Kin Selection as the Key to Altruism: Its Rise and Fall

Edward O. Wilson Kin Selection as the Key to Altruism: Its Rise and Fall 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 immedi­ ate 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 subdi­ vided further into specialized subcastes—for example, large, aggressive (but sterile) soldiers and small nurses and foragers. How could such crea­ tures 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 ofthe queen ant formed a colony that allowed her to produce more offspring than could an otherwise comparable solitaiy female, sterile castes would evolve as part ofthe variation ofa single hereditaiy type. That hereditaiy type, not the plastic forms it produces, is therefore the unit of selection. The altru­ istic 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 modem genetic theoiy of evolution, put a new twist on the altrusocial research Vol 72 : No 1 : Spring 2005 159 ism 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 rescu­ ing 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, w hether 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 sepa­ rate 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 moth­ ers and daughters (one-half). Second, almost all of the known 11 inde­ pendent 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 160 social research 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...