The Selfish Gene (1989 edition)

Battle of the sexes

A similar battle as described between the generations arises between the sexes. Each parent has 50 genetic shareholding in a child but if one parent can get away with investing less than his or her fair share of costly resources in each child, he will be better off since he will have more to spend on other children by other sexual partners, and so propagate more of his genes. Thus, each partner tries to exploit the other and force them to invest more.

When two gametes fuse, both contribute equal numbers of genes to the new individual but the egg contributes far more in the way of food resources. Therefore, the asymmetry starts as early as conception because the mother stands to lose more if child dies than male because of this initial investment. This would mean that there is some evolutionary pressure on males to invest a little bit less in each child, and to try and have more children by different wives, if they can be sure that the wife has a reasonable chance of rearing the child on her own.

There are several options available to the female to prevent being left with the sole responsibility of the child. She could refuse to copulate. She is in demand because she supplies the large, nutritious egg and therefore a male who successfully copulates, gains a valuable food reserve for his offspring. Dawkins describes two different scenarios where "driving a hard bargain" could evolve by natural selection. The first he calls the domestic bliss strategy. This is when the female tries to spot signs of fidelity and domesticity in advance. She does this by playing hard to get for a long time so that any male who is patient enough to wait until the female consents is likely to be a good bet as a faithful husband. Courtship rituals often include considerable pre-copulation investment, such as building a nest or courtship feeding, so that the male is forced to invest so heavily before he can mate with the female so that is would no longer pay him to desert after copulation. However, this is dependent on all females playing the same game and Maynard Smith carried out a game theory test that supported the idea that coyness in the female and faithfulness in the male could be an ESS.

The second strategy Dawkins describes is the "He-man strategy". This is when the females resign themselves to getting no help from the father in rearing the children and so they go all-out for good genes, refusing to reproduce with anyone other than the best. They choose their male on evidence of ability to survive because this means that the father will be passing on genes that will benefit the survival prospects of the offspring. They may choose a mate because they have strong muscles and so can escape from predators, or they may go for sexual attractiveness which will benefit their sons when it is their time to reproduce because they will be picked by the new generation of females and consequently provide lots of grandchildren. Another theory on how females choose their mates, as proposed by Zahavi, is the Handicap principle. This is when handicaps evolve purely because they are handicaps - they indicate that the male is worthy of mating with because he can survive in spite of the handicap.

Therefore, the various different kinds of breeding systems that are found among animals can be understood in terms of conflicting interests between males and females, termed the battle of the sexes by Dawkins. Individuals of either sex "want" to maximise their total reproductive output during their lives but it is precisely this that causes the clash.

You scratch my back, I'll ride on yours

Dawkins argues that "if animals live together in groups, their genes must get more benefit out of the association than they put in." For example, Hyenas can catch a larger prey if they hunt in a pack, spiders can build a larger communal web if they work together, and fish that swim behind another fish may gain hydrodynamic advantage. More importantly, if they are in a group they are able to take more precautions from being eaten by predators, namely by staying in the middle of the pack so that there is another individual between you and any possible hiding places for the predator.

However, bird alarms appear, at first sight, to be a genuinely altruistic behaviour because it has the effect of warning others of predators while at the same time drawing the predator's attention to the caller. However, there are several possible "selfish" explanations. Firstly, there is a good chance that the flock contains some close relatives and so a gene for giving an alarm call can prosper in the gene pool because it has a food chance of being in the bodies of some of the individuals saved. Another possible explanation is that one bird has seen the predator while the rest of the flock has not. At this stage the predator has not noticed the flock and so the "spotter" could crouch low and hope not to be seen by the predator. However, this will not do much good if the rest of the flock are being conspicuous because they will attract the predators attention to the area and then every member of the flock, including the "spotter" are in danger. Therefore, from a purely selfish point of view it is in the spotter's interests to warn the rest of the flock so that they too hide from the predator.

Other animals demonstrate apparently suicidal altruism, such as the stotting Thomson's gazelle. However, even this behaviour can be explained by the selfish gene theory. Zahavi argues that the stotting is not, in fact, intended as a warning for other gazelles but instead is directed at the predator. What the gazelle is actually doing by stotting is letting the predator know that he is a fit and healthy gazelle and that the predator would be better off chasing another gazelle from the herd that is not so fit. Therefore, this behaviour is far from altruistic!

Social insects also demonstrate astonishing feats of co-operation and apparent altruism but on closer inspection, one can see that they are initiated by gene selfishness. The workers are sterile and therefore their only means of propagating their genes into the next generation is to help the queen to produce more brothers and sisters. They do this by sacrificing themselves when they attack intruders; they provide the reproductive members with food and they help care for the brood.

