Proc. Nati Acad. Sci. USA
Vol. 78, No. 7, pp. 4440-4443, July 1981
Evolution
Genes, individuals, and kin selection
(insect and human societies/cost of selection)
PHILIP J. DARLINGTON, JR.
Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138
Contributed by Philip J. Darlington, Jr., March 26, 1981
ABSTRACT The altruistic-gene theory of kin selection requires conditions so improbable that its reality is doubtful. The
gene-quantity theory, including the theory of inclusive fitness,
assumes that selection acts on sums of kins' genes, but no effective
mechanism is apparent. Insect and human societies may have
evolved by individual selection, in two steps: first something made
staying together advantageous to individuals, and then altruistic
behaviors evolved in net-gain lotteries, also (statistically) advantageous tindividuals. Kin seleition is not required in these or any
other unequivocal cases; the theory should be reexamined and
probably abandoned. The probability of kin selection is further
reduced by the cost of evolution by selection. Much current evolutionary mathematics and determinist sociobiology, which ignore
how the cost of selection limits the precision of adaptations, including adaptive behaviors, may be dangerously unrealistic.
form demes consisting only of bearers of a new, rare altruistic
gene within a population made up mainly of nonaltruists, and
then that nonaltruists dispersing from elsewhere in the population do not enter the demes later and compete with and eliminate the altruists. These conditions are improbable. A better
explanation ofspread ofaltruistic genes, which does not depend
on kin selection, is that the genes increase rather than decrease
the fitness of individuals carrying them, in net-gain lotteries,
as described later in the present paper.
The gene-quantity theory of kin selection is that kin share
identical genes in proportion to kinship; that altruism to kin increases the quantity of genes identical with the altruist's own
in the next generation; that this is selectively advantageous if
the cost to the altruist in loss of offspring is less than the gain
in genes, some or all of the altruist's own offspring being traded
off for more-than-equivalent quantities of genes transmitted by
kin (this being the essential dogma of the theory); and that for
this reason (with no other return to the altruists) genetically
determined behaviors by which individuals select kin to be the
beneficiaries of altruism have evolved by selection. This theory
was proposed by Hamilton (1) and is graphically illustrated by
Wilson in Sociobiology (ref. 2, p. 119, figure 5-9).
For example-the example parallels Haldane's (4) two-brothers case but is not the same, because he was concerned with
single altruistic genes rather than with gene quantities-kinselection theorists calculate that half the genes of brothers are
identical, derived by replication of the genes of their common
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
of genes he transmits himself; and thatfor this reason--because
it increases the quantity of genes identical with the altruist's own
in the next generation-selection should have put brothers under strong, genetically determined compulsion to save each
other, if the risk (expected cost) is less than half the altruist's
own chance of surviving and reproducing.
This calculation is usually accepted uncritically, and'has been
endlessly repeated and elaborated. But if one brother lets another drown and takes his mate, the one runs no risk and hands
on all his own genes instead ofonly half;,selection should therefore have put brothers under even stronger compulsion to let
each other drown. The calculation ignores the probability that
a brother's offspring will compete with the altruist's own. And
it ignores the fact that all members of a Mendelian population
share many genes, so that altruism to a brother has only a small
genetic advantage over altruism to other individuals in the population. These criticisms suggest that the usual kin-selection
arithmetic is oversimplified.
However, the theory more than the arithmetic requires criticism. Two questions should be asked about it. First, how can
selection act on quantities of genes? The unit ofnatural selection
is the individual; I (ref. 6, pp. 87-88 and 140-142) have argued
this point informally, and Hull (7) has put it in more formal
Many influential biologists, including mathematicians (e.g., ref.
1), sociobiologists (e.g., ref. 2), and determinists (e.g., ref. 3),
accept the geneticitheory of kin selection, and some of them try
to explain human behavior by it. If this is a mistake, the sooner
it is corrected the better.MTheories such as this, that purport to
explain us to ourselves, are like maps of dangerous terrain. If
they are correct, we need them and should not blame them for
the dangers. But if they are wrong, they are dangerous in
themselves.
