The genetical theory of multilevel selection.

A Gardner

doi:10.1111/jeb.12566

Abstract

The theory of multilevel selection (MLS) is beset with conceptual difficulties. Although it is widely agreed that covariance between group trait and group fitness may arise in the natural world and drive a response to ‘group selection’, ambiguity exists over the precise meaning of group trait and group fitness and as to whether group selection should be defined according to changes in frequencies of different types of individual or different types of group. Moreover, the theory of MLS has failed to properly engage with the problem of class structure, which greatly limits its empirical application to, for example, social insects whose colonies are structured into separate age, sex, caste and ploidy classes. Here, I develop a genetical theory of MLS, to address these problems. I show that taking a genetical approach facilitates a decomposition of group-level traits – including reproductive success – into the separate contributions made by each constituent individual, even in the context of so-called emergence. However, I uncover a novel problem with the group-oriented approach: in many scenarios, it may not be possible to express a meaningful covariance between trait and fitness at the level of the social group, because the group's constituents belong to separate, irreconcilable classes.

Highlights

Having moved on from the controversy as to whether or not selection can operate at multiple levels – which was, in part, fuelled by confusing the weak notion of selection at the group level with the much stronger notion of adaptation at the group level – social evolution theorists widely agree that a covariance between group trait and group fitness may arise in the natural world, resulting in a response to group selection
A genetical approach to multilevel selection (MLS) addresses several of the difficulties that have beset this theory of social evolution
I have resolved the meaning of group trait and group fitness, highlighted that MLS is defined by change in a genetical character driven by its covariance with fitness at individual and group levels and clarified the connection between MLS and Simpson’s paradox

Summary

GARDNER

School of Biology, University of St Andrews, St Andrews, UK doi: 10.1111/jeb.12566 Keywords: class structure; covariance; emergence; evolutionary genetics; group selection; natural selection; Price’s theorem; reproductive value; Simpson’s paradox; social evolution.

Introduction

Conclusion