In some social colonies, altruism can be explained by the unusual system of sex determination which results in the relatedness between full sisters being ¾ and not ½ as it would be for normal sexual animals. Therefore, a hymenopteran female is more closely related to her full sisters than she is to her offspring of any sex and so it would be genetically beneficial for them to farm their mother as an efficient sister- making machine! Thus, worker sterility evolved because workers could use their mother as a more efficient manufacturer of copies of their own genes than they would be themselves.

Apparent reciprocal altruism has been seen to occur between members of different species as well, where relatedness cannot be used as an explanation. For example, ants "milk" aphids for the plant juice that they have stored in their abdomen and in return receive protection from their enemies. This occurs because the different species have different "skills" to offer the partnership. Aphids have the right sort of mouthparts for pumping up plant sap, but sucking mouthparts are no good for self-defence. Ants are no good at sucking sap from plants, but they are good fighters. Therefore, ant genes for cultivating and protecting aphids have been favoured in ant gene pools and similarly, aphid genes for co-operating with the ants have been favoured in aphid gene pools, thus becoming an ESS.

The exchange of favours between the ant and the aphid can be seen to take place simultaneously. But reciprocal altruism has also been seen to occur when there is a delay between the giving of the favour and its repayment. Examples include the removal of disease-infected ticks from the top of a bird's head where it is unable to remove it itself and the cleaning symbiosis between the wrasse and the grouper. This delayed reciprocal altruism can evolve in species that are capable of recognising and remembering each other as individuals. However, there is the threat of cheating because an individual can benefit from exploiting the co-operative efforts of others. If the same individuals interact over a long period of time it is possible for reciprocity to become evolutionary stable, as subsequent interactions would lead selection to discriminate against the cheater. The Prisoner's Dilemma model is used to demonstrate this and it is described in the chapter "Nice guys finish first".

Memes: the new replicators

This chapter focuses in on man in particular. Dawkins believes that there are good reasons for supposing our species is unique, namely "culture". He believes that there is such a thing as cultural transmission, analogous to the genetic transmission we have been discussing above; and it is through this cultural transmission that things such as language, fashions, ceremonies, customs, arts, and technology have evolved.

To explain this, he returns to first principles. He argues that what is true of all life, wherever it is found and whatever the basis of its chemistry is, is that "all life evolves by the differential survival of replicating entities". Up to this point in his book, he has argued that the gene, the DNA molecule, is the only replicating entity on our planet, but now he introduces the possibility of a new type of replicator that has emerged.

Using the analogy of the primeval soup of DNA molecules, he suggests that there is a new soup, the soup of human culture, and the individual units in this soup he calls memes. He believes that by making brains for their survival machines, the traditional gene-selected evolution provided this "soup" in which the first memes arose. Examples of memes are tunes, ideas, catch phrases, and clothes fashions. He argues that "just as genes propagate themselves in the gene pool by leaping from body to body via sperm or eggs, so memes propagate themselves in the meme pool by leaping from brain to brain via a process, which in the broad sense, can be called imitation".

For example, if a scientist hears or reads about a good idea, he may pass it on to his colleagues and he may mention it in his articles and lectures. If the idea catches on, it can be said to propagate itself, spreading from brain to brain. And just as with gene evolution, some memes are more successful in the meme pool than others. This will depend on the meme's longevity, fecundity and copying fidelity.

He pursues the analogy between memes and genes further by asking if it is possible to have selfish or ruthless memes? The difference here between genes and memes concerns the nature of competition, because memes do not have the equivalent to chromosomes or alleles. However, he argues that memes do have an alternative form of competition over memory storage space in the brain and time spent being attended to. If a meme is to dominate the attention of a human brain, it must do so at the expense of "rival" memes because the human brain cannot do more than one or a few things at once.

Therefore, he concludes that cultural traits have evolved because they are advantageous to themselves, and not because they are advantageous to the genes (or the individual, the group or the species). He emphasises that DNA molecules are not the only entities that can form the basis for Darwinian evolution, and that any slight inaccurate self-replicating entity can become the basis for such selection if given the right conditions and enough generations.

