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Home , Kin selection, Sociality

Proc. Nati Acad. Sci. USA Vol. 78, No. 7, pp. 4440-4443, July 1981

Genes, individuals, and ( and /cost of selection) PHILIP J. DARLINGTON, JR. Museum ofComparative Zoology, Harvard University, Cambridge, Massachusetts 02138 Contributed by Philip J. Darlington, Jr., March 26, 1981 ABSTRACT The altruistic- theory of kin selection re- form demes consisting only of bearers of a new, rare altruistic quires conditions so improbable that its reality is doubtful. The gene within a population made up mainly of nonaltruists, and gene-quantity theory, including the theory of inclusive , then that nonaltruists dispersing from elsewhere in the popu- assumes that selection acts on sums of kins' , but no effective lation do not enter the demes later and compete with and elim- mechanism is apparent. Insect and human societies may have inate the altruists. These conditions are improbable. A better evolved by individual selection, in two steps: first something made explanation ofspread ofaltruistic genes, which does not depend staying together advantageous to individuals, and then altruistic on kin selection, is that the genes increase rather than decrease behaviors evolved in net-gain lotteries, also (statistically) advan- the fitness of individuals them, in net-gain lotteries, tageous tindividuals. Kin seleition is not required in these or any carrying other unequivocal cases; the theory should be reexamined and as described later in the present paper. probably abandoned. The probability of kin selection is further The gene-quantity theory of kin selection is that kin share reduced by the cost of evolution by selection. Much current evo- identical genes in proportion to ; that to kin in- lutionary mathematics and determinist , which ignore creases the quantity of genes identical with the altruist's own how the cost of selection limits the precision of adaptations, in- in the next generation; that this is selectively advantageous if cluding adaptive behaviors, may be dangerously unrealistic. the cost to the altruist in loss of offspring is less than the gain in genes, some or all ofthe altruist's own offspring being traded Many influential biologists, including mathematicians (e.g., ref. offfor more-than-equivalent quantities ofgenes transmitted by 1), sociobiologists (e.g., ref. 2), and determinists (e.g., ref. 3), kin (this being the essential dogma of the theory); and that for accept the geneticitheory ofkin selection, and some ofthem try this reason (with no other return to the altruists) genetically to explain human behavior by it. Ifthis is a mistake, the sooner determined behaviors by which individuals select kin to be the it is corrected the better.MTheories such as this, that purport to beneficiaries ofaltruism have evolved by selection. This theory explain us to ourselves, are like maps of dangerous terrain. If was proposed by Hamilton (1) and is graphically illustrated by they are correct, we need them and should not blame them for Wilson in Sociobiology (ref. 2, p. 119, figure 5-9). the dangers. But if they are wrong, they are dangerous in For example-the example parallels Haldane's (4) two-broth- themselves. ers case but is not the same, because he was concerned with My thesis now is that the complex mathematical theory ofkin single altruistic genes rather than with gene quantities-kin- selection is vulnerable because it is based on mistaken assump- selection theorists calculate that half the genes ofbrothers are tions, and that the assumptions rather than the complexities identical, derived by replication of the genes of their common need reexamination. parents; that if one brother saves another from drowning and enables him to reproduce, the one (in effect) transmits half his own genes through his brother and adds them to the quantity DEFINITIONS AND DISCUSSION ofgenes he transmits himself; and thatfor this reason--because Two theories ofkin selection are current, although they are not it increases the quantity ofgenes identical with the altruist's own always clearly distinguished. One theory is concerned with sin- in the next generation-selection should have put brothers un- gle altruistic genes; the other, with quantities of genes ex- der strong, genetically determined compulsion to save each pressed as fractions ofgenotypes. Both theories are determinist; other, if the risk (expected cost) is less than half the altruist's they assume that individuals' behavior is determined in consid- own chance of surviving and reproducing. erable detail by their genes. This calculation is usually accepted uncritically, and'has been The altruistic-gene theory ofkin selection is