fitness: "the effect of one individual's actions on everybody's numbers of offspring […] weighted by the relatedness [10Grafen A. Natural selection, kin selection and group selection.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 62-84Google Scholar]; the sum of direct and indirect fitness; the quantity maximised by Darwinian individuals.Indirect fitness: the component of fitness gained from aiding related individuals.Kin selection: process by which traits are favoured because of their beneficial effects on the fitness of relatives.Mutual benefit: a benefit to both the actor and the recipient.Mutualism: two-way cooperation between species.Recipient: an individual who is affected by the behaviour of the focal individual.Relatedness: a measure of the genetic similarity of two individuals, relative to the average; the statistical (least-squares) regression of the recipient's breeding value for a trait on the breeding value of the actor.A behaviour is cooperative if it provides a benefit to another individual and if it has evolved at least partially because of this benefit [1West S.A. Griffin A.S. Gardner A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection.J. Evol. Biol. 2007; 20: 415-432Crossref PubMed Scopus (371) Google Scholar]. Such behaviours pose a problem to evolutionary theory because — all else being equal — they would reduce the relative fitness of the performer of that behaviour and hence be selected against [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar] (Figure 1). To give a specific example, consider the star of many a nature documentary, the meerkat. Meerkats generally live in groups of up to 30 adults with their young. The adults of a group can be divided into the dominant male and female, who do most of the breeding, and the subordinates, who help the dominants raise their offspring [3Griffin A.S. Pemberton J.M. Brotherton P.N.M. McIlrath G. Gaynor D. Kansky R. O'Riain J. Clutton-Brock T.H. A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta).Behav. Ecol. 2003; 14: 472-480Crossref Scopus (106) Google Scholar]. When one of these subordinates has found a tasty scorpion, why should it hand it over to one of the offspring produced by the dominant pair? How can we reconcile this behaviour with selfish interests, even at the level of the gene, and the Darwinian struggle for survival and reproduction in the natural world? Actor: the focal individual performing a behaviour.Altruism: a behaviour that is costly to the actor and beneficial to the recipient. Cost and benefit are defined on the basis of the lifetime direct fitness consequences of a behaviour.Cheaters: individuals who do not cooperate or who cooperate less than their fair share, but are potentially able to gain the benefit of others cooperating.Cooperation: a behaviour that provides a benefit to another individual (recipient), and the evolution of which has been dependent on its beneficial effect for the recipient.Direct fitness: the component of fitness gained from producing offspring; the component of personal fitness due to one's own behaviour.Greenbeard: a hypothetical gene that causes in carriers both a phenotype that can be recognised by conspecifics (a 'green beard') and a cooperative behaviour towards conspecifics who show a green beard.Inclusive fitness: "the effect of one individual's actions on everybody's numbers of offspring […] weighted by the relatedness [10Grafen A. Natural selection, kin selection and group selection.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 62-84Google Scholar]; the sum of direct and indirect fitness; the quantity maximised by Darwinian individuals.Indirect fitness: the component of fitness gained from aiding related individuals.Kin selection: process by which traits are favoured because of their beneficial effects on the fitness of relatives.Mutual benefit: a benefit to both the actor and the recipient.Mutualism: two-way cooperation between species.Recipient: an individual who is affected by the behaviour of the focal individual.Relatedness: a measure of the genetic similarity of two individuals, relative to the average; the statistical (least-squares) regression of the recipient's breeding value for a trait on the breeding value of the actor. This problem also applies to economics and human morality, with a famous example being the 'tragedy of the commons' [4Hardin G. The tragedy of the commons.Science. 1968; 162: 1243-1248Crossref PubMed Google Scholar]: imagine a number of shepherds, each deciding how many sheep to keep on a shared pasture. The addition of extra sheep will have both a benefit and a cost. The benefit is that the shepherd will gain from extra sheep. The cost is potential overgrazing, which can damage the pasture. However, whilst our focal shepherd gains all of the benefit, he pays only a fraction of the cost, which is shared between all of the shepherds. Consequently, the individual shepherd has more to gain than to lose from adding extra sheep. The tragedy is that — as a group — all the shepherds would benefit from grazing less sheep. Such cooperation, however, is not stable, because each individual can gain by selfishly pursuing their own interests. Most attention on the problem of cooperation (see Box 1 for glossary) has been focused on interactions between animals. However, the same problem occurs at all levels of biological organisation [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar, 5Hamilton W.D. Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 1972; 3: 193-232Crossref Google Scholar, 6Leigh E.G. Genes, bees and ecosystems: the evolution of a common interest among individuals.Trends Ecol. Evol. 1991; 6: 257-262Abstract Full Text PDF PubMed Google Scholar, 7Maynard Smith J. Szathmary E. The Major Transitions in Evolution. W.H. Freeman, Oxford1995Google Scholar]. The very existence of multicellular organisms relies upon cooperation between the eukaryotic cells that make them up. The mitochondria upon which these eukaryotic cells rely were once free-living prokaryotic cells but now live cooperative lives. Separate genes, which make up the genome, cooperate in what has been termed the 'parliament of the genes' [8Leigh E.G. Adaptation and Diversity. Freeman, Cooper and Company, San Francisco1971Google Scholar]. The tree of life is dominated by single-celled microorganisms that appear to perform a huge range of cooperative behaviours [9West S.A. Griffin A.S. Gardner A. Diggle S.P. Social evolution theory for microbes.Nat. Rev. Microbiol. 2006; 4: 597-607Crossref PubMed Scopus (306) Google Scholar]. For example, the growth and survival of bacteria depend upon excreted products that perform a variety of functions, such as scavenging nutrients, communication, defence and movement. The benefits of such extracellular products can be shared by neighbouring cells and hence they represent a 'public good' that is open to the problem of cooperation [9West S.A. Griffin A.S. Gardner A. Diggle S.P. Social evolution theory for microbes.Nat. Rev. Microbiol. 2006; 4: 597-607Crossref PubMed Scopus (306) Google Scholar]. Almost all of the major evolutionary transitions from replicating molecules to complex animal societies have relied upon solving the problem of cooperation being solved [7Maynard Smith J. Szathmary E. The Major Transitions in Evolution. W.H. Freeman, Oxford1995Google Scholar]. As cooperation is in evidence throughout the natural world, there must be a solution to the problem. Theoretical explanations for the evolution of cooperation (or any behaviour) are broadly classified into two categories: direct fitness benefits or indirect fitness benefits [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar, 10Grafen A. Natural selection, kin selection and group selection.in: Krebs J.R. Davies N.B. Behavioural Ecology: An Evolutionary Approach. Second Edition. Blackwell Scientific Publications, Oxford, UK1984: 62-84Google Scholar, 11Frank S.A. Foundations of Social Evolution. Princeton University Press, Princeton, New Jersey1998Crossref Google Scholar, 12Lehmann L. Keller L. The evolution of cooperation and altruism. A general framework and classification of models.J. Evol. Biol. 2006; 19: 1365-1378Crossref PubMed Scopus (308) Google Scholar] (Figure 2). This follows from Hamilton's [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar] insight that individuals gain inclusive fitness through their impact on the reproduction of related individuals (indirect fitness effects) as well as through their impact on their own reproduction (direct fitness effects) (Figure 3). The importance of Hamilton's work cannot be overstated — it is one of the few truly fundamental advances since Darwin in our understanding of natural selection.Figure 3Inclusive fitness and cooperation.Show full captionInclusive fitness is the sum of direct and indirect fitness [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar]. Social behaviours affect the reproductive success of self and others. The impact of the actor's behaviour (yellow hands) on its reproductive success (yellow offspring) is the direct fitness effect. The impact of the actor's behaviour (yellow hands) on the reproductive success of social partners (blue offspring), weighted by the relatedness (r) of the actor to the recipient, is the indirect fitness effect. Inclusive fitness does not include all of the reproductive success of relatives (blue offspring), only that which is due to the behaviour of the actor (yellow hands). Also, inclusive fitness does not include all of the reproductive success of the actor (yellow offspring), only that which is due to its own behaviour (yellow hands).View Large Image Figure ViewerDownload Hi-res image Download (PPT) Inclusive fitness is the sum of direct and indirect fitness [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar]. Social behaviours affect the reproductive success of self and others. The impact of the actor's behaviour (yellow hands) on its reproductive success (yellow offspring) is the direct fitness effect. The impact of the actor's behaviour (yellow hands) on the reproductive success of social partners (blue