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Behavioral Ecology Vol. 12 No. 3: 261-264
© 2001 International Society for Behavioral Ecology
Hamilton Symposium |
W. D. Hamilton and the evolution of sociality
Department of Ecology and Evolutionary Biology, Rice University, PO Box 1892, Houston, TX 77251-1892, USA
Address correspondence to D.C. Queller. E-mail: queller{at}rice.edu .
Bill Hamilton was always at his best in small groups, and I would like to open and close my reflections with some thoughts generated by two small scientific meetings that Bill Hamilton attended. I was not present at the first meeting, in Tvarminne, Finland, but a photograph from the meeting made an impression on me. In the foreground stood Pekka Pamilo, the organizer of the meeting, with a rather worried expression on his face. In the background was Bill Hamilton, skating across the ice. Bill had brought his ice skates, intent on taking every advantage of this visit to the north. It turned out, however, that the ice was quite thin, so the organizers attempted to dissuade Bill. They made a general request that speakers at the meeting should please not attempt any ice skating, at least until after they had delivered their talks. Bill followed the letter of this request, but did not follow its spirit. After giving his talk, he donned his skates and set off.
This picture brought to mind all sorts of associations. How can one not remember J. B. S. Haldane's musings about being willing to rescue two drowning brothers, or eight cousins. I hope Pekka will forgive me if I try to imagine his thoughts about the possibility of Bill falling though the ice. "Well, I do not think I am related to him... On the other hand, everyone in Finland is more or less related! But then, he is not from Finland, is he? Still, we may not share many genes, but we do share a great many memes."
The other thought that comes to my mind is one that has been noted
frequently since Bill's recent death from malaria. Bill Hamilton was a risk
taker, not just in his life, but also in his science. In his work, too, he
sometimes skated on thin ice, traveling where others would not. E. O. Wilson
once used exactly this metaphor to describe a certain kind of scientist who is
always drawn to the dangerous or to the forbidden: "They are the taboo
breakers who enjoy the whiff of grapeshot and the crackle of thin ice"
(Wilson, 1978
: 283). When Bill
skated on thin ice in Finland, the results were satisfactory: the ice may have
crackled but it did not give way. When he skated on thin scientific ice, the
results were usually not just satisfactory, but glorious.
Bill Hamilton's most glorious ideas were kin selection and inclusive
fitness. Talking about Hamilton's contributions to inclusive fitness is a bit
like talking about Isaac Newton's contributions to dynamics or Charles
Darwin's contributions to natural selection. He invented the idea, and he
developed most of its important implications. There were some forerunners, as
there always are in science. I think of Hamilton's contribution as a fusing of
two traditions. First, there was population genetics. Hamilton didn't
completely invent the idea of kin selection. The idea was foreshadowed by
Haldane (1955), Fisher
(1958), and Williams
(Williams and Williams, 1957).
However, none of them developed it in any detail, perhaps because they did not
appreciate its general importance in nature. For that we can thank animal
behaviorists, particularly those like Wynne-Edwards
(1962) and Emerson
(1960), who believed that
cooperation was very common in nature. Bill neatly hybridized the two
traditions. If cooperation and altruism were important in nature, then we
needed an explanation that was consistent with population genetics, and so
inclusive fitness was born.
Hamilton was well suited to make this match. Those acquainted with Hamilton
only through his best-known papers may think of him as a theoretician and
might conclude that he had the theoretician's superficial knowledge of the
natural world. But in fact it was his mathematical skills that were hard won,
while as a natural historian he was, well, a natural. You can see evidence of
this in many of his papers, but it comes out particularly in his lesser known
papers on insects under bark (Hamilton,
1978) and on fig wasps
(Hamilton, 1979).
So was Hamilton's contribution a simple merging of the insights of an ethologist and a population geneticist? No, it wasn't that simple, for several reasons. First, there was a lot of thin ice between these areas, and skating from one to the other was not encouraged in the early 1960s. Geneticists were leery of anything that smacked of eugenics. That included any application of population genetics to behavior. It included most of all applications to understanding social behavior, something we have always been a little touchy about. If nature was nasty, rude, or bawdy, better not to know about it, let alone let the public know. Let me illustrate the idea in an unconventional way, with a bit of verse that I call "Family Values":
Would I jump in a lakeTo save my drowning cousin?
It's not a risk I'd take
For him plus half a dozen.
But if you raise the stake
And make the prize my brother?
Now that's a deal I'll make...
If you'll just toss in another.
