Taming fitness: Organism‐environment interdependencies preclude long‐term fitness forecasting

Abstract

Fitness is a central but notoriously vexing concept in evolutionary biology. The propensity interpretation of fitness is often regarded as the least problematic account for fitness. It ties an individual's fitness to a probabilistic capacity to produce offspring. Fitness has a clear causal role in evolutionary dynamics under this account. Nevertheless, the propensity interpretation faces its share of problems. We discuss three of these. We first show that a single scalar value is an incomplete summary of a propensity. Second, we argue that the widespread method of "abstracting away" environmental idiosyncrasies by averaging over reproductive output in different environments is not a valid approach when environmental changes are irreversible. Third, we point out that expanding the range of applicability for fitness measures by averaging over more environments or longer time scales (so as to ensure environmental reversibility) reduces one's ability to distinguish selectively relevant differences among individuals because of mutation and eco-evolutionary feedbacks. This series of problems leads us to conclude that a general value of fitness that is both explanatory and predictive cannot be attained. We advocate for the use of propensity-compatible methods, such as adaptive dynamics, which can accommodate these difficulties.

Tradeoff breaking as model of evolutionary transitions in individuality and the limits of the fitness decoupling metaphor

“…One classical way to characterise particle fitness is to measure long-term reproductive success under a given set of environmental conditions relative to other particles (Pence & Ramsey, 2013; Doulcier et al, 2021). In a more practical sense, fitness is often measured as a per capita growth rate—that is, the average number of offspring produced by an individual per unit of time (or per generation) (Fisher, 1930; Metz et al, 1992).…”

“…Note importantly that we assume here that whether an entity is in a given environment is independent of its type. If a dependence of the environment on the type exists, this environment effectively becomes an extended phenotype (Lu and Bourrat 2018). If the environmental changes are not deterministic, a weaker condition than the same temporal succession of environments is that the two organisms experience the same distribution of environments and transition probabilities between environments (steady-state) (see Doulcier et al, 2021). This type of scenario is not discussed in the main text (but see Box 3).…”

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

“…The main reason is that it seems to imply that fitness is a material quantity that can be transferred from one entity to another, comparable to a liquid that can be poured from one container to another. While, at first glance, this analogy may seem a helpful image to get an intuitive idea of the problem, it contradicts our modern understanding of fitness as a predictor of evolutionary success (Bourrat, 2015a, 2015b; Doulcier et al, 2021). First, it implies that some cells with nil fitness or close to it are not dead, contradicting the principle of natural selection.…”

“…Instead, it must be tied to its potential success (or success in the long run). Without this point acknowledged, fitness is condemned to be tautological, as philosophers and biologists alike have long recognized (Manser, 1965; Popper, 1974; Smart, 2014; reviewed in Doulcier et al, 2021). 2 This conundrum led to establishing several frameworks for the interpretation of fitness, one among which is the propensity interpretation of fitness (Beatty, 1984; Brandon, 1978; Pence & Ramsey, 2013).…”

Facts, Conventions, and the Levels of Selection

“…Suppose a two-level setting in which particles are nested in collectives. Suppose, further, that collective-level and particle-level reproduction occurs 58 Another way to make the same point is that several authors have argued that, to be associated with natural selection, fitness must be a "static" property (see Ramsey 2006;Abrams 2009;Pence and Ramsey 2013;Bourrat 2015a;Bourrat 2017;Doulcier et al 2021). If fitness is variable, as in Okasha's example, it can no longer refer to natural selection.…”