that a single gene endlessly repeated and elaborated. But if one brother lets an- may induce individuals to select kin for altruism, decreasing the other drown and takes his mate, the one runs no risk and hands altruists' own chances of surviving and reproducing-that is, on all his own genes instead ofonly half;,selection should there- decreasing their fitness-but increasing the chances of related fore have put brothers under even stronger compulsion to let individuals who are likely to carry the same gene. The gene is each other drown. The calculation ignores the probability that disadvantageous at first, but becomes advantageous ifit spreads a brother's offspring will compete with the altruist's own. And to all members of a population, all ofwhom then receive more it ignores the fact that all members of a Mendelian population benefit from each other than their altruism costs. Ingenious share many genes, so that altruism to a brother has only a small mathematical models, suggested by Haldane (ref. 4, p. 44) and genetic advantage over altruism to other individuals in the pop- recently reviewed by Boorman and Levitt (5), have been de- usual kin-selection vised to show how such a gene might spread through a popu- ulation. These criticisms suggest that the lation by genetic drift and small-deme selection. However, the arithmetic is oversimplified. models require first that kin altruism and random genetic drift However, the theory more than the arithmetic requires crit- icism. Two questions should be asked about it. First, how can The publication costs ofthis article were defrayed in part by page charge selection acton quantities ofgenes? The unit ofnatural selection payment. This article must therefore be hereby marked "advertise- is the individual; I (ref. 6, pp. 87-88 and 140-142) have argued ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. this point informally, and Hull (7) has put it in more formal

4440 Downloaded by guest on September 26, 2021 Evolution: Darlington Proc. Natl. Acad. Sci. USA 78 (1981) 4441 terms, concluding (p. 313) that"... only individuals can be se- the ' predisposition to , and I can suggest one: lected," although individuals are not always easy to recognize. ability to sting. The situation is comparable to that in Mullerian Genes may be selected if they benefit single individuals that mimicry, in which distasteful species evolve similarities so that carry them, or if they induce that benefits a taste of any one protects all against a predator. Among solitary two or more interacting individuals, or ifthey command support aculeates, each individual must sting for itself and risk its life for key individuals in groups, as in the described in doing so. (The risk lies in the predator's attack; the act ofsting- hereafter. But, except in special cases such as these, no mech- ing is itself fatal only to some .) But if individuals stay to- anism is apparent by which selection can favor either single gether, any one can sting for all. This gives a strong selective genes or gene quantities in the way kin-selection theory re- advantage to staying together, and anything that keeps individ- quires. Selection does increase the quantities of advantageous uals together may favor evolution of reciprocal altruistic behav- genes in a population, but this does not mean that individuals iors. Possession of the sting is only part of the advantage. Acu- act to "maximize representation of their genes in the next gen- leate have narrow-waisted, flexible bodies that eration." They act to maximize successful offspring-individu- allow them to aim the sting effectively; their mandibulate als-in continuing, adaptable lineages. Increase of gene quan- mouths allow them to manipulate objects (ref. 8, p. 328); and tities is the result ofthis process; it is not selectively advantageous the powerofflight ofprimitive social aculeates probably allowed in itself. This is conventional Darwinian theory, and if it is cor- them to use the resources of extended areas while living to- rect (as I think it is), the gene-quantity theory of kin selection gether. Note that stinging is not primarily altruistic; the stinger is unrealistic. protects itselfas well as its associates. The individuals that sting It follows that the current theory ofinclusive fitness (1), which are determined by chance, by which happen to meet predators is that the fitness of an individual is determined by the sum of or competitors, which is to say by a lottery. And the advantage genes carried by itself and its kin, is unrealistic too-mathe- is reciprocal, not dependent on kinship, although close kin are matically elegant but with no basis in reality-although I do not often involved. Not