Group and individual selection during evolutionary transitions in individuality: meanings and partitions

Abstract

The Price equation embodies the ‘conditions approach’ to evolution in which the Darwinian conditions of heritable variation in fitness are represented in equation form. The equation can be applied recursively, leading to a partition of selection at the group and individual levels. After reviewing the well-known issues with the Price partition, as well as issues with a partition based on contextual analysis, we summarize a partition of group and individual selection based on counterfactual fitness, the fitness that grouped cells would have were they solitary. To understand ‘group selection’ in multi-level selection models, we assume that only group selection can make cells suboptimal when they are removed from the group. Our analyses suggest that there are at least three kinds of selection that can be occurring at the same time: group-specific selection along with two kinds of individual selection, within-group selection and global individual selection. Analyses based on counterfactual fitness allow us to specify how close a group is to being a pseudo-group, and this can be a basis for quantifying progression through an evolutionary transition in individuality (ETI). During an ETI, fitnesses at the two levels, group and individual, become decoupled, in the sense that fitness in a group may be quite high, even as counterfactual fitness goes to zero. This article is part of the theme issue ‘Fifty years of the Price equation’.

The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

“…Many of the major conceptual topics surrounding the evolution of multicellularity fall under this category. These include: (i) how multicellular groups form and become Darwinian units capable of adaptation [ 18 , 29 , 30 , 31 , 32 , 33 ], (ii) how the transition to multicellularity affects subsequent evolutionary processes [ 6 , 34 ], (iii) how cooperative behaviors associated with complex multicellular organisms (e.g., cellular differentiation) evolve and remain stable in the face of social defection [ 35 , 36 , 37 , 38 , 39 , 40 ], (iv) how multicellular life cycles arise and shape the subsequent evolution of multicellularity [ 13 , 14 , 41 ], and (v) how multicellular lineages co-opt and modify traits of their unicellular ancestor for novel multicellular purposes [ 21 , 27 , 42 , 43 , 44 ].…”

Variation and multilevel selection of SARS‐CoV‐2

“…Further considerations of individual and group selection were stimulated by the Price equation (Price 1972), which describes selection at multiple hierarchical levels and “provides an ideal framework for addressing philosophical questions about the levels of selection” (Okasha 2006). Based on the Price equation, Shelton and Michod (2020) suggest that several types of selection should be considered in a group‐structured population (e.g., within‐group individual selection, between‐group selection, and global individual selection). When a pathogen infects a host population, selection on the pathogen can be conceptualized as within‐host individual selection, between‐host group selection, and global individual selection.…”

“…2) have been evolving in bat and perhaps other animal populations for some time. Driven by global individual selection (Shelton and Michod 2020), a strain can jump to human hosts, and this has occurred to produce SARS‐CoV and SARS‐CoV‐2. While to date the data are fragmentary and inconclusive, the following scenario remains plausible for the latter.…”

“…Finally, we should keep in mind that the conditions that produced the SARS‐CoV‐2 pandemic have not changed. As human society occupies more and more of the biosphere, global individual selection (Shelton and Michod 2020) increasingly favors parasites that invade human‐related niches—human crops, human livestock, and human beings.…”

Life history tradeoffs, division of labor and evolutionary transitions in individuality

“…Recent work has helped solving these issues by proposing a new interpretation of fitness at different levels of organization (Shelton & Michod, 2014, 2020). Following this new interpretation, the term “cell fitness” does not represent the cell’s fitness within the collective but rather the one it would have if it were without a collective (counterfactual fitness).…”