ON MULTILEVEL SELECTION AND KIN SELECTION: CONTEXTUAL ANALYSIS MEETS DIRECT FITNESS

Kin selection theory and multilevel selection theory are distinct approaches to explaining the evolution of social traits. The latter claims that it is useful to regard selection as a process that can occur on multiple levels of organisation such as the level of individuals and the level of groups. This is reflected in a decomposition of fitness into an individual component and a group component. This multilevel view is central to understanding and characterising evolutionary transitions in individuality, e.g., from unicellular life to multicellular organisms, but currently suffers from the lack of a consistent, quantifiable measure. Specifically, the two major statistical tools to determine the coefficients of such a decomposition, the multilevel Price equation and contextual analysis, are inconsistent and may disagree on whether group selection is present. Here we show that the reason for the discrepancies is that underlying the multilevel Price equation and contextual analysis are two non-equivalent causal models for the generation of individual fitness effects (thus leaving different “remainders” explained by group effects). While the multilevel Price equation assumes that the individual effect of a trait determines an individual's relative success within a group, contextual analysis posits that the individual effect is context-independent. Since these different assumptions reflect claims about the causal structure of the system, the correct approach cannot be determined on general theoretical or statistical grounds but must be identified by experimental intervention. We outline interventions that reveal the underlying causal structure and thus facilitate choosing the appropriate approach. We note that kin selection theory with its focus on the individual is immune to such inconsistency because it does not address causal structure with respect to levels of organisation. In contrast, our analysis of the two approaches to measuring group selection demonstrates that multilevel selection theory adds meaningful (falsifiable) causal structure to explain the sources of individual fitness and thereby constitutes a proper refinement of kin selection theory. Taking such refined causal structure into account seems indispensable for studying evolutionary transitions in individuality because these transitions are characterised by changes in the selection pressures that act on the respective levels.

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Identifying causes of social evolution: The Price approach, contextual analysis, and multilevel selection

10.1101/2020.08.14.233122 ◽

2020 ◽

Author(s):

Christoph Thies ◽

Richard A. Watson

Keyword(s):

Kin Selection ◽

Group Selection ◽

Causal Structure ◽

Multilevel Selection ◽

Contextual Analysis ◽

Price Equation ◽

Selection Theory ◽

Individual Fitness ◽

Multilevel Selection Theory ◽

The Individual

AbstractKin selection theory and multilevel selection theory are different approaches to explaining the evolution of social traits. The latter claims that it is useful to regard selection as a process that can occur on multiple levels of organisation such as the level of individuals and the level of groups. This is reflected in a decomposition of fitness into an individual component and a group component. However, the two major statistical tools to determine the coefficients of such a decomposition, the multilevel Price equation and contextual analysis, are inconsistent and may disagree on whether group selection is present. Here we show that the reason for the discrepancies is that underlying the multilevel Price equation and contextual analysis are two nonequivalent causal models for the generation of individual fitness effects (thus leaving different ‘remainders’ explained by group effects). While the multilevel Price equation assumes that the individual effect of a trait determines an individual’s relative success within a group, contextual analysis posits that the individual effect is context-independent. Since these different assumptions reflect claims about the causal structure of the system, the correct approach cannot be determined on general theoretical or statistical grounds but must be identified by experimental intervention. We outline interventions that reveal the underlying causal structure and thus facilitate choosing the appropriate approach. We note that the reductionist viewpoint of kin selection theory with its focus on the individual is immune to such inconsistency because it does not address causal structure with respect to levels of organisation. In contrast, our analysis of the two approaches to measuring group selection demonstrates that multilevel selection theory adds meaningful (falsifiable) causal structure to explain the sources of individual fitness and thereby constitutes a proper refinement of kin selection theory.

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Current indirect fitness and future direct fitness are not incompatible

Biology Letters ◽

10.1098/rsbl.2017.0592 ◽

2018 ◽

Vol 14 (2) ◽

pp. 20170592 ◽

Cited By ~ 3

Author(s):

Anindita Brahma ◽

Souvik Mandal ◽

Raghavendra Gadagkar

Keyword(s):

Kin Selection ◽

Feeding Behaviour ◽

Multilevel Selection ◽

Ropalidia Marginata ◽

Eusocial Insects ◽

Naturally Occurring ◽

Direct Fitness ◽

Indirect Fitness ◽

Primitively Eusocial ◽

Worker Behaviour

In primitively eusocial insects, many individuals function as workers despite being capable of independent reproduction. Such altruistic behaviour is usually explained by the argument that workers gain indirect fitness by helping close genetic relatives. The focus on indirect fitness has left open the question of whether workers are also capable of getting direct fitness in the future in spite of working towards indirect fitness in the present. To investigate this question, we recorded behavioural profiles of all wasps on six naturally occurring nests of Ropalidia marginata , and then isolated all wasps in individual plastic boxes, giving them an opportunity to initiate nests and lay eggs. We found that 41% of the wasps successfully did so. Compared to those that failed to initiate nests, those that did were significantly younger, had significantly higher frequency of self-feeding behaviour on their parent nests but were not different in the levels of work performed in the parent nests. Thus ageing and poor feeding, rather than working for their colonies, constrain individuals for future independent reproduction. Hence, future direct fitness and present work towards gaining indirect fitness are not incompatible, making it easier for worker behaviour to be selected by kin selection or multilevel selection.