all social Hymenoptera sting now; some like to think what might happen to a Ph.D. candidate who tried have evolved other means of defense; but the primitive ones to tell his professor so! evidently did and still do. And not all can fly now; flightless The second question is, does selection favor transmitting worker have evolved other means of utilizing resources in identical genes? This is a question that kin-selection theorists smaller areas but perhaps more efficiently. usually do not ask, much less answer. It was asked me by a group The stinging hypothesis is only one possible alternative to kin ofnonprofessional naturalists, who asked why, ifselection favors selection in evolution of sociality in Hymenoptera. There may gene identity in offspring, most and outcross, so be others. Haploid/diploid sex determination may have played that the genes oftheir offspring are not identical but diversified? a part too, not by kin selection, but in ways suggested by Snell This is a deadly question for the genetic theory ofkin selection. (10) almost half a century ago. It allows deleterious recessive The conventional Darwinian answer is that gene diversity is to be eliminated promptly and cheaply. (Why does it not selectively advantageous because it promotes individual vari- occur more widely in other animals?) And it favors mutual rec- ability and population adaptability. Do individual plants and ognition and cooperation of colony mates, because a mutant animals expend energy and take risks to increase gene diversity gene may be immediately shared by all the workers in a colony. in their offspring, by outcrossing, and at the same time expend In , which do not sting, and in which sex determi- energy and take risks to reduce gene diversity, by altruism to nation is not haploid/diploid, what kept individuals together kin? And why should selection favor genes simply because they and initiated their social evolution is thought to have been their are identical? Identical genes may not be selectively advanta- dependence on symbiotic cellulose-digesting microorganisms geous; the genes of an average individual in a population are transmitted by "anal feeding" (ref. 11, p. 18). Individuals had presumably neither better nor worse than those of another av- to stay together to obtain symbionts from each other after molt- erage individual; and if an individual's genes are superior, what ing, and offspring had to stay with their parents to obtain sym- is the selective advantage to the individual of presence of its bionts, and social behaviors then evolved. But symbiont trans- superior genes in offsprings' probable competitors? A distinc- mission was not primarily altruistic; all individuals gained by tion is sometimes made between genes "identical by common the presence ofother individuals; the advantage was reciprocal. descent" and other identical genes, but what is the difference The Ant Colony. Closer analysis of a simple ant colony is in- to the individuals carrying them, if the selective effect of the structive. The colony may consist of one fertilized queen, who genes is the same? does all the reproducing, and (say) 99 sterile female workers My conclusion is that the theories of gene-quantity kin se- irrevocably committed to caring for the queen, who is their lection and are based on erroneous assumptions mother, and forheroffspring, who are their sisters and brothers. and should be abandoned. What, then, are alternative expla- This is all that most observers see, and it looks like a clear case nations of the of insect and human societies? of one-way kin altruism, the workers neither receiving nor ex- Insect Societies. We see something that looks like genetic pecting any return for their self-sacrifice. But we know now (and kin selection in aculeate (stinging) Hymenoptera. Sex deter- might have predicted) that whether a female becomes a queen mination in Hymenoptera is haploid/diploid, haploid (unfer- or a worker is not determined by her genes but by a lottery, by tilized) eggs producing males, diploid (fertilized) eggs produc- what food and care she happens to get as a (11). In the ing females; all the sperms that a female receives from one male simple ant colony just described, each individual female begins are genetically identical, and her daughters are then half-iden- with one chance in a hundred to become a reproducing queen tical-twin sisters; and societies based on sister altruism have rather than a worker. Of course this is oversimplified. New evolved about a dozen times in these insects-separately in queens do not reproduce in their natal colonies but later, in ants, , and bees, and repeatedly in some of these groups colonies they found themselves, and many