Kin selection as the key to altruism: its rise and fall

Social Research, Spring, 2005 by Edward O. Wilson

ONE OF THE ENDURING UNSETTLED ISSUES OF EVOLUTIONARY BIOLOGY is the paradox of collateral altruistic behavior--that is, when some individuals subordinate their own interests and those of their immediate offspring in order to serve the interests of a larger group beyond offspring (Wilson, 1975). How might such behavior evolve if the genes promoting it are at such a disadvantage in competition with genes that oppose it?

Charles Darwin saw that the paradox was dangerous to his theory of evolution by natural selection. He was particularly concerned by the social behavior of ants. Not only do flagrantly selfless individuals exist, but they form distinct worker castes, which in some species are subdivided further into specialized subcastes--for example, large, aggressive (but sterile) soldiers and small nurses and foragers. How could such creatures come into existence if they never reproduce? Darwin solved the dilemma to his own satisfaction and that of other biologists for nearly a hundred years by noting that if the combined offspring of the queen ant formed a colony that allowed her to produce more offspring than could an otherwise comparable solitary female, sterile castes would evolve as part of the variation of a single hereditary type. That hereditary type, not the plastic forms it produces, is therefore the unit of selection. The altruistic castes, he said, are like the well-flavored vegetable part in a single crop strain produced by selective breeding (Darwin, 1859).

In 1932 and again in 1955 J. B. S. Haldane, one of the founders of the modern genetic theory of evolution, put a new twist on the altruism problem (Haldane, 1932; 1955). He pointed out how selflessness could evolve even if individuals are not organized into societies. His solution later came to be known as kin selection. Your genes, Haldane said, can be multiplied in a population even if you never reproduce, providing your actions favor the differential survival and reproduction of collateral relatives, such as siblings, nieces, and cousins, to sufficient degree. Suppose, he argued, you see a relative drowning, and if in rescuing him you have a one-tenth chance of drowning yourself. Your genes, including those predisposing you to perform this act of altruism, will nevertheless be increased in the population if such actions increase the number of offspring of the relative by more than the reciprocal of the fraction of genes you share by common descent with the person saved. Thus, if the drowning person is a brother (one-half genes shared) you need only increase the number of his children by more than twice, if a nephew (one-fourth genes shared) the payoff needs only to be more than fourfold, and so on.

In 1964 and in subsequent publications, William D. Hamilton expanded this perception into a general theory (Hamilton, 1964). He defined the property of inclusive fitness, which totals the result of all interactions, whether altruistic, neutral, or negative, throughout a group of relatives and nonrelatives. Turning to ants and other social insects, Hamilton then proposed a theory of the origin of colonies separate from (but not contrary to) the competition among colonies and solitaires conceived by Darwin. By brilliant insight, he connected the following two facts. First, the haplodiploid mechanism practiced by the Hymenoptera (ants, bees, and wasps), in which fertilized eggs become females and unfertilized eggs become males, causes full sisters to be more closely related to one another (by three-fourths) than are mothers and daughters (one-half). Second, almost all of the known 11 independent origins of such colonial life in nature have occurred in the Hymenoptera. Only one such phylad (branch of an evolutionary tree), the termites, was known in the 1960s that practice ordinary, diplodiploid sex determination. In diplodiploidy, sisters are no more closely related than are mothers and daughters. Hamilton concluded, quite reasonably, that kin selection is a decisive driving or at least strongly biasing force in the origin of the advanced insect colonies. In such colonial phylads, sterile workers put more of their genes into the next generation by sacrificing their personal reproduction, and even their lives, to produce sisters as opposed to daughters.

Hamilton's perception, later called the haplodiploid hypothesis, and intensively promoted (not least by myself, while synthesizing the new discipline of sociobiology in the 1970s [Trivers and Hare, 1976]), became firmly entrenched as an explanatory idea in studies of the evolution of animal colonies. It became further influential in the study of human societies under the aegis of the branch of sociobiology usually called evolutionary psychology.

The core conception by Haldane and Hamilton is expressed in what has come to be called Hamilton's rule:

rb > c

That is, altruistic behavior will evolve if the benefit b in offspring to the recipient discounted (multiplied by) the fraction of genes shared by common descent between recipient and altruist exceeds the cost in offspring to the altruist. Hamilton's rule, until very recently, has been the textbook encapsulation of the binding force in the origin of colonies that contain altruistic workers.