Individual selection and altruistic relationships: the legacy of W. D. Hamilton.

Bill Hamilton, one of the most influential Darwinian thinkers of our time, was, above all, immensely curious. He was intrigued by nature's riddles, whether they arose in his backyard or in the faraway rain forests of Brazil or Africa, where he recently came to his tragic death. Walking with him in the woods or in the desert, sometimes even in a crowded street in the midst of a city, one had to expect an adventure; an uncommon beetle or some unexplained behavior of a bird could turn an innocent journey into a research expedition. There was a continuity between the curiosity of the person as revealed in his backyard research and the most basic questions dealt with in his scientific work. Why do we grow old (Hamilton 1966)? Why does the sex ratio come close to even in one population but deviate from it in another (Hamilton 1967)? Why is it that we so often observe gregarious behavior of a potential prey when such behavior could apparently only be of advantage to its predator (Hamilton 1971a,b)? Why is it that the investment in dispersal is so often high even in cases where the expected reproductive success far from home is apparently no larger than it is close to home (Hamilton and May 1977, 1980)? And finally, a central theme in his last 20 years of research, Why do we reproduce sexually (e.g., Hamilton, 1980; Hamilton et al., 1981; Hamilton and Zuk, 1982; and many later works)? Hidden in these papers are many concepts and ideas that later would become widely accepted as being central to the quantitative theory of evolution. Perhaps the most prominent example is that of the Unbeatable Strategy (Hamilton, 1967), which foreshadowed the future development of the concept of ESS (Maynard Smith and Price, 1973). Yet, for most biologists and social scientists, Hamilton's name was, and still is, connected most intimately with the evolution of altruistic behavior (Hamilton 1963, 1964, 1970, 1971b, 1972). In the present paper we concentrate on that part of his work. However, almost any subject that he studied can be interpreted in terms of the basic philosophy that led him to his insights about the evolution of altruistic traits. Altruistic traits, a term first coined by Haldane (1932), are those that decrease the fitness of their carrier but increase that of other individuals in the population. While still an undergraduate student in Cambridge, Hamilton wondered how natural selection can maintain traits that, even if advantageous for the population, apparently reduce the number of their carriers below their share in the population? The answer he gave to this question is now referred to as Hamilton 's rule: An inherited behavior is selected for in a population if and only if it results in an increase in the number of genes, identical by descent to those of the individual doing that behavior, namely those genes carried by the offspring of the individual in question or by its other relatives. To measure the effect of one's behavior on the number of his or her genes in the population, Hamilton first employed Wright 's kinship coefficient (Wright, 1922), measuring relatedness by the chance r that an allele carried by one individual would be identical by descent to an allele carried by its relative. Employing this measure of relatedness, Hamilton concluded that natural selection would favor altruism toward a relative if and only if the ratio doi:10.1006 tpbi.2000.1507, available online at http: www.idealibrary.com on