queens fail to found (8). This is usually supposed to be cause and effect, the excep- colonies. But these complications do not change the fact that, tionally close genetic relatedness of sisters predisposing them as an egg, each female has a chance to be a queen rather than to evolve altruistic-social behaviors by kin selection. But some a worker, and that the outcome is determined by a lottery that entomologists, including Evans (9), who have studied social each female has achance to win. The workers' altruism therefore Hymenoptera think that factors other than kinship may explain contributes to the reproductive success of queens who might Downloaded by guest on September 26, 2021 ,.2 Evolution: Darlington Proc. Natl. Acad. Sci. USA 78 (1981) have been themselves. The queen carries genes that, although A secondary factor reduces the probability of kin selection: not expressed in herself, determine the supporting behaviors the cost of selection (ref. 6, pp. 113-117 and pages indexed). of her daughter workers. This system is like that in a multicel- can operate only by elimination. One lular organism, in which the fertilized germ cell carries genes substitution may cost the elimination ofmany times the number that, although not expressed in the germ itself, determine the of individuals in one generation of a population (14). One ad- supporting behaviors of the somatic daughter cells. In these aptation may require many allele substitutions. And in real pop- systems, individual queen ants and individual germ cells are ulations thousands of structures, functions, and behaviors are selected according to the support their genes can command, by under selection; each selective process is costly, and they affect ordinary Darwinian selection, with no need ofthe devious and each other in ways that increase costs, partly by the Red Queen improbable mechanism of "kin selection." effect (ref. 15, pp. 17 and following and note 32); the populations Human Societies. We see kin altruism in too, both themselves and their environments continually change in ways from parents to offspring and among collateral kin. These two that change selective forces; and populations cannot pay the cases differ in an essential way, and Dawkins (3, 12) was mis- cumulative costs. So, most organisms most ofthe time are prob- taken not to distinguish them. The difference is that some de- ably far from perfectly adapted to their environments, but are gree of parental altruism-at least the expenditure of energy just a little better than their competitors, for the time being. required for -is essential to continuity oflineages Specifically, cost would be expected to limit the evolution of and must be maintained by ordinary Darwinian selection, complex, genetically determined kin-recognition and kin-pref- whereas this is not true of altruism among collateral kin. Kin- erence behaviors in situations in which many selective pro- selection theorists interpret altruism among human sibs and cesses are going on together in populations and environments more distant kin as due to genetic kin selection. But anthro- that have changed as complexly and as rapidly as they have in pologists (e.g., ref. 13) find that the relationship between al- human populations in the last few thousand or few hundred truism and kinship is not precise in primitive societies, and we generations. see that altruism among people is not metered out in proportion For example, reciprocal-responsive altruism is simpler than to kinship, but excludes incompatible kin (history provides kin selection, but its precision too would be expected to be lim- many examples) and includes unrelated friends and sometimes ited by the cost of its evolution by selection. Much human be- strangers. What we see does not fit the predictions of kin-se- havior does seem to conform to a general pattern ofaltruism and lection theory, but looks more like reciprocal-responsive altru- response, but both the offers of altruism and the responses are ism (ref. 6, pp. 149-150) in which offers of altruism are made far from consistent or precise. good only if responded to, and which form net-gain lotteries in which all compatible individuals gain or (unconsciously) expect CONCLUSIONS to gain more than their altruism costs. Kin are often included The altruistic-gene theory of kin selection is improbable, and in the lotteries but are not uniquely favored. This pattern of the gene-quantity theory, and also the theory of inclusive fit- behavior may reflect social rather than genetic pressures. If it ness, are based on erroneous assumptions. Supposed examples is genetic, the altruist may say (in effect), not "I help you because are better explained as results ofindividual