Nice guys finish first

Axelrod and Hamilton (1981) used game theory and the concept of an evolutionary stable strategy (ESS) to develop a model of evolution of co-operation based on reciprocity. They used the Prisoner's Dilemma game to solve the problem of achieving co-operation, mainly concentrating on the two-player version of the game which describes situations that involve the interactions between pairs of individuals. In the Prisoner's Dilemma game, two individuals can each either cooperate or defect. No matter what the other does, the selfish choice of defection yields a higher payoff than co-operation. But if both defect, both do worse than if both had co-operated. The payoff matrix of the Prisoner's Dilemma can be seen below:

Imagine player A finds another individual B who always co-operates. If A co-operates too it gets a reward of 3, whereas if it defects it gets 5. Therefore, if B co-operates, it pays A to defect. Now imagine player A discovers that B always defects. If A co-operates it gains nothing (the sucker's pay-off) whereas if it defects it gets 1. Therefore, if B defects, it pays A to defect. The conclusion is that irrespective of the other player's choice, in a one-off game it pays to defect even though with both players defecting they get less (1) than they would have got it they had both co-operated (3). In other words, co-operation is not an ESS because in a population of "all co-operators" a mutant who defected would spread. On the other hand, always defecting (ALL D) is an ESS because in a population of "all defect" a mutant co- operator does not gain an advantage.

However, this reasoning does not apply if the players interact an indefinite number of times, which is a more realistic assumption than the idea of single or finite meetings. With an indefinite number of interactions, co-operation can emerge because it is the possibility that players meet again that brings about the possibility of co-operation. Axelrod (1984) ran a computer tournament in which different strategies, submitted by scientists from all over the world, were paired against each other in a round robin tournament to determine how best to act when in a Prisoner's Dilemma situation. Some of the strategies adopted in this tournament were very complex, using procedures such as a Markov process or Bayesian inference, and others were very unforgiving. However, the winning strategy was the simplest one of them all, called "Tit for Tat". Tit for Tat is the policy of co-operating on the first move and then doing whatever the other player did on the previous move. This policy means that Tit for Tat will defect once after each defection of the other player, and thus is a strategy of co-operation based on reciprocity. In the terms of the title of this chapter, Tit for Tat can be seen to be a "nice" strategy, defined as one that is never the first to defect. Axelrod also pointed out that Tit for Tat is a forgiving strategy, defined as one that, although it may retaliate, has a short memory and so swiftly overlooks old misdeeds. Throughout several sequential rounds of the tournament, the robustness of Tit for Tat was demonstrated in that it continued to win and it was subsequently discovered that in the long run, Tit for Tat continued to do well while the less successful strategies were displaced. Therefore, Axelrod identified that two characteristics of winning strategies are niceness and forgivingness.

From this, Dawkins points out that Tit for Tat cannot be invaded by any nasty strategy and so one is tempted to conclude that it is an ESS. However, Tit for Tat can be invaded by another nice strategy such as Always Cooperate. When these two strategies meet, they will always cooperate with each other, thus looking and behaving exactly like the other. In this way, although Always Cooperate does not enjoy a positive selective advantage over Tit for Tat, it can still drift into the population with out being noticed and thus Tit for Tat is not strictly an ESS because it can be invaded by other nice strategies. Therefore, Axelrod coined the phrase "collectively stable" to describe it.

Furthermore, as in the case of true ESSs, it is possible for more than one strategy to be collectively stable at the same time and this is true of the Prisoner's Dilemma as well. Always Defect is also stable if it has already become established because no other strategy invading can do better against it. Therefore, Dawkins suggests that we treat the system as being bistable, with Always Defect being one of the stable points and Tit for Tat (or some mixture of mostly nice, retaliatory strategies) as the other. Which stable point comes to dominate the population will depend on mechanisms such as genetic kinship and clustering. Genetic kinship could be responsible for initiation of co-operation from a previously asocial state because animals of most species are likely to find themselves living close to their sisters, brothers and cousins, rather than to random members of the population. In this way, the chances of the individuals that live near you containing the same gene for Tit for Tat tendencies as you do are good and so you will all tend to benefit from mutual co-operation.

The other possible mechanism that allows reciprocal co-operation to gain a foothold in a population that is presently using ALL D is clustering. This is when mutant strategies arrive in a cluster of individuals all using the same strategy so that they form a nontrivial proportion of the interactions. For example, if Tit for Tat individuals occur in clusters then they can interact with each other more than expected from random encounters in the population at large, and hence enjoy the increased benefits of mutual co- operation. In this way, they will be able to become established as a more successful strategy and will soon reach fixation. Therefore, unrelated individuals are seen to cooperate with each other is they have a sufficiently high probability of meeting again so that they have a stake in their future interaction.

Dawkins summaries by saying that the success of non-envious, forgiving niceness (as a behaviour) depends on three factors:

1. that nature should set up circumstances that fit these games of Prisoner's Dilemmas
2. that the shadow of the future is long (by which he means that neither "player" should know when the game is going to end)
3. that the games should be nonzero sum games (by which he means that both players can "win" if they cooperate i.e. a win for one player does not automatically mean a loss for the other).