offspring), weighted by the relatedness (r) of the actor to the recipient, is the indirect fitness effect. Inclusive fitness does not include all of the reproductive success of relatives (blue offspring), only that which is due to the behaviour of the actor (yellow hands). Also, inclusive fitness does not include all of the reproductive success of the actor (yellow offspring), only that which is due to its own behaviour (yellow hands). A cooperative behaviour yields direct fitness benefits when the reproductive success of the actor, who performs the cooperative behaviour, is increased. Cooperative behaviours that benefit both the actor and the recipient(s) of the behaviour are termed 'mutually beneficial' [1West S.A. Griffin A.S. Gardner A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection.J. Evol. Biol. 2007; 20: 415-432Crossref PubMed Scopus (371) Google Scholar]. A cooperative behaviour can be explained by indirect fitness benefits if it is directed towards other individuals who carry the gene for cooperation [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar]. This is usually termed 'kin selection' [13Maynard Smith J. Group selection and kin selection.Nature. 1964; 201: 1145-1147Crossref Scopus (479) Google Scholar], because the simplest and most common way this could occur is if cooperation is directed at relatives, who share genes from a common ancestor [11Frank S.A. Foundations of Social Evolution. Princeton University Press, Princeton, New Jersey1998Crossref Google Scholar]. By helping a close relative reproduce, an individual is still passing copies of its genes on to the next generation, albeit indirectly. Cooperative behaviours that are costly to the actor and beneficial to the recipient are termed 'altruistic' [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar] and can only be explained by indirect fitness benefits. A key point here is that we are considering the average consequences of a behaviour and not the consequences of every single instance. Hamilton's inclusive fitness (kin selection) theory shows how altruistic cooperation can be favoured between relatives. This is encapsulated in a pleasingly simple form by Hamilton's rule [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar], which states that a behaviour or trait will be favoured by selection, when rb−c>0, where c is the fitness cost to the actor, b is the fitness benefit to the recipient, and r is their genetic relatedness. Putting this inequality into words, altruistic cooperation can therefore be favoured if the benefits to the recipient (b), weighted by the genetic relatedness of the recipient to the actor (r), outweigh the costs to the actor (c). This follows from inclusive fitness theory because −c represents the direct fitness consequences of a social behaviour and rb the indirect fitness consequences. Hamilton's rule predicts greater levels of cooperation when r or b are higher and c is lower. Explanations for cooperation based on indirect fitness benefits, i.e. kin selection, require a sufficiently high genetic relatedness (r) between interacting individuals. The coefficient of relatedness (r) is a statistical concept, describing the genetic similarity between two individuals, relative to the average similarity of all individuals in the population [11Frank S.A. Foundations of Social Evolution. Princeton University Press, Princeton, New Jersey1998Crossref Google Scholar]. Hamilton [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar] suggested two possible mechanisms through which a high relatedness could arise between social partners: kin discrimination and limited dispersal. The first mechanism for generating sufficiently high relatedness to make kin selection viable is kin discrimination, when an individual can distinguish relatives from non-relatives and preferentially direct aid towards them (nepotism) [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar]. This has been demonstrated in several cooperatively breeding vertebrates, such as long-tailed tits [14Russell A.F. Hatchwell B.J. Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate.Proc. Roy. Soc. Lond. B. 2001; 268: 2169-2174Crossref PubMed Scopus (101) Google Scholar], where individuals that fail to breed independently help at the nest of closer relatives [14Russell A.F. Hatchwell B.J. Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate.Proc. Roy. Soc. Lond. B. 2001; 268: 2169-2174Crossref PubMed Scopus (101) Google Scholar] (Figure 4A). In this species, individuals distinguish between relatives and non-relatives on the basis of vocal contact cues, which are learned from adults during the nesting period (associative learning) [15Sharp S.P. McGowan A. Wood M.J. Hatchwell B.J. Learned kin recognition cues in a social bird.Nature. 2005; 434: 1127-1130Crossref PubMed Scopus (89) Google Scholar]. This leads to a situation in which individuals tend to help relatives whom they have been associated with during the nestling phase. Kin selection theory also explains the variation in the level of kin discrimination across species [16Griffin A.S. West S.A. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates.Science. 2003; 302: 634-636Crossref PubMed Scopus (179) Google Scholar]. In contrast to the long-tailed tits, other cooperatively breeding vertebrates, such as meerkats [17Clutton-Brock T.H. Brotherton P.N.M. Oriain M.J. Griffin A.S. Gaynor D. Sharpe L. Kansky R. Manser M.B. McIlrath G.M. Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta.Proc. R. Soc. Lond. B. 2000; 267: 301-305Crossref PubMed Google Scholar], do not show kin discrimination when helping. The advantage of kin discrimination will be positively correlated with the extent of the benefit (b) provided by helping. In the extreme, if a supposedly 'helping' behaviour provides little or no benefit to its recipients, then there is little or no advantage in directing it towards closer relatives. This leads to the prediction that the extent of kin discrimination should be greater in species where a greater fitness benefit is derived from receiving help — a pattern indeed observed across cooperatively breeding vertebrate species [16Griffin A.S. West S.A. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates.Science. 2003; 302: 634-636Crossref PubMed Scopus (179) Google Scholar] (Figure 5). Overall, the benefit that helping brings to the recipient can explain 42% of the variation in the extent of kin discrimination across species. Kin discrimination has also been found in species that are not usually thought of from a social perspective. Dictyostelium purpureum is a unicellular slime mould found in forest soils [18Mehdiabadi N.J. Jack C.N. Farnham T.T. Platt T.G. Kalla S.E. Shaulsky G. Queller D.C. Strassman J.S. Kin preference in a social microbe.Nature. 2006; 442: 881-882Crossref PubMed Scopus (72) Google Scholar]. When starved of its bacterial food source, the cells of this species aggregate in thousands to form a multicellular, motile 'slug'. Slugs migrate to the soil surface, where they transform into a fruiting body composed of a stalk structure holding aloft a ball of spores. The non-viable stalk cells are sacrificed to aid the dispersal of the spores. This requires explanation because cooperative cells that form stalk cells could be exploited by cheaters who avoid the stalk and instead migrate to form spores in the fruiting body. Kin selection offers a potential solution to this problem, because stalk cells could gain an indirect fitness benefit from helping relatives disperse. This suggests that it would be advantageous for the individual amoebae to preferentially form a slug with relatives. Indeed, kin discrimination during slug formation has recently been observed in D. purpureum[18Mehdiabadi N.J. Jack C.N. Farnham T.T. Platt T.G. Kalla S.E. Shaulsky G. Queller D.C. Strassman J.S. Kin preference in a social microbe.Nature. 2006; 442: 881-882Crossref PubMed Scopus (72) Google Scholar]. Specifically, when two lineages are mixed and allowed to form slugs on agar plates, they discriminate to the extent that the average relatedness in fruiting bodies increases to a value of 0.8, as opposed to the expected value of 0.5 (Figure 4B). Kin discrimination can occur through the use of environmental or genetic cues [19Grafen A. Do animals really recognise kin?.Anim. Behav. 1990; 39: 42-54Crossref Google Scholar]. The most common mechanism appears to involve environmental cues, such as prior association or shared environment, as in long-tailed tits and a range of other animals from humans to ants [20Helanterä H. Sundström L. Worker policing and nest mate recognition in the ant Formica fusca.Behav. Ecol. Sociobiol. 2007; 61: 1143-1149Crossref Scopus (19) Google Scholar, 21Lieberman D. Tooby J. Cosmides L. Does morality have a biological basis? An empirical test of the factors governing moral sentiments relating to incest.Proc. Roy. Soc. Lond. B. 2003; 270: 819-826Crossref PubMed Google Scholar]. In contrast, in the case of the slime mould some genetic cue of relatedness is likely to be involved — also termed 'kin recognition', 'genetic similarity detection', 'matching' or 'tags'. In order to detect genetic similarity, an individual must have some cue that is genetically determined — such as the cuticular hydrocarbon profile of an insect [22Boomsma J.J. Nielsen J. Sundstrom L. Oldham N.J. Tentschert J. Petersen H.C. Morgan E.D. Informational constraints on optimal sex allocation in ants.Proc. Natl. Acad. Sci. USA. 2003; 100: 8799-8804Crossref PubMed Scopus (88) Google Scholar], or the odour produced by scent glands in a mammal [23Mateo J.M. Kin-recognition abilities and nepotism as a function of sociality.Proc. Roy. Soc. Lond. B. 2002; 269: 721-727Crossref PubMed Scopus (86) Google Scholar] — and a 'kin template' for comparison [19Grafen A. Do animals really recognise kin?.Anim. Behav. 