My thesis now is that the complex mathematical theory ofkin
selection is vulnerable because it is based on mistaken assumptions, and that the assumptions rather than the complexities
need reexamination.
DEFINITIONS AND DISCUSSION
Two theories of kin selection are current, although they are not
always clearly distinguished. One theory is concerned with single altruistic genes; the other, with quantities of genes expressed as fractions of genotypes. Both theories are determinist;
they assume that individuals' behavior is determined in considerable detail by their genes.
The altruistic-gene theory of kin selection is that a single gene
may induce individuals to select kin for altruism, decreasing the
altruists' own chances of surviving and reproducing-that is,
decreasing their fitness-but increasing the chances of related
individuals who are likely to carry the same gene. The gene is
disadvantageous at first, but becomes advantageous if it spreads
to all members of a population, all of whom then receive more
benefit from each other than their altruism costs. Ingenious
mathematical models, suggested by Haldane (ref. 4, p. 44) and
recently reviewed by Boorman and Levitt (5), have been devised to show how such a gene might spread through a population by genetic drift and small-deme selection. However, the
models require first that kin altruism and random genetic drift
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4440
Evolution:
Darlington
terms, concluding (p. 313) that"... only individuals can be selected," although individuals are not always easy to recognize.
Genes may be selected if they benefit single individuals that
carry them, or if they induce reciprocal altruism that benefits
two or more interacting individuals, or if they command support
for key individuals in groups, as in the ant colony described
hereafter. But, except in special cases such as these, no mechanism is apparent by which selection can favor either single
genes or gene quantities in the way kin-selection theory requires. Selection does increase the quantities of advantageous
genes in a population, but this does not mean that individuals
act to "maximize representation of their genes in the next generation." They act to maximize successful offspring-individuals-in continuing, adaptable lineages. Increase of gene quantities is the result of this process; it is not selectively advantageous
in itself. This is conventional Darwinian theory, and if it is correct (as I think it is), the gene-quantity theory of kin selection
is unrealistic.
It follows that the current theory ofinclusive fitness (1), which
is that the fitness of an individual is determined by the sum of
genes carried by itself and its kin, is unrealistic too-mathematically elegant but with no basis in reality-although I do not
like to think what might happen to a Ph. D. candidate who tried
to tell his genetics professor so!
The second question is, does selection favor transmitting
identical genes? This is a question that kin-selection theorists
usually do not ask, much less answer. It was asked me by a group
of nonprofessional naturalists, who asked why, ifselection favors
gene identity in offspring, most plants and animals outcross, so
that the genes of their offspring are not identical but diversified?
This is a deadly question for the genetic theory of kin selection.
The conventional Darwinian answer is that gene diversity is
selectively advantageous because it promotes individual variability and population adaptability. Do individual plants and
animals expend energy and take risks to increase gene diversity
in their offspring, by outcrossing, and at the same time expend
energy and take risks to reduce gene diversity, by altruism to
kin? And why should selection favor genes simply because they
are identical? Identical genes may not be selectively advantageous; the genes of an average individual in a population are
presumably neither better nor worse than those of another average individual; and if an individual's genes are superior, what
is the selective advantage to the individual of presence of its
superior genes in offsprings' probable competitors? A distinction is sometimes made between genes "identical by common
descent" and other identical genes, but what is the difference
to the individuals carrying them, if the selective effect of the
genes is the same?
My conclusion is that the theories of gene-quantity kin selection and inclusive fitness are based on erroneous assumptions
and should be abandoned. What, then, are alternative explanations of the evolutions of insect and human societies?
