Hamilton's rule generalized: Foundations of Social Evolution by Steven A. Frank

Abstract

Princeton University Press, Monographs in Behavior and Ecology, 1998. £35.00 / $49.50 hbk, £13.95 / $16.95 pbk (ix + 268 pages)ISBN 0 691 05933 0 / 0 691 05934 9Social evolution has been a controversial subject. Its products are all around us, but discussions as to whether they are the result of natural selection, cultural evolution or both still have a tendency to quickly blur distinctions between scientific arguments and political, philosophical and religious convictions.‘Social evolution occurs when there is a tension between conflict and cooperation’. This first sentence of Steven Frank's book, Foundations of Social Evolution, sets the agenda of an ambitious attempt to show that the theory of social evolution is not just an idiosyncratic branch for ant hunters and Australian bird watchers (most social birds occur on the fifth continent), but an important general framework, providing new and pivotal insights to general evolutionary questions. The opening sentence can be turned around to mean that there can only be equilibrium (stasis) in a social system when the costs of conflict are balanced by the advantages of cooperation. Any consistent imbalance between these two forces will induce social evolution – that is, changes in the mean and/or variance of social traits – but the actual causes of such change can be manifold: genetic, ecological, socio-economical and cultural.Reading this book, one quickly notices that it mainly addresses issues of social natural selection. As it turns out, this is not because the author wants to single out genetic conflict (although there is a fair amount of coverage of genetic issues), but because he wants to drive another point home: that by concentrating on the common characteristics of the factors (vectors) that have the potential to make social systems change, one can gain surprising insights in fundamental, general aspects of biological organization.The architect of Frank's foundations is W.D. Hamilton, whose seminal papers in the 1960s and early 1970s have inspired much of what has happened in evolutionary and behavioural ecology. After a brief introduction of fundamental insights by Ronald Fisher and George Price, the first chapters of the book are devoted to Hamilton's rule (that cooperative behaviour will evolve when the average inclusive fitness benefits exceed the direct fitness costs to the actor): its formal derivation, its general significance and its ramifications. In what follows, Frank develops a number of parallels between natural selection and economic principles. He shows that much of the foundations of social evolution can be reduced to three basic exchange mechanisms of value: the correlation between trait-values among social partners (relatedness); the expected contribution to the future population (reproductive value); and marginal valuation yielding a common currency for comparative analysis of cost and benefit (which turns out to be equivalent to frequency dependence in subsequent examples). The final chapters provide an integrative review and expansion of sex-allocation theory in the light of these economically inspired generalizations.The conclusion is that Hamilton's rule is very general: shared genealogy is only one process that causes statistical association between traits of interacting individuals. As far as cultural or non-kin interactions can achieve the same statistical associations, their basic dynamics can be understood by a similar Hamiltonian approach. What matters for pay-offs is the information content or predictability of a social interactant. Formulated like this, Hamilton's rule becomes a fundamental theorem, having ramifications for such seemingly disparate issues as the tragedy of the commons, optimal dispersal, juvenile mortality, cytoplasmic incompatibility, signalling and parasite virulence. In other words, nothing in social evolution makes sense except in the light of kin selection.This book is a must for every evolutionary biologist interested in synthetic concepts, kinship theory, optimization principles, sex allocation and much more. My criticism is that it is not easy for a non-mathematical reader to see the wood for the trees. Although the derivations are indispensable to prove the generalizations made, I could not help feeling that more effort should have been made to put the maths into boxes, so that it would be easier for those readers inclined to assume the calculus correct to follow the verbal arguments. Otherwise, the book is a major achievement. It integrates and synthesizes several areas where evolutionary theory has been remarkably successful in making testable predictions and highlights issues where further progress towards a general theory of evolution can be expected. The best that can ultimately happen to a scientific theory is being proven to be a special case of a more general theory. Steven Frank's book shows some of the ways in which this is likely to happen to Hamilton's rule in the years to come.