1990; 39: 42-54Crossref Google Scholar]. This kin template could be determined by the individual's own genotype or cues ('self-matching') and/or through learning the cues of its rearing associates [23Mateo J.M. Kin-recognition abilities and nepotism as a function of sociality.Proc. Roy. Soc. Lond. B. 2002; 269: 721-727Crossref PubMed Scopus (86) Google Scholar]. Kin discrimination based on genetic cues is often unlikely to be evolutionarily stable. The reason is that recognition mechanisms require genetic variability (polymorphism) in order to provide a cue. However, individuals with common genetic variants would be more likely to be helped, and thus more common genes would be driven to fixation [24Rousset, F., and Roze, D., (2007). Constraints on the origin and maintenance of genetic kin recognition. Evolution, Submitted.Google Scholar]. Consequently, kin discrimination is, as it were, its own worst enemy, eliminating the genetic variability that it requires to work. Thus, kin discrimination based on genetic cues is often not found where it might be expected [25Keller L. Indiscriminate altruism: unduly nice parents and siblings.Trends Ecol. 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In cases where kin discrimination based upon genetic cues has been observed, it can usually be argued that there is some other selective force maintaining variability at the recognition loci, such as host-parasite co-evolution in the major histocompatibility complex (MHC) of vertebrates [24Rousset, F., and Roze, D., (2007). Constraints on the origin and maintenance of genetic kin recognition. Evolution, Submitted.Google Scholar]. Cue diversity may also be maintained if there is limited dispersal, such that interactants tend to be relatives anyway [24Rousset, F., and Roze, D., (2007). Constraints on the origin and maintenance of genetic kin recognition. Evolution, Submitted.Google Scholar, 29Axelrod R. Hammond R.A. Grafen A. Altruism via kin-selection strategies that rely on arbitrary tags with which they coevolve.Evolution. 2004; 58: 1833-1838Crossref PubMed Google Scholar], as is likely to be the case with the slime mould discussed above. Indirect fitness benefits will also be obtained if cooperation is directed towards non-relatives who share the same cooperative gene [2Hamilton W.D. The genetical evolution of social behaviour, I & II.J. Theor. Biol. 1964; 7: 1-52Crossref PubMed Google Scholar, 30Hamilton W.D. Innate social aptitudes of man: An approach from evolutionary genetics.in: Fox R. Biosocial Anthropology. Wiley, New York, NY1975: 133-155Google Scholar]. Dawkins [31Dawkins R. The Selfish Gene. Oxford University Press, Oxford, UK1976Google Scholar] illustrated this with a hypothetical example of a gene that gave rise to green beards, while simultaneously prompting individuals with green beards to preferentially direct cooperation towards other green-bearded individuals. This mechanism can also occur without a visible tag — for example, if the cooperative gene also caused some effect on habitat preference that led to individuals who carried that gene settling together [30Hamilton W.D. Innate social aptitudes of man: An approach from evolutionary genetics.in: Fox R. Biosocial Anthropology. Wiley, New York, NY1975: 133-155Google Scholar]. Consequently, although this mechanism is usually termed a 'greenbeard', it more generally represents an assortment mechanism, requiring a single gene — or a number of tightly linked genes — that encodes both the cooperative behaviour and causes cooperators to associate [12Lehmann L. Keller L. The evolution of cooperation and altruism. A general framework and classification of models.J. Evol. Biol. 2006; 19: 1365-1378Crossref PubMed Scopus (308) Google Scholar]. Greenbeards are likely to be rare, because cheaters that display the green beard, or assorting behaviour, without also performing the cooperative behaviour, could invade and overrun the population. Furthermore, in the absence of relatedness over the whole genome, the altruistic greenbeard would be in conflict with genes elsewhere in the genome, where there would be strong selection for suppression of the greenbeard [32Grafen A. Optimisation of inclusive fitness.J. Theoret. Biol. 2006; 238: 541-563Crossref PubMed Scopus (119) Google Scholar, 33Helanterä H. Bargum K. Pedigree relatedness, not greenbeard genes, explains eusociality.Oikos. 2007; 116: 217-220Crossref Google Scholar]. One of the few cases where a cooperative greenbeard occurs is in the slime mould Dictyostelium discoideum, which forms fruiting bodies in a very similar way to D. purpureum. In. D. discoideum, individual amoebae with the csa cell-adhesion gene adhere to each other in aggregation streams and cooperatively form fruiting bodies at the exclusion of csa mutants [34Queller D.C. Ponte E. Bozzaro S. Strassmann J.E. Single-gene greenbeard effects in the social amoeba Dictostelium discoideum.Science. 2003; 299: 105-106Crossref PubMed Scopus (130) Google Scholar]. It is perhaps not surprising that greenbeards should be rare, given that the idea was not developed as a theory to explain altruism, but as a thought experiment to show that genetic relatedness — rather than genealogical relationship per se — is the key to kin selection. Limited dispersal (population
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