There is no fitness but fitness, and the lineage is its bearer

Abstract

One contribution of 18 to a theme issue 'The evolution of cooperation based on direct fitness benefits'. Inclusive fitness has been the cornerstone of social evolution theory for more than a half-century and has matured as a mathematical theory in the past 20 years. Yet surprisingly for a theory so central to an entire field, some of its connections to evolutionary theory more broadly remain contentious or underappreciated. In this paper, we aim to emphasize the connection between inclusive fitness and modern evolutionary theory through the following fact: inclusive fitness is simply classical Darwinian fitness, averaged over social, environmental and demographic states that members of a gene lineage experience. Therefore, inclusive fitness is neither a generalization of classical fitness, nor does it belong exclusively to the individual. Rather, the lineage perspective emphasizes that evolutionary success is determined by the effect of selection on all biological and environmental contexts that a lineage may experience. We argue that this understanding of inclusive fitness based on gene lineages provides the most illuminating and accurate picture and avoids pitfalls in interpretation and empirical applications of inclusive fitness theory.

Invasion fitness, inclusive fitness, and reproductive numbers in heterogeneous populations

“…The mathematical theory we present thus provides a formal framework for understanding the broad notion that fitness measures must align (e.g., Metz et al. ; Rousset ; Roff ; Akçay and Van Cleve ). Our results also reveal interesting features of the different fitness measures, which we now discuss.…”

“…Lineage fitness can be interpreted as a gene‐centered measure of fitness (Dawkins , ), as this perspective emphasizes that it is the combined fitness effects of all replica gene copies of a mutant lineage in the population that matters for selection (e.g., Dawkins ; Haig ; Rousset ; van Baalen ; see also Akçay and Van Cleve ). Accordingly, lineage fitness can be thought of as the goal function of a focal strategic gene (Dawkins ; Haig , ); namely, a gene (lineage) attempting to maximize its own transmission for a population where individuals behave according to the strategy of another gene.…”

“…Despite their apparent differences, it has been emphasized that the various fitness measures are in fact tightly connected (Rousset , p. 194, Akçay and Van Cleve ). For example, when groups are of constant size, the inclusive fitness effect amounts to evaluating the sensitivity of the number of emigrants or of invasion fitness with respect to variation in continuous trait values (Ajar ; Lehmann et al.…”

Inclusive fitness is an indispensable approximation for understanding organismal design

“…; Allen et al. ; Allen ; Allen and Nowak ; Nowak and Allen ; Akçay and Van Cleve ; van Veelen et al. ) have suggested abandoning inclusive fitness for what they refer to as “standard natural selection” models, which track gene frequencies.…”

Reproductive success is predicted by social dynamics and kinship in managed animal populations

“…For example, see the following for a recent paper which uses a game theoretic approach to ask behavioral questions in an inclusive fitness context: Akçay &Van Cleve, 2016 1 .…”