William Hamilton is widely acknowledged as one of the most important theoretical biologists of the 20th century. In 1964, at the age of 27, he published The Genetical Evolution of Social Behaviour. For several years it was the most cited paper in the Journal of Theoretical Biology ever, and this may still be so. Hamilton died in 2000 after contracting malaria in Africa. The following interview took place at the University of Oxford, December 1996.
Some of your ideas were foreshadowed by Sir Ronald Fisher's explanation, in the thirties, of the distastefulness of some insects. In what way?
Fisher saw there was a difficulty about the evolution of distastefulness in insects, as also in the further matter of the insects becoming brightly coloured in order to advertise their distastefulness. He realized that if the insect is actually eaten by the predator in the course of learning to avoid them, then whatever made that insect conspicuous to the predator is obviously disadvantageous. So he reasoned that the only way in which you could see that kind of selection getting started would be if firstly, the insects were gregarious, secondly, the group was a group of siblings, and thirdly, having tasted one and found it awful, the predator would then leave the rest of the group alone. The genes of the one eaten would then be promoted. Fisher also realised that this was not such a strong form of selection, not as if it were the individual itself that had a form of protection. He made some remark about the selection going ahead at half the speed than it would have if it were direct selection. And that was one key early statement of the selection principle concerning the closeness of relatedness that I later came to develop.
You describe in part two of your 1964 article the post-reproductive behaviour of two kinds of moths. What was the general phenomenon being illustrated?
I noticed that someone had written about the post-reproductive spans of two kinds of moths, one kind being cryptic, and the other kind warningly coloured as in the case we have just discussed. The author had noticed that the cryptic insect tended to die very soon after it had laid its eggs, whereas the warningly coloured ones often have a long life after they had laid their eggs. Again this could be interpreted in terms of the kinship principle in a rather neat way. In case of the cryptic one, if there are any relatives around in the neighbourhood at all, it is advantageous for the moth to give up its life as soon as it finished its own main business, laying its eggs. Because if it is around and the predator detects the moth and eats it, then that is a step in the predator learning to detect other moths, perhaps including those which have not yet laid their eggs. So by causing itself to die soon after it has laid its eggs, it is actually doing a service to its cousins which are in the neighbourhood. Quite the contrary holds for the warningly coloured one. Once it has laid its eggs, it is in a position freely to use its warning-colours to warn everyone it can. So it should continue to live and wait, actually expose itself to being tasted by the predator, because that would be a step in teaching the predator to avoid its relatives. It was gratifying that all this theory fitted very well with the findings.
In moths both sexes have wings, but in some other insects either the males or the females are wingless. Why?
Gene dispersal is a very crucial evolutionary phenomenon, because where you are, your descendants almost certainly will have to die out. So there has to be a continual search for other places to colonise. And therefore for a female to sacrifice wings without having some other way of dispersal for her offspring would be a deadly mistake sooner or later. In fact we find that in all the cases where females have become wingless, there is some other way in which they or their offspring are dispersed to other localities. Most commonly they have a young stage, a larva, which is very mobile. Either it may climb onto other insects, or onto a twig and from there be dispersed by wind. Often such larvae have long hairs which enable them to balloon on the wind very satisfactorily. In some species the wingless female is carried by the winged male, -in his arms almost literally. During this flight-time he is mating her, and finally he drops her off in a place suitable for egg laying.
As to the males becoming wingless, if the male can inseminate a female who is mobile herself, then he doesn't have to worry about wings too much, because his genes can be carried off by the female. This often happens in cases where wingless males mate their close relatives. So I think we can find some sort of a rationale for many particular cases; but as far as I know there is no very sweeping theory that explains why in some groups there is male winglessness, and in others female winglessness.
You went to Brazil in 1975 to study the fig-wasp, where the males don't have wings, and often also don't have a mouth.
I didn't actually go to Brazil to study them, I went to study life in rotting wood, but I ended up studying fig-wasps because the rotting wood was dry and not in good condition. The fig is a little world in itself. In some species of fig-wasps the males indeed have no mouth; these are entirely fighting and mating machines, a very strange kind of an animal with a very short life as an adult and mating as quickly as possible, and fighting lethally whenever rivals intrude and compete.
Before going to Brazil I had known there was something very special for my theorising about fig wasps. I knew how they participate in this incredible symbiotic pollination system in the fig-trees. In adapting to living inside the fig-fruit they developed various marvellous adaptations, including completely wingless males with very specialized habits, and with exactly the biased sex-ratio's which my theory predicted they should have.
Why should they have biased sex-ratio's?
Well, it is a case where the males are in a unique confining situation inside the fig. They hatch out as adults from the gall flowers, and the easiest -indeed the only- females to mate are the females who are also hatching inside the same fig. So they do so. Theory says that if males mate with their sisters, and their sisters are capable of storing sperm, then you must expect the proportion of males to be cut down drastically. It is adaptive because a female mother who programs her eggs to become either males or females, should do much better if she produces a lot of females, and just enough males to fertilize them. In that way she would get more descendants. That bias is very nicely illustrated in what happens in figs. Other people that followed and tested my reasoning further have shown that it is illustrated with an accuracy that I would never have dared myself to expect. So this became a really strong and well-upheld prediction out of evolutionary theory.
Why do males sometimes engage in lethal fighting with other males, while at other times they tend to bluff?
