Identifying Causes of Social Evolution: Contextual Analysis, the Price Approach, and Multilevel Selection

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.

Evaluating kin and group selection as tools for quantitative analysis of microbial data

Kin selection and multilevel selection theory are often used to interpret experiments about the evolution of cooperation and social behaviour among microbes. But while these experiments provide rich, detailed fitness data, theory is mostly used as a conceptual heuristic. Here, we evaluate how kin and multilevel selection theory perform as quantitative analysis tools. We reanalyse published microbial datasets and show that the canonical fitness models of both theories are almost always poor fits because they use statistical regressions misspecified for the strong selection and non-additive effects we show are widespread in microbial systems. We identify analytical practices in empirical research that suggest how theory might be improved, and show that analysing both individual and group fitness outcomes helps clarify the biology of selection. A data-driven approach to theory thus shows how kin and multilevel selection both have untapped potential as tools for quantitative understanding of social evolution in all branches of life.

The music and social bonding hypothesis does require multilevel selection

Is musicality an individual level adaptation? The authors of this target article reject the need for group selection within their model, yet their arguments do not fulfill the conceptual requirements for justifying such a rejection. Further analysis can highlight the explanatory value of embracing multilevel selection theory as a foundational element of the music and social bonding (MSB) hypothesis.

How competition drove social complexity: the role of war in the emergence of States, both ancient and modern

ABSTRACT The origin of human ultrasociality - the ability to cooperate in huge groups of genetically unrelated individuals - has long interested evolutionary and social theorists. In this article, we use cultural group or multilevel selection theory to explain how cultural traits needed to sustain large-scale complex societies necessarily arose as a result of competition among cultural groups. We apply the theory at two key particular junctures: (i) the emergence of the first States and hierarchical societies, and (ii) the Rise of Modern Nation-States and the associated Great Divergence in incomes between the West and the “Rest” that began in the eighteenth century.

Developing the Evolved Social Brain

For human hypersociality to evolve required that natural selection operate both at the levels of the individual and the group as described by multilevel selection theory. According to the social brain hypothesis, increased social cognition was the driving force in human social-cognitive evolution. Infants evolved “psychological weapons” designed to obtain attention and caregiving from adults. According to Tomasello’s shared intentionality theory, infants view others as intentional agents, as reflected in shared attention beginning around 9 months, and later, between 3 and 5 years of age, in collective intentionality, in which children establish a group-minded “we” with other people. The development and evolution of hypersociality is reflected in: treating others as intentional agents, perspective taking, empathy, normativity, social learning, prosociality (helping, sharing, sense of fairness), and collaboration. Each of these and other social-cognitive abilities were necessary for the evolution of a hypersocial species and evolved as a result of changes in great ape ontogeny.

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

Kin 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.

The role of multilevel selection in host microbiome evolution

Animals are associated with a microbiome that can affect their reproductive success. It is, therefore, important to understand how a host and its microbiome coevolve. According to the hologenome concept, hosts and their microbiome form an integrated evolutionary entity, a holobiont, on which selection can potentially act directly. However, this view is controversial, and there is an active debate on whether the association between hosts and their microbiomes is strong enough to allow for selection at the holobiont level. Much of this debate is based on verbal arguments, but a quantitative framework is needed to investigate the conditions under which selection can act at the holobiont level. Here, we use multilevel selection theory to develop such a framework. We found that selection at the holobiont level can in principle favor a trait that is costly to the microbes but that provides a benefit to the host. However, such scenarios require rather stringent conditions. The degree to which microbiome composition is heritable decays with time, and selection can only act at the holobiont level when this decay is slow enough, which occurs when vertical transmission is stronger than horizontal transmission. Moreover, the host generation time has to be short enough compared with the timescale of the evolutionary dynamics at the microbe level. Our framework thus allows us to quantitatively predict for what kind of systems selection could act at the holobiont level.