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

Abstract

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.

Keywords: Hamilton's rule; class structure; inclusive fitness; invasion fitness; lineage; non-additive interactions.

Figure 1.

Simulations of the fates of lineages founded by a single mutant in an additive social dilemma (i.e. when b = b and c = c from equation (2.2) with b and c constant). In each of the panels, the grey lines represent one instance of the invasion process, whereas the thicker red line is the average of 500 simulations. When a grey line disappears below vertically, the mutant lineage has gone extinct. In all panels, r = 0.2. In the top row, there is no class structure and c = 0.2. The top left has b = 1.1 and top right b = 0.9. The two benefit values straddle the threshold for the invasion fitness ρ to be greater than one (i.e. satisfying Hamilton's rule, or equivalently, the mutant trait being adaptive). These figures demonstrate that while plenty of lineages either increase or go extinct in each case, Hamilton's rule predicts the average behaviour of many such invasions, hence the expected outcome of the evolutionary process. In the bottom row, we simulate a case with two classes of individuals, subordinates and dominants (as described in §3) with where subordinates forgo almost all reproduction (s = 0.01) to help the dominants and pay a cost , while dominants do not help subordinates, In the bottom left panel, the benefit to the dominant is and in the bottom right, it is As in the non-class-structured case, individual lineages might increase or go extinct, and the class-structured version of Hamilton's rule (equation (3.1)) predicts the expected success of the lineage in the bottom left and extinction in the bottom right. (Online version in colour.)