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Group Selection and Kin Selection: Formally Equivalent Approaches Opinion Group selection and kin selection: formally equivalent approaches James A.R. Marshall Department of Computer Science/Kroto Research Institute, University of Sheffield, Sheffield, S3 7HQ, UK Inclusive fitness theory, summarised in Hamilton’s Historical roots rule, is a dominant explanation for the evolution of The roots of the theories of social evolution discussed here social behaviour. A parallel thread of evolutionary the- extend back into at least the mid-19th century. Over these ory holds that selection between groups is also a many years, concepts and terminology have shifted, even candidate explanation for social evolution. The mathe- when used by the same authors. This section summarises matical equivalence of these two approaches has long these roots, which are discussed at greater length else- been known. Several recent papers, however, have objected that inclusive fitness theory is unable to deal with strong selection or with non-additive fitness effects, and concluded that the group selection frame- Glossary work is more general, or even that the two are not Altruism: donation of aid to another individual or individuals, such that their equivalent after all. Yet, these same problems have lifetime individual fitness is increased while the lifetime individual fitness of already been identified and resolved in the literature. the donor is decreased (see ‘Benefit’ and ‘Cost’). Benefit: the lifetime individual fitness increment resulting from receipt of aid Here, I survey these contemporary objections, and (see ‘Altruism’). examine them in the light of current understanding Cost: the lifetime individual fitness decrement resulting from donation of aid of inclusive fitness theory. (see ‘Altruism’). Fecundity: the total production of potentially reproductive offspring of an individual (cf. ‘Fitness’). Approaches to understanding social evolution Fitness: the long-term descendants of an individual over evolutionary time (cf. The theory of inclusive fitness, formalised by Hamilton ‘Fecundity’). Group selection: a partitioning of selective forces into between-group and [1,2], was arguably the most fundamental advance in within-group components. Group selection theory is mathematically equiva- understanding evolution since Darwin. Hamilton’s lent to inclusive fitness theory. breakthrough was to realise that natural selection acts Hamilton’s rule: a summary prediction of the direction of selection on some social trait, according to inclusive fitness theory, taking account of genetic not only on genes according to their effect on the fitness of relatedness, and costs and benefits of interactions defined in terms of fitness. their bearers, but also according to the fitness change Inclusive fitness theory: the theory of natural selection extended to deal with they effect on genetic relatives containing copies of the inclusive fitness. The direction of selection according to inclusive fitness theory is often summarised in Hamilton’s rule. Inclusive fitness theory is mathema- same gene [1,2]. Inclusive fitness theory has had great tically equivalent to group selection theory. success in explaining diverse aspects of social evolution Inclusive fitness: the total fitness of an individual owing to the effects of their (e.g. [3–8]). own actions on their own individual fitness, additionally taking account of the effects of the action of an individual on the individual fitnesses of other Inclusive fitness theory is not the only attempt to un- population members, weighted by the genetic relatedness of the focal derstand social evolution, however. An alternative per- individual to them. Inclusive fitness is mathematically equivalent to personal fitness. spective is to argue that natural selection acts on Individual fitness (or direct fitness): the fitness of an individual calculated in groups, and those groups whose members are more fre- terms of direct descendants. quently pro-social outcompete those with fewer pro-social Kin selection: a popular term for inclusive fitness theory, originating from early explanations of the theory in terms of relatedness estimated from pedigree. members. Although the theory of group selection had Payoff: the outcome of a social interaction in some currency that is inauspicious origins, as proponents talked of ‘benefit to proportional to changes in individual fecundity. Care must be taken in making the group’ while neglecting the importance of ‘benefit to the evolutionary predictions based on using payoff as a proxy for fitness. Personal fitness (or neighbour-modulated fitness): the total fitness of an individual’ [9], since Hamilton’s original work a contempo- individual owing to the effects of their own actions on their own individual rary version of the group selection perspective has been fitness, as well as the effects owing to the actions of other population shown, in fact, to be simply a different viewpoint on the members. Personal fitness is mathematically equivalent to inclusive fitness. Price equation: a general equation for describing change in terms of selective same process as that described by inclusive fitness theory and other forces. When applied to modelling evolution, the Price equation [10]. Despite this, several recent papers argue that the two considers the association between possession of a trait, and individual are distinct processes [11] (but see [12–18]), or that inclu- fecundity. Relatedness: a measure of the genetic similarity between two or more sive fitness theory is vulnerable to limitations that do not individuals, often described in terms of pedigree, but more correctly trouble group selection [11,19,20]. As a result, some considered as genetic association howsoever caused. Strong selection: selection on a trait having a large average effect on the authors argue that group selection should now become fitness of the bearer (see ‘Weak selection’). the predominant explanation for the evolution of social Weak selection: selection on a trait having a small average effect on the fitness behaviour [11]. of the bearer in a population; for example, owing either to a small effect when expressed relative to other fitness components, or to rare expression (cf. ‘Strong selection’). Corresponding author: Marshall, J.A.R. ([email protected]). 0169-5347/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.04.008 Trends in Ecology and Evolution, July 2011, Vol. 26, No. 7 325 Opinion Trends in Ecology and Evolution July 2011, Vol. 26, No. 7 where [21–23], but also settles on contemporary definitions interacting individuals, selection can be decomposed into of the key concepts to be discussed here. within and between-group components [26],andaltruism can be favoured when between-group selection for altru- What is group selection? istic groups exceeds within-group selection against altru- Even allowing for the earliest glimmerings of inclusive ists [10,27]. Given that most models of group selection to fitness theory during the ‘modern synthesis’, group selec- date are of this type [21],oneofthemainaimshereis tion can lay claim to a much longer intellectual pedigree. to summarise the relationship between this contempo- Darwin himself discussed the possibility of selection at the rary conception of group selection, and inclusive fitness level of the tribe favouring altruism [24]. Models of early theory. proposals for group selection, based on differential survival and reproduction of isolated groups, led some to conclude What is inclusive fitness theory? that group selection was unlikely to be important, owing to Inclusive fitness theory is a generalisation of classical its susceptibility to non-altruist cheats invading groups of Darwinian theory that deals with social behaviour, altruists [25]. Others considered that group-level benefits achieved by extending Darwin’s concept of individual fit- arising from individual selection could occur, but that ness to also take account of the effects of the actions of an adaptations exclusively for the benefit of the group were individual on the fitness of others they interact with [1,2]. unlikely [9]. With these apparently definitive analyses, The fitness effects on others are weighted according to their group selection receded as an explanation for social evolu- relatedness to the focal individual, because close relatives tion. are more likely to share genes for the social behaviour of It was not long, however, until new approaches interest than are distant relatives. The problem of how to showed how, for a population subdivided into groups of define relatedness is actually nontrivial, but before dealing Box 1. Eleven misunderstandings of inclusive fitness theory More than 30 years ago, Richard Dawkins listed ‘twelve misunderstandings of kin selection’ [91]. Today, eleven mostly different misunderstandings seem worth addressing (Table I). Many of these misunderstandings have a long history but, for simplicity, only the most recent re-statements of them are cited. Table I. Inclusive fitness theory: misunderstandings and reality Misunderstanding Reality Inclusive fitness theory is Hamilton’s rule [11,19] Hamilton’s rule is a summary of the direction of selection based on inclusive fitness. Inclusive fitness theory does not preclude more sophisticated analyses of selection [32,71] Inclusive fitness theory is the Price equation [20] The Price equation is one popular approach to deriving Hamilton’s rule and studying inclusive fitness [92]. Other approaches, such as population genetics and evolutionary game theory, are equally applicable
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