selection. Until and you have my genes," but "Our genes make us respond to each unless kin-selection theorists can produce unequivocal cases other and help each other for our own and our offsprings' sakes." and can answer criticisms satisfactorily, students ofbehavior and This is genetically determined altruism, but not genetic kin se- especially of human behavior are wise to discount the theory. lection. In it, altruism is reciprocally advantageous; fitness is More broadly, we should discount the theories of any evo- measured by number ofsuccessful offspring, as it should be; the lutionists who do not define selection, or who define it as dif- unrealistic concept of inclusive fitness is dispensed with; and ferential reproduction or change ofgene ratios, without recog- altruistic behaviors evolve by ordinary Darwinian selection be- nizing that natural selection acts by elimination, and that its cost cause they are selectively advantageous to individuals, all of limits what evolution can do. Theoretical-mathematical models whom are statistically more likely to gain than lose by the al- of evolution that assume "maximization" or precision of adap- truistic transactions. tations are likely to be wrong because they ignore the cost of Our prehuman ancestors, incidentally, may first have been selection, and this is especially true ofsociobiology models that kept together by the advantages ofliving in groups-selectively assume that selection has determined details ofhuman behav- advantageous to all individuals in finding food and in defense- ior. Much current evolutionary mathematics and determinist and later by the additional advantages of social transmission of sociobiology may be not just a little wrong, but dangerously primitive technologies (transmitted by imitation) and informa- unrelated to reality. tion and ideas (transmitted by language). Postscript. Dawkins (12) lists "twelve misunderstandings of An important principle emerges from comparison of these kin selection." Some are inconsequential, but others seem to cases. Evolution ofsocieties seems usually to have involved two me to be valid criticisms which Dawkins does not answer sat- steps. First, something made staying together advantageousfor isfactorily, and which I repeat in my present paper. individuals, so that genes that kept individuals together were Finally, I should ask more bluntly a question, implied in established by individual selection. And then reciprocally ad- preceding pages, which proponents oftheories ofkin selection vantageous behaviors evolved, also by individual selection, in and inclusive fitness should be required to answer. What which altruism was not a one-way sacrifice but part of net-gain good-what selective advantage-is it to an individual to have lotteries in which all individuals gained or expected (were sta- its genes represented in other individuals which, in any ordi- tistically likely) to gain more than their altruism cost. The (hy- nary population, will be competitors? pothetical) factors that first made staying together advantageous were different in different cases: in social Hymenoptera, de- I thank Edward 0. Wilson and Howard E. Evans for reading my fensive-aggressive behavior; in termites, transmission of cel- manuscript and for useful criticism, but they are not responsible for my lulose-digesting symbionts; and in prehumans, transmission of conclusions. technologies, information, and ideas by imitation and language, 1. Hamilton, W. D. (1964)1. Theor. Biol. 7, 1-52. although the reciprocal advantages of defensive-aggressive be- 2. Wilson, E. 0. (1975) Sociobiology (Harvard Univ., Cambridge, havior may have helped keep prehumans together too. MA). Downloaded by guest on September 26, 2021 Evolution: Darlington Proc. Natl. Acad. Sci. USA 78 (1981) 4443

3. Dawkins, R. (1976) (Oxford, New York). 9. Evans, H. E. (1977) BioScience 27, 613-617. 4. Haldane, J. B. S. (1955) New Biology 18, 34-51. 10. Snell, G. D. (1932) Am. Nat. 66, 381-384. 5. Boorman, S. A. & Levitt, P. R. (1980) The Genetics ofAltruism 11. Oster, G. F. & Wilson, E. 0. (1978) Caste and in the (Academic, New York). Social Insects (Princeton Univ., Princeton, NJ). 6. Darlington, P. J., Jr. (1980) Evolutionfor Naturalists, The Simple 12. Dawkins, R. (1979) Z. Tierpsychol. 51, 184-200. Principles and Complex Reality (Wiley, New York). 13. Sahlins, M. (1976) The Use and Abuse ofBiology (Univ. of Mich- 7. Hull, D. R. (1980) Annu. Rev. Ecol. Syst. 11, 311-332. igan, Ann Arbor, MI). 8. Wilson, E. 0. (1971) The Insect Societies (Harvard Univ., Cam- 14. Haldane, J. B. S. (1957)J. Genet. 55, 511-524. bridge, MA). 15. Van Valen, L. (1973) Evol. Theory 1, 1-30. Downloaded by guest on September 26, 2021