Insect Societies. We see something that looks like genetic
kin selection in aculeate (stinging) Hymenoptera. Sex determination in Hymenoptera is haploid/diploid, haploid (unfertilized) eggs producing males, diploid (fertilized) eggs producing females; all the sperms that a female receives from one male
are genetically identical, and her daughters are then half-identical-twin sisters; and societies based on sister altruism have
evolved about a dozen times in these insects-separately in
ants, wasps, and bees, and repeatedly in some of these groups
(8). This is usually supposed to be cause and effect, the exceptionally close genetic relatedness of sisters predisposing them
to evolve altruistic-social behaviors by kin selection. But some
entomologists, including Evans (9), who have studied social
Hymenoptera think that factors other than kinship may explain
Proc. Natl. Acad. Sci. USA 78 (1981)
4441
the insects' predisposition to sociality, and I can suggest one:
ability to sting. The situation is comparable to that in Mullerian
mimicry, in which distasteful species evolve similarities so that
a taste of any one protects all against a predator. Among solitary
aculeates, each individual must sting for itself and risk its life
in doing so. (The risk lies in the predator's attack; the act of stinging is itself fatal only to some bees.) But if individuals stay together, any one can sting for all. This gives a strong selective
advantage to staying together, and anything that keeps individuals together may favor evolution of reciprocal altruistic behaviors. Possession of the sting is only part of the advantage. Aculeate Hymenoptera have narrow-waisted, flexible bodies that
allow them to aim the sting effectively; their mandibulate
mouths allow them to manipulate objects (ref. 8, p. 328); and
the power offlight ofprimitive social aculeates probably allowed
them to use the resources of extended areas while living together. Note that stinging is not primarily altruistic; the stinger
protects itself as well as its associates. The individuals that sting
are determined by chance, by which happen to meet predators
or competitors, which is to say by a lottery. And the advantage
is reciprocal, not dependent on kinship, although close kin are
often involved. Not all social Hymenoptera sting now; some
have evolved other means of defense; but the primitive ones
evidently did and still do. And not all can fly now; flightless
worker ants have evolved other means of utilizing resources in
smaller areas but perhaps more efficiently.
The stinging hypothesis is only one possible alternative to kin
selection in evolution of sociality in Hymenoptera. There may
be others. Haploid/diploid sex determination may have played
a part too, not by kin selection, but in ways suggested by Snell
(10) almost half a century ago. It allows deleterious recessive
alleles to be eliminated promptly and cheaply. (Why does it not
occur more widely in other animals?) And it favors mutual recognition and cooperation of colony mates, because a mutant
gene may be immediately shared by all the workers in a colony.
In termites, which do not sting, and in which sex determination is not haploid/diploid, what kept individuals together
and initiated their social evolution is thought to have been their
dependence on symbiotic cellulose-digesting microorganisms
transmitted by "anal feeding" (ref. 11, p. 18). Individuals had
to stay together to obtain symbionts from each other after molting, and offspring had to stay with their parents to obtain symbionts, and social behaviors then evolved. But symbiont transmission was not primarily altruistic; all individuals gained by
the presence of other individuals; the advantage was reciprocal.
The Ant Colony. Closer analysis of a simple ant colony is instructive. The colony may consist of one fertilized queen, who
does all the reproducing, and (say) 99 sterile female workers
irrevocably committed to caring for the queen, who is their
mother, and for her offspring, who are their sisters and brothers.