For some species of fig-wasps there is not much point in bluffing inside the fig, because there is no time to 'live and fight another day' if they accept a bluff. Everything is over in a few hours, and if you don't fight now and try to win, then you won't be given another chance.
I think I saw bluffing with the giant Chilean stag beetle, where I did find that in all the tournaments that I held between males, inducing them to fight one another in the presence of a female, it always turned out to be the second largest one who was the overall victor. This suggests rather that those with the biggest 'tongs' were not actually as strong as they seemed to be. And they live in a situation where I can imagine that bluffing would pay off. Stag beetles are quite long-lived, and there are many flowers on the trees they could visit where females are arriving and so it might be worthwhile to pretend that you are bigger than you are, in the hope that a male will accept that you are stronger and go away to other flowers. Then you could win the local contest; bluff would have paid.
You use a lot of mathematics in your work, and you write (Narrow Roads of Gene Land I, 1995: 230): "I had realized from experience that university people sometimes don't react well to common sense and in any case most of them listen to it harder if you first intimidate them with equations."
Equations seem to frighten a lot of people; if you come at them with an display of mathematical strength then they often back off. With me you might call it a kind of bluff. A nice anecdote about people's fear of mathematics occurs to me. There was an IRA bomb discovered in this town, which had never actually been fired, and yet had not been found either for about a year. Can you guess where it was planted? The person put it behind the calculus books in one of the major bookshops of Oxford! I guess he choose calculus-books because he reckoned that those would be the ones least often be pulled off the shelves. This perhaps illustrates the general fear of mathematics, but I guess another interpretation might be that, second to Brits in Northern Ireland, the bomber just hated maths!
Is there not a risk that someone writes an article filled with equations but without ideas, and it is accepted as science just because it looks so scientific?
That's exactly it. A lot of work does get by, by having an aura of mathematics about it. Whether it is serious and necessary or not, it certainly impresses people. You can find biologists who are very hot on this issue, like my old colleague Richard Alexander. He doesn't like mathematics in evolutionary theory, he says you can have all the same thoughts without it. So these biologists would call it bluff, and I think very largely they are right. If you have a simple idea, state it simply, and forget about the mathematics.
Nevertheless, you use mathematics.....
I use it. Often I use mathematics because I needed to straighten out my own ideas. I have a somewhat illogical brain, and unless I put it through the mill of mathematics, I can continue to believe in the impossible for a long time. But eventually, either by mathematical argument or by computer-simulation I suddenly realise that something I thought followed in fact does not follow, and I abandon that and come to see the truth. Sometimes that math goes into the paper in order to convince other people.
And then there is DNA, chromosomes, genes, etcetera. This can be quite intimidating to social scientists. Do you need to know a lot about genetics and math to understand evolutionary theory?
I do think you do need to know the basics of genetics. I am not sure you need to know a tremendous amount about modern molecular genetics. I always found that good old standard Mendelism serves me quite well, and the modern ideas have not really changed the picture very much. I also think in the mathematical field you just have to know something about probability theory, to understand how genes work in evolutionary processes, and so fundamentals of probability and statistics are just about essential in understanding modern Darwinism.
A general question. Do living organisms behave as if they want to pass on their own genes, or do they behave as if each of their genes is trying to replicate itself, possibly at the expense of other genes of the same genome?
This is a very deep and difficult question I think. One's impression is that there is a conflict between selfish genes, but largely it is being over-ridden by a kind of democracy that has arisen in the genome. It combines to suppress this intergene conflict and the outcome is that the organism acts largely as a whole.
You write that evolutionary ideas "turn out to have, or are perceived to have, the unfortunate property of being solvents of a vital societal glue". What kind of glue is this?
The glue that I am thinking of is various myths that tend to hold societies together. When these myths are wrong, I think that they exist because they have helped people to be more cooperative than they would be if proceeding with a full understanding of evolutionary theory. This is the most unfortunate fact about teaching evolution. I also think that it is the threat that is dimly perceived by all religious people. They think that if people 'believe' evolution instead of believing, say, the gospels, they will no longer be able to celebrate simple honesty, or kindly and warm feelings toward others, as unequivocally 'good'.
I think they exaggerate the danger, but they don't exaggerate a nothing. There is a danger of that kind.
How are evolutionists trying to deal with this problem?
They are trying to deal with it by showing that the implications of a fully rational and evolutionary theory of behaviour, and that includes human behaviour, is not such a nasty thing as it may seem at first. If you believe that we evolved out of animals, -are animals-, and have the same kinds of drives, it doesn't mean that we have to be selfish and inhumane. When you fully work out the consequences of the rules of kinship and of reciprocation, and ensure maintenance of the standards implied, you will see that the outcome is in fact quite a moderate kind of behaviour, avoiding evil and as good in holding the society together as are the religious myths. Indeed, under a rational theory we should be able to do better for human happiness by avoiding various naive errors.
You write that long ago there was a man who claimed that humans descended from bears, and not from apes. As his theory got rejected and the man got more and more isolated, he probably looked like an angry bear. Didn't this description for a long time fit sociobiologists? "The world doesn't understand us and doesn't like us"?
I guess it fits anyone who feels himself to be very isolated, so I guess and hope we have gone recently from being angry bears to being rather comfortable and accepted bears. I wish I could remember who it was that founded this ridiculous theory about bears. I am sure that it exists, but I have not managed to recall the book. Perhaps one of your readers can help to remind me.