If this poem, and the Haldane quip it is based upon, elicit chuckles, it is in large part because they treat a topic that is uncomfortable for us. Most humor is built on discomfort of one form or another. In this case, we recognize that we make unconscious judgments akin to these, with awkward balances of self-interest and family interest, but we don't like to see ourselves as calculating self-servers. Now throw in a good dash of genetics, and the mixture becomes truly taboo. Perhaps that's why Haldane and others did not pursue the topic.
Bill's recollections of his graduate career
(Hamilton, 1996) describe the
price that he paid for his desire to be where the ice is thin. He had
difficulty finding advisors. He had no desk. He had no invitations to talk
about his work. It was not even clear that his thesis work, which would
produce some of the most heavily cited papers in evolutionary biology
(Hamilton,
1964a,b),
would be acceptable for a Ph.D. For someone who was not socially outgoing in
the first place, the effect of this isolation was severe. He feared that he
might be a crank; why else would all these manifestly smart people fail to see
the interest in what he was doing? He took to working in train stations and
public parks simply to have some minimal level of human interaction.
Mary Jane West Eberhard made a telling point in her talk about Bill at a
recent meeting (West-Eberhard,
2000). She noted that Bill's life serves as a counter-example to
those critics who said that sociobiological knowledge was dangerous. He was
proof that one can see all that is grim in the depths of our nature and still
live a life of decency and kindness. Bill would have been uncomfortable with
hagiography. His writings allude to a knowledge of the dark side of human
nature, obvious to him through introspection, so clearly his thoughts were not
always saintly. But whatever dark thoughts swirled in his mind, on the
surface—and this is where it counts—he was basically a gentle man.
Despite his highly critical mind, I never heard him criticize anyone in
anything but the kindest, most self-effacing manner. He did not judge people
by credentials and had time for people that others might consider to be
amateurs or even crackpots, George Price being a notable example. And while he
no doubt appreciated the recognition he eventually received, particularly
given his lonely days as a graduate student, he did not seem to crave
recognition excessively. Dawkins reported one example where Bill gave credit
to someone else for an idea that was really his own and had to be confronted
with the evidence from his own paper
(Dawkins, 2000). Then, as
Dawkins described it with an adverbial tour de force, Bill
"eeyorishly" admitted that, yes, he'd had the idea, but the other
fellow had put it much better.
I can give another small illustration from my own experience. In 1985 I
published a paper using Price's rule to obtain a new expression for inclusive
fitness (Queller, 1985). Alan
Grafen then chided me (Grafen,
1985), quite rightly, for having neglected to cite Hamilton's
paper using Price's rule (Hamilton,
1970). My only excuse is that Bill had read my paper in manuscript
without ever pointing out the omission, which he must have noticed. For that
matter, I had learned about Price's rule directly from Bill in seminars at the
University of Michigan. If I remembered Price's rule well and forgot Bill's
uses of it, it is partly because of the selfless way that Bill taught the
subject.
There is a another reason that Hamilton's contribution cannot be viewed as
a simple merging of naturalist and theoretical traditions. He did not just
come up with any old theoretical model. For example, one could model the
evolution of altruism for some particular limited set of conditions (George
and Doris Williams had already done this;
Williams and Williams, 1957),
but then one has to wonder how general the conclusions are. And it is also
possible, as other modelers later showed, to add so many mathematical bells
and whistles that we lose track of the general theme. In contrast, what
Hamilton came up with was a theory that was not only basically true, but also
beautiful and elegant. I'm not speaking of the mathematical derivation in his
1964 paper, which was actually rather gruesome. I'm speaking of the result,
what has come to be known as Hamilton's rule. It is so simple that even a
non-mathematical mind can easily understand it and wield it, and so general
that it can often be applied to new social evolution problems without any
fresh mathematical modeling.
How was this simple elegance achieved? I think there are two main reasons. First, Hamilton was willing to make assumptions that allowed the result to be simple without seriously compromising the biology. For example, he assumed that selection would be weak. Stronger selection has the effect of distorting the relatednesses away from their familiar values, and it makes them dependent on genetic details such as dominance. Hamilton's assumption was justified because weak selection is presumably common. For that matter, it's probably not so bad an approximation for stronger selection. A little distortion of correlation coefficients doesn't matter too much to someone interested in the real world, where estimates of parameters are typically only good to about one significant digit anyway.