Indeed, he points out that these conditions are commonly met around the living kingdoms and consequently the cooperative behaviour evolves.

The long reach of the gene

Throughout the entire book, Dawkins has argued that evolution in terms of selection occurs at the level of the gene and not at the level of the individual. However, this theory has always faced resistance from those who insist on asking questions about organisms, why organisms do this, why organisms do that and why organisms group themselves into societies. What Dawkins believes is that we should in fact ask why living matter (the replicators) groups itself into organisms in the first place. He asks: "Why isn't the sea still a primordial battleground of free and independent replicators? Why did the ancient replicators club together to make, and reside in, lumbering robots, and why are those robots - individual bodies - you and me - so large and so complicated?"

Dawkins understands that many biologists find it hard to see that there is a question here at all because individuals have now evolved into a form so large and coherently purposeful. However, in this final chapter, he attempts to briefly answer these questions (although he says his detailed explanation can be found in The Extended Phenotype). He reminds us that what is important is for the replicator to survive and propagate itself into the next generation. However, now he introduces the idea that replicators survive, not only by the quality of their intrinsic properties, but also by the quality of their consequences on the world. By this he means that genes have tools that extend outside the individual body wall which can be use to manipulate other individuals for their benefit.

Using several examples from nature, including snails and flukes, the microscopic protozoan parasite called Nosema and flour beetles, and crabs and Sacculina, Dawkins describes how one individual can influence the behaviour of the other to their advantage. This influence may be of benefit or cost to the host, depending on whether the host and the parasite "want the same thing". It has been suggested that the host will benefit from the presence of the parasite if the parasite's genes are to be transmitted to future generations via the same vehicle as the host's genes. If this is not the case, one would expect the parasite to damage the host in one way or another. For example, the Sacculina effectively castrates the crab so that the crab diverts the energy and resources, that would otherwise have gone towards reproduction, into its own body which the Sacculina then sucks out for its own nourishment. However, there are cases when both individuals "share" the same vehicles to propagate their genes into the next generation. One example of this is when the wood-boring ambrosia beetle is parasitised by bacteria that not only lives in the host's body, but also uses the host's eggs as their transport into a new host. In this case, the bacteria does more than simply cooperate with the beetle and in fact play an essential role in "pricking the unfertilised egg into action, provoking them to develop into male beetles.

Dawkins takes this idea and argues that parasites such as these will cease to be parasitic and become mutualistic, with the two bodies ultimately merging into the "host" body completely. He then applies this theory to human genes. From above, we have already established that individuals will cooperate if they share the same impartial exit channel into the future. He follows this through to argue that our own genes cooperate with one another purely for this reason - that they share the same outlet, and that the individual genes have ceased to be parasitic and have become mutualistic, giving the appearance of a coherent "whole".

He uses this theory to finish his book by asking three questions. Why did genes gang up in cells? Why did cells gang up in many-celled bodies? And why did bodies adopt what he calls a "bottlenecked" life style?

He answers the first question by using an analogy of a pharmaceutical factory. The synthesis of a useful chemical needs a production line because the starting chemical cannot be transformed into the desired end-product without a series of intermediates arranged in a strict sequence. In the same way, single enzymes (made by one gene) cannot achieve the synthesis of a useful by-product without the "help" of intermediates and so the enzymes (or genes) will have had to cooperate with each other in order to achieve their goal. This will have started as elementary co-operation between the replicators in the primeval soup, but eventually a cell wall will probably have formed in order to keep the useful chemical together and prevent them leaking away. And this is how cells came together.

The second question is just as simple for the selfish gene theory to explain. Each cell will benefit from co-operating with other cells because this will mean that each cell will be able to specialise and therefore become more efficient at performing its particular task, while at the same time taking advantage form the efficiency of the other specialists. In economics, this principle is called Economies of Scale.

And thirdly, why do bodies participate in a "bottlenecked" life cycle? By bottlenecked, Dawkins means that "no matter how many cells, of no matter how many specialised types, cooperate to perform the unimaginably complicated task of running an adult body, the efforts of all those cells converge on the final goal of producing single cells again - sperms and eggs." He argues three reasons why this occurs: "back to the drawing board", "orderly timing" and "cellular uniformity". All these three mechanisms benefit the vehicles in evolution and additionally result in the vehicles becoming more discrete and vehicle like, to the extent that biologist often believe that the organisms use the DNA to reproduce themselves, in much the same way as they use an eye to see, which in fact is the truth turned upside-down!