The added effect it has on its own genes passed into the next generation is its inclusive fitness: the sum of all the benefits and costs, discounted by the degree of kinship with each other group member. With inclusive fitness the unit of selection had passed subtly from the gene to the individual.
At first I found the theory of inclusive fitness, winnowed down to a few cases of kin selection that might be studied in nature, enchanting. In 1965, a year after Hamilton’s article, I defended the theory at a meeting of the Royal Entomological Society of London. Hamilton himself was at my side that evening. In my two books formulating the new discipline of sociobiology, The Insect Societies (1971) and Sociobiology: The New Synthesis (1975), I promoted kin selection as a key part of thegenetic explanation of advanced social behavior, treating it as equal in importance to caste, communication, and the other principal subjects that make up sociobiology. In 1976 the eloquent science journalist Richard Dawkins explained the idea to the general public in his best-selling book The Selfish Gene . Soon kin selection and some version of inclusive fitness were installed in textbooks and popular articles on social evolution. During the following three decades a large volume of general and abstract extensions of the theory of kin selection was tested, especially in ants and other social insects, and purportedly found proof in studies on rank orders, conflict, and gender investment.
By 2000 the central role of kin selection and its extensive inclusive fitness had approached the stature of dogma. It was a common practice for writers of technical papers to acknowledge the truth of the theory, even if the content of the data to be presented were only distantly relevant to it. Academic careers had been built upon it by then, and international prizes awarded.
Yet the theory of inclusive fitness was not just wrong, but fundamentally wrong. Looking back today, it is apparent that by the 1990s two seismic flaws had already appeared and begun to widen. Extensions of the theory itself were growing increasingly abstract, hence remote from the empirical work that continued to flourish elsewherein sociobiology. At the same time the empirical research devoted to the theory remained limited to a small number of measurable phenomena. Writings on the theory mostly in the social insects were repetitive. They offered more and more about proportionately fewer topics. The grand patterns of ecology, phylogeny, division of labor, neurobiology, communication, and social physiology remained virtually untouched by the asseverations of the inclusive theorists. Much of the popular writing devoted to it was not new but affirmative in tone, declaring how great the theory was yet to become.
Inclusive fitness theory, fondly called IF theory for short by its defenders, was showing increasing signs of senescence. By 2005 questions about its soundness were being openly expressed, especially among leading experts on the details of the biology of the ants, termites, and other eusocial insects, as well as a few theoreticians bold enough to seek alternative explanations of the origin and evolution of eusociality. The researchers most committed to IF theory either ignored these deviations or summarily dismissed them. By 2005 they had gained enough representation in the anonymous peer review system to hinder publication of contrary evidence and opinions in leading journals. For example, a keystone early support of inclusive fitness theory, cited in textbooks, was the prediction of overrepresentation of theHymenoptera (bees, wasps, ants) among eusocial animal species. When after a time one investigator pointed out that new discoveries had nullified the prediction, he was told, in effect, “We already knew that.” They did know that, but hadn’t done more than just drop the subject. The “Hymenoptera hypothesis” was not wrong; it had just become “irrelevant.” When a