The second reason inclusive fitness is so useful is its inversion of
fitness calculation methods. Instead of grouping together all effects of
others on x's fitness, it calculated all the inclusive effects of
x on others' fitnesses. This actor-centered approach is what makes
the method so easy to apply. In Hamilton's own words: "The social
behaviour of a species evolves in such a way that in each distinct
behaviour-evoking situation the individual will seem to value his neighbors'
fitness against his own according to the coefficients of relationship
appropriate to the situation"
(Hamilton, 1964b: 19).
It has become clear in recent years that the same behaviors can also often
be understood as a form of group selection—not the old group selection
of Wynne-Edwards, but nevertheless a method that involves partitioning of
selection into within-group and between-group components (see
Sober and Wilson, 1998). But
the fact remains that almost no one uses these methods much to think about and
solve interesting problems. Each of the two methods can dissect social
evolution into component parts, but where inclusive fitness divides nature
neatly at the joints, other methods seem to hack clumsily through the long
bones.
Inclusive fitness and kin selection were important on several levels.
First, of course, they provided an explanation for the evolution of altruism.
We still don't know whether Hamilton's famous haplodiploid hypothesis, based
on three-quarters relatedness (Hamilton,
1964b,
1972), explains the origin of
eusociality. But it seems certain that the answer does lie within his more
general framework of relatedness, costs, and benefits. For the study of social
insects, another result of inclusive thinking was perhaps even more
interesting. The theory did not simply explain the altruism that we already
knew about. It also predicted something we did not know much about: conflicts
within colonies. Because inclusive fitness interests often differ even among
close relatives (Hamilton,
1972), there can be conflicts over who should be queen, conflicts
over who should lay the male-destined eggs, and conflicts over sex ratios
(reviewed in Queller and Strassmann,
1998). Studies in these areas have amply satisfied the requirement
that a good theory should not just explain what is known, but also make novel
and successful predictions.
I think a parallel phenomenon occurs in the world beyond social insects.
Perhaps even more important than the explanation of altruism itself was the
general validation given to selfish gene models. If selfish genes are to be of
any value in explaining the evolution of social behavior, they simply must be
able to explain the cases where the behavior is not phenotypically selfish.
Otherwise the method must be counted as a failure. So kin-selected
explanations of altruistic behavior gave life to selfish gene explanation in
areas where kinship was not paramount. Hamilton's own work clearly shows this.
He didn't stop with altruism. He made pioneering contributions in many other
areas. The accompanying pieces in this issue describe his contributions to the
study of sexual selection and parasites, but his work also included important
contributions to senescence theory
(Hamilton, 1966), sex ratios
(Hamilton, 1967), selfish
herds (Hamilton, 1971),
dispersal (Hamilton and May,
1977), tit-for-tat cooperation
(Axelrod and Hamilton, 1981),
and within-individual conflict (Hamilton,
1967). This truly formidable list of accomplishments, and the
whole selfish gene tradition of which it is a part, emerged from a confidence
based on Hamilton's success in solving the potentially fatal problem of
altruism.
Finally, in recent years it has become increasingly clear that a theory of
altruism and cooperation is important for a much grander reason than solving
the annoying puzzle of the social insects. It is also needed to explain a much
more pervasive kind of cooperation; the evolution of the organism itself
(Maynard Smith and
Szathmáry, 1995) why do cells
cooperate in a body? Why do formerly independent bacteria evolve into
organelles? How did replicators get together in the first place? Organisms,
though they compete selfishly with each other, are themselves cooperative
entities. Cooperation is therefore fundamental to all of life.
I began with a small scientific meeting in Finland. Let me close with
another one, in Castiglioncello, Italy. The highest scientific compliment I
have ever received was one that Bill delivered there, actually to my wife and
collaborator Joan Strassmann. Bill had, many years previously, done field work
in Brazil on the troubling question of how sociality could be maintained in
wasps with many queens. We had recently helped show, with molecular tools that
had not been available to Bill, how relatedness was kept at levels consistent
with kin selection (Queller et al.,
1988,
1993;
West Eberhard, 1978). What he
said to Joan was "Now I will have to think up a different question to
ask St. Peter when I meet him." Of course, this was ridiculously
inflated praise, a reflection of Bill's generosity rather than his acumen. He
was no doubt signaling this exaggeration by his use of the religious
reference, since Bill did not seem to be a conventionally religious man.
Instead, he is some one who saw his afterlife more in terms of burying beetles
(Hamilton, 2000) than in terms
of meeting St. Peter.
