Jonathan Birch

Working together creates mutual obligations. For example, the members of a football team owe it to each other to work hard for the good of the team. A player who doesn’t try hard enough, or who makes a costly mistake, lets the side down. When the team loses, feelings of responsibility, guilt, and shame ensue. Players ought to feel committed to the team and responsible for its failures. If they don’t, they deserve to be dropped. The idea at the heart of Michael Tomasello’s ‘natural history’ of human morality is that these oughts—the oughts of teamwork—were the first oughts.

Hamilton’s theory of kin selection is the best-known framework for understanding the evolution of social behavior but has long been a source of controversy in evolutionary biology. A recent critique of the theory by Nowak, Tarnita, and Wilson sparked a new round of debate, which shows no signs of abating. In this overview, we highlight a number of conceptual issues that lie at the heart of the current debate. We begin by emphasizing that there are various alternative formulations of Hamilton’s rule, including a general version, which is always true; an proximate version, which assumes weak selection; and a special version, which demands other restrictive assumptions. We then examine the relationship between the neighbor-modulated fitness and inclusive fitness approaches to kin selection. Finally, we consider the often-strained relationship between the theories of kin and multilevel selection.

The theories of inclusive fitness and multilevel selection provide alternative perspectives on social evolution. The question of whether these perspectives are of equal generality remains a divisive issue. In an analysis based on the Price equation, Queller argued (by means of a principle he called the separation condition) that the two approaches are subject to the same limitations, arising from their fundamentally quantitative-genetical character. Recently, van Veelen et al. have challenged Queller’s results, using this as the basis for a broader critique of the Price equation, the separation condition, and the very notion of inclusive fitness. Here we show that the van Veelen et al. model, when analyzed in the way Queller intended, confirms rather than refutes his original conclusions. We thereby confirm (i) that Queller’s separation condition remains a legitimate theoretical principle and (ii) that the standard inclusive fitness and multilevel approaches are indeed subject to the same limitations.

Inclusive fitness theory was not originally designed to explain the major transitions in evolution, but there is a growing consensus that it has the resources to do so. My aim in this paper is to highlight, in a constructive spirit, the puzzles and challenges that remain. I first consider the distinctive aspects of the cooperative interactions we see within the most complex social groups in nature: multicellular organisms and eusocial insect colonies. I then focus on one aspect in particular: the extreme redundancy these societies exhibit. I argue that extreme redundancy poses a distinctive explanatory puzzle for inclusive fitness theory, and I offer a potential solution which casts coercion as the key enabler. I suggest that the general moral to draw from the case is one of guarded optimism: while inclusive fitness is a powerful tool for understanding evolutionary transitions, it must be integrated within a broader framework that recognizes the distinctive problems such transitions present and the distinctive mechanisms by which these problems may be overcome

Hamilton introduced two conceptions of social fitness, which he called neighbour-modulated fitness and inclusive fitness. Although he regarded them as formally equivalent, a re-analysis of his own argument for their equivalence brings out two important assumptions on which it rests: weak additivity and actor's control. When weak additivity breaks down, neither fitness concept is appropriate in its original form. When actor's control breaks down, neighbour-modulated fitness may be appropriate, but inclusive fitness is not. Yet I argue that, despite its more limited domain of application, inclusive fitness provides a distinctively valuable perspective on social evolution.

The notion that natural selection is a process of fitness maximization gets a bad press in population genetics, yet in other areas of biology the view that organisms behave as if attempting to maximize their fitness remains widespread. Here I critically appraise the prospects for reconciliation. I first distinguish four varieties of fitness maximization. I then examine two recent developments that may appear to vindicate at least one of these varieties. The first is the ‘new’ interpretation of Fisher's fundamental theorem of natural selection, on which the theorem is exactly true for any evolving population that satisfies some minimal assumptions. The second is the Formal Darwinism project, which forges links between gene frequency change and optimal strategy choice. In both cases, I argue that the results fail to establish a biologically significant maximization principle. I conclude that it may be a mistake to look for universal maximization principles justified by theory alone. A more promising approach may be to find maximization principles that apply conditionally and to show that the conditions were satisfied in the evolution of particular traits.

Evolution and Rationality marks the end of a three-year project, ‘Evolution, Cooperation, and Rationality’, directed at the University of Bristol by the book’s editors, Samir Okasha and Ken Binmore. The collection draws together the editors’ pick of the papers delivered at the conferences the project hosted, and covers a wide range of topics at the intersection of evolutionary theory and the social sciences. It is a splendid anthology: timely, interdisciplinary, thematically cohesive, and full of substantive and interesting disagreements between the contributors