This is all that most observers see, and it looks like a clear case
of one-way kin altruism, the workers neither receiving nor expecting any return for their self-sacrifice. But we know now (and
might have predicted) that whether a female becomes a queen
or a worker is not determined by her genes but by a lottery, by
what food and care she happens to get as a larva (11). In the
simple ant colony just described, each individual female begins
with one chance in a hundred to become a reproducing queen
rather than a worker. Of course this is oversimplified. New
queens do not reproduce in their natal colonies but later, in
colonies they found themselves, and many queens fail to found
colonies. But these complications do not change the fact that,
as an egg, each female has a chance to be a queen rather than
a worker, and that the outcome is determined by a lottery that
each female has a chance to win. The workers' altruism therefore
contributes to the reproductive success of queens who might
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Evolution:
Darlington
have been themselves. The queen carries genes that, although
not expressed in herself, determine the supporting behaviors
of her daughter workers. This system is like that in a multicellular organism, in which the fertilized germ cell carries genes
that, although not expressed in the germ itself, determine the
supporting behaviors of the somatic daughter cells. In these
systems, individual queen ants and individual germ cells are
selected according to the support their genes can command, by
ordinary Darwinian selection, with no need of the devious and
improbable mechanism of "kin selection."
Human Societies. We see kin altruism in humans too, both
from parents to offspring and among collateral kin. These two
cases differ in an essential way, and Dawkins (3, 12) was mistaken not to distinguish them. The difference is that some degree of parental altruism-at least the expenditure of energy
required for reproduction-is essential to continuity of lineages
and must be maintained by ordinary Darwinian selection,
whereas this is not true of altruism among collateral kin. Kinselection theorists interpret altruism among human sibs and
more distant kin as due to genetic kin selection. But anthropologists (e.g., ref. 13) find that the relationship between altruism and kinship is not precise in primitive societies, and we
see that altruism among people is not metered out in proportion
to kinship, but excludes incompatible kin (history provides
many examples) and includes unrelated friends and sometimes
strangers. What we see does not fit the predictions of kin-selection theory, but looks more like reciprocal-responsive altruism (ref. 6, pp. 149-150) in which offers of altruism are made
good only if responded to, and which form net-gain lotteries in
which all compatible individuals gain or (unconsciously) expect
to gain more than their altruism costs. Kin are often included
in the lotteries but are not uniquely favored. This pattern of
behavior may reflect social rather than genetic pressures. If it
is genetic, the altruist may say (in effect), not "I help you because
you have my genes," but "Our genes make us respond to each
other and help each other for our own and our offsprings' sakes. "
This is genetically determined altruism, but not genetic kin selection. In it, altruism is reciprocally advantageous; fitness is
measured by number of successful offspring, as it should be; the
unrealistic concept of inclusive fitness is dispensed with; and
altruistic behaviors evolve by ordinary Darwinian selection because they are selectively advantageous to individuals, all of
whom are statistically more likely to gain than lose by the altruistic transactions.
Our prehuman ancestors, incidentally, may first have been
kept together by the advantages of living in groups-selectively
advantageous to all individuals in finding food and in defenseand later by the additional advantages of social transmission of
primitive technologies (transmitted by imitation) and information and ideas (transmitted by language).
An important principle emerges from comparison of these
cases. Evolution of societies seems usually to have involved two
steps. First, something made staying together advantageousfor
individuals, so that genes that kept individuals together were
established by individual selection. And then reciprocally advantageous behaviors evolved, also by individual selection, in
which altruism was not a one-way sacrifice but part of net-gain
lotteries in which all individuals gained or expected (were statistically likely) to gain more than their altruism cost. The (hypothetical) factors that first made staying together advantageous
were different in different cases: in social Hymenoptera, defensive-aggressive behavior; in termites, transmission of cellulose-digesting symbionts; and in prehumans, transmission of
technologies, information, and ideas by imitation and language,
although the reciprocal advantages of defensive-aggressive behavior may have helped keep prehumans together too.
Proc. Natl. Acad. Sci. USA 78 (1981)
A secondary factor reduces the probability of kin selection:
the cost of selection (ref. 6, pp. 113-117 and pages indexed).
Natural selection can operate only by elimination. One allele
substitution may cost the elimination of many times the number
of individuals in one generation of a population (14). One adaptation may require many allele substitutions. And in real populations thousands of structures, functions, and behaviors are
under selection; each selective process is costly, and they affect
each other in ways that increase costs, partly by the Red Queen
effect (ref. 15, pp. 17 and following and note 32); the populations
themselves and their environments continually change in ways
that change selective forces; and populations cannot pay the
cumulative costs. So, most organisms most of the time are probably far from perfectly adapted to their environments, but are
just a little better than their competitors, for the time being.