Still, I'd like to run with idea for just a moment. In the sad days after Bill died, the thought of him interrogating St. Peter gave me a certain amount of solace, and perhaps even pleasure. It's not that I can imagine what Bill's question was. Nor was it the thought of him receiving a satisfactory answer. Instead, what appeals to me is the impact on old St. Peter. I imagine him at first flummoxed because he couldn't answer the question, then annoyed because he had never thought of it himself, and finally intrigued by the implications. I imagine him spending his free moments over the next few centuries thinking about it, making new observations on the teeming life below, scribbling some population genetic equations in the margins of his heavenly register, and perhaps running some simulations on God's fastest supercomputer. Perhaps I overestimate St. Peter's curiosity, but Bill's questions have always had that kind of effect. That they will long continue to do so is his legacy to us.
REFERENCES
Axelrod R, Hamilton WD, 1981. The evolution of
cooperation. Science 211:
1390-1396.
Dawkins R, 2000. Obituary for W. D. Hamilton. The Independent (London), 10 March 2000.
Emerson AE, 1960. The evolution of adaptation in population systems. In: Evolution after Darwin, vol. 1, (Tax S, ed). Chicago: University of Chicago Press; 307-348.
Fisher RA, 1958. The genetical theory of natural selection, 2nd ed. New York: Dover, 1958.
Grafen A, 1985. Hamilton's rule OK. Nature 318: 310-311.
Haldane JBS, 1955. Population genetics. New Biology 18: 34-51.
Hamilton WD, 1964a. The genetical evolution of social behaviour. I. J Theor Biol 7: 1-16.
Hamilton WD, 1964b. The genetical evolution of social behaviour. II. J Theor Biol 7: 17-52.
Hamilton WD, 1966. The moulding of senescence by natural selection. J Theor Biol 12: 12-45.[Web of Science][Medline]
Hamilton WD, 1967. Extraordinary sex ratios.
Science 156:
477-488.
Hamilton WD, 1970. Selfish and spiteful behavior in an evolutionary model. Nature 228: 1218-1220.[Medline]
Hamilton WD, 1971. Geometry for the selfish herd. J Theor Biol 31: 295-311.[Web of Science][Medline]
Hamilton WD, 1972. Altruism and related phenomena mainly in the social insects. Annu Rev Ecol Syst 3: 193-232.
Hamilton WD, 1978. Evolution and diversity under bark. In: Diversity of insect faunas. Symposia of the Royal Entomological Society of London No. 9 (Mound LA, Waloff N, eds). Oxford: Blackwell Scientific; 154-175.
Hamilton WD, 1979. Wingless and fighting males in fig wasps and other insects. In: Reproductive competition, mate choice and sexual selection in insects, (Blum MS, Blum NA, eds). New York: Academic Press; 167-220.
Hamilton WD, 1996. Narrow roads of geneland, vol. 1: The evolution of social behaviour. Oxford: W. H. Freeman.
Hamilton WD, 2000. My intended burial and why. Ethol Ecol Evol 12: 111-112.
Hamilton WD, May RM, 1977. Dispersal in stable habitats. Nature 269: 578-581.
Maynard Smith J, Szathmáry E, 1995. The major transitions in evolution. Oxford: W. H. Freeman.
Queller DC, 1985. Kinship, reciprocity and synergism in the evolution of social behaviour. Nature 318: 366-367.
Queller DC, Strassmann JE, 1998. Kin selection and social insects. Bioscience 48: 165-174.
Queller DC, Strassmann JE, Hughes CR, 1988. Genetic
relatedness in colonies of tropical wasps with multiple queens.
Science 242:
1155-1157.
Queller DC, Strassmann JE, Solís CR, Hughes CR, DeLoach DM, 1993. A selfish strategy of social insect workers that promotes social cohesion. Nature 365: 639-641.
Sober E, Wilson DS, 1998. Unto others: The evolution and psychology of unselfish behavior. Cambridge, Massachusetts: Harvard University Press.
West-Eberhard MJ, 1978. Temporary queens in
Metapolybia wasps: nonreproductive helpers without altrusim?
Science 200:
441-443.
West-Eberhard MJ, 2000. Humane sociobiology, or Hamilton's second rule. Human Behavior and Evolution meetings, Amherst College, 11 June 200.
Williams GC, Williams DC, 1957. Natural selection of individually harmful social adaptations among sibs with special reference to social insects. Evolution 11: 32-39.
Wilson EO, 1978. The attempt to suppress human behavioral genetics. J Gen Educ 29: 277-287.
Wynne-Edwards VC, 1962. Animal dispersion in relation to social behavior. Edinburgh: Oliver and Boyd.
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