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Kin and multilevel selection in social evolution: a never-ending controversy?

F1000Research ◽

10.12688/f1000research.8018.1 ◽

2016 ◽

Vol 5 ◽

pp. 776 ◽

Cited By ~ 26

Author(s):

Jos Kramer ◽

Joël Meunier

Keyword(s):

Kin Selection ◽

Group Selection ◽

Evolutionary Biology ◽

Social Evolution ◽

Selection Process ◽

Structured Populations ◽

Multilevel Selection ◽

Current Debate ◽

The Relationship ◽

Shed Light

Kin selection and multilevel selection are two major frameworks in evolutionary biology that aim at explaining the evolution of social behaviors. However, the relationship between these two theories has been plagued by controversy for almost half a century and debates about their relevance and usefulness in explaining social evolution seem to rekindle at regular intervals. Here, we first provide a concise introduction into the kin selection and multilevel selection theories and shed light onto the roots of the controversy surrounding them. We then review two major aspects of the current debate: the presumed formal equivalency of the two theories and the question whether group selection can lead to group adaptation. We conclude by arguing that the two theories can offer complementary approaches to the study of social evolution: kin selection approaches usually focus on the identification of optimal phenotypes and thus on the endresult of a selection process, whereas multilevel selection approaches focus on the ongoing selection process itself. The two theories thus provide different perspectives that might be fruitfully combined to promote our understanding of the evolution in group-structured populations.

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Direct fitness or inclusive fitness: how shall we model kin selection?

Journal of Evolutionary Biology ◽

10.1111/j.1420-9101.2006.01196.x ◽

2007 ◽

Vol 20 (1) ◽

pp. 301-309 ◽

Cited By ~ 94

Author(s):

P. D. TAYLOR ◽

G. WILD ◽

A. GARDNER

Keyword(s):

Kin Selection ◽

Inclusive Fitness ◽

Direct Fitness

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Kin Selection

Ecology ◽

10.1093/obo/9780199830060-0051 ◽

2012 ◽

Author(s):

Andrew F. G. Bourke

Keyword(s):

Natural Selection ◽

Social Behavior ◽

Kin Selection ◽

Inclusive Fitness ◽

Social Behaviors ◽

Selection Theory ◽

Direct Fitness ◽

Inclusive Fitness Theory ◽

Gene Copies ◽

Genetical Theory

According to Hamilton’s kin selection theory (also known as “inclusive fitness” theory), kin selection is the process by which social evolution occurs in nature. The theory extends the genetical theory of natural selection to social behaviors and finds that their evolution is affected by the likelihood that individuals share genes (relatedness). In biology, a social behavior occurs when one individual (the actor) behaves so as to affect the direct fitness (number of offspring) of itself and another individual (the recipient). For example, altruism occurs when the actor’s behavior decreases the actor’s direct fitness and increases the recipient’s direct fitness. Conversely, selfishness occurs when the actor’s behavior increases the actor’s direct fitness and decreases the recipient’s. Social behaviors are widespread in nature. A classic example is the altruism shown by the sterile workers of social insects such as ants, which sacrifice their own reproduction in order to rear the queen’s offspring. At first sight, altruism poses a problem for the genetical theory of natural selection, which seems to preclude the spread of a gene for reduced reproduction. Kin selection was devised by William Hamilton in the early 1960s to address this “problem of altruism.” The basic principle behind kin selection had been hinted at by Darwin, Fisher, and Haldane, but it was Hamilton who provided the first general model. Hamilton called his idea “inclusive fitness” theory, and it was later dubbed “kin selection” by Maynard Smith in 1964. For most purposes, the two can be considered identical, although inclusive fitness theory technically includes kin selection theory because the relatedness it invokes need not involve kin (genealogical relatives). Kin selection theory solved the problem of altruism by showing that a gene for altruism can spread if altruism is directed at individuals likely to bear the same gene. By definition, kin are likely to share genes. So, a gene for altruism can spread if altruism is directed at kin and the loss of gene copies through the actor’s decreased reproduction is more than offset by the gain in gene copies through the increased reproduction of the recipient. The algebraic version of this condition is termed “Hamilton’s rule.” Although kin selection theory was devised to explain altruism, it also applies to the other forms of social behavior such as selfishness. The theory is therefore now widely used to investigate and explain many kinds of social behavior in living organisms as diverse as bacteria and human beings.

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