Specifically, cost would be expected to limit the evolution of
complex, genetically determined kin-recognition and kin-preference behaviors in situations in which many selective processes are going on together in populations and environments
that have changed as complexly and as rapidly as they have in
human populations in the last few thousand or few hundred
generations.
For example, reciprocal-responsive altruism is simpler than
kin selection, but its precision too would be expected to be limited by the cost of its evolution by selection. Much human behavior does seem to conform to a general pattern ofaltruism and
response, but both the offers of altruism and the responses are
far from consistent or precise.
CONCLUSIONS
The altruistic-gene theory of kin selection is improbable, and
the gene-quantity theory, and also the theory of inclusive fitness, are based on erroneous assumptions. Supposed examples
are better explained as results ofindividual selection. Until and
unless kin-selection theorists can produce unequivocal cases
and can answer criticisms satisfactorily, students ofbehavior and
especially of human behavior are wise to discount the theory.
More broadly, we should discount the theories of any evolutionists who do not define selection, or who define it as differential reproduction or change of gene ratios, without recognizing that natural selection acts by elimination, and that its cost
limits what evolution can do. Theoretical-mathematical models
of evolution that assume "maximization" or precision of adaptations are likely to be wrong because they ignore the cost of
selection, and this is especially true of sociobiology models that
assume that selection has determined details of human behavior. Much current evolutionary mathematics and determinist
sociobiology may be not just a little wrong, but dangerously
unrelated to reality.
Postscript. Dawkins (12) lists "twelve misunderstandings of
kin selection." Some are inconsequential, but others seem to
me to be valid criticisms which Dawkins does not answer satisfactorily, and which I repeat in my present paper.
Finally, I should ask more bluntly a question, implied in
preceding pages, which proponents of theories of kin selection
and inclusive fitness should be required to answer. What
good-what selective advantage-is it to an individual to have
its genes represented in other individuals which, in any ordinary population, will be competitors?
I thank Edward 0. Wilson and Howard E. Evans for reading my
manuscript and for useful criticism, but they are not responsible for my
conclusions.
1. Hamilton, W. D. (1964)1. Theor. Biol. 7, 1-52.
2. Wilson, E. 0. (1975) Sociobiology (Harvard Univ., Cambridge,
MA).
Evolution: Darlington
3. Dawkins, R. (1976) The Selfish Gene (Oxford, New York).
4. Haldane, J. B. S. (1955) New Biology 18, 34-51.
5. Boorman, S. A. & Levitt, P. R. (1980) The Genetics of Altruism
(Academic, New York).
6. Darlington, P. J., Jr. (1980) Evolutionfor Naturalists, The Simple
Principles and Complex Reality (Wiley, New York).
7. Hull, D. R. (1980) Annu. Rev. Ecol. Syst. 11, 311-332.
8. Wilson, E. 0. (1971) The Insect Societies (Harvard Univ., Cambridge, MA).
Proc. Natl. Acad. Sci. USA 78 (1981)
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9. Evans, H. E. (1977) BioScience 27, 613-617.
10. Snell, G. D. (1932) Am. Nat. 66, 381-384.
11. Oster, G. F. & Wilson, E. 0. (1978) Caste and Ecology in the
Social Insects (Princeton Univ., Princeton, NJ).
12. Dawkins, R. (1979) Z. Tierpsychol. 51, 184-200.
13. Sahlins, M. (1976) The Use and Abuse of Biology (Univ. of Michigan, Ann Arbor, MI).
14. Haldane, J. B. S. (1957)J. Genet. 55, 511-524.
15. Van Valen, L. (1973) Evol. Theory 1, 1-30.