The Extended Phenotype

by Richard Dawkins

  This chapter is intended to begin the process of undermining the reader’s confidence in the central theorem of the selfish organism. That theorem states that individual animals are expected to work for the good of their own inclusive fitness, for the good of copies of their own genes. The chapter has shown that animals are quite likely to work hard and vigorously for the good of some other individual’s genes, and to the detriment of their own. This is not necessarily just a temporary departure from the central theorem, a brief interlude of manipulative exploitation before counterselection on the victim lineage redresses the balance. I have suggested that fundamental asymmetries such as the life/dinner principle, and the rare-enemy effect, will see to it that many arms races reach a stable state in which animals on one side permanently work for the benefit of animals on the other side, and to their own detriment; work hard, energetically, wantonly against their own genetic interests. When we see the members of a species consistently behaving in a certain way, ‘anting’ in birds or whatever it is, we are apt to scratch our heads and wonder how the behaviour benefits the animals’ inclusive fitness. How does it benefit a bird to allow ants to run all through its feathers? Is it using the ants to clean it of parasites, or what? The conclusion of this chapter is that we might instead ask whose inclusive fitness the behaviour is benefiting! Is it the animal’s own, or that of some manipulator lurking behind the scenes? In the case of ‘anting’ it does seem reasonable to speculate about advantages to the bird, but perhaps we should give at least a sideways glance at the possibility that it is an adaptation for the good of the ants!

  5 The Active Germ-line Replicator

  In 1957, Benzer argued that ‘the gene’ could no longer continue as a single, unitary concept. He split it into three: the muton was the minimum unit of mutational change; the recon was the minimum unit of recombination; and the cistron was defined in a way that was directly applicable only to microorganisms, but it was effectively equivalent to the unit responsible for synthesizing one polypeptide chain. I have suggested adding a fourth unit, the optimon, the unit of natural selection (Dawkins 1978b). Independently, E. Mayr (personal communication) coined the term ‘selecton’ to serve the same purpose. The optimon (or selecton) is the ‘something’ to which we refer when we speak of an adaptation as being ‘for the good of’ something. The question is, what is that something; what is the optimon?

  The question of what is the ‘unit of selection’ has been debated from time to time in the literature both of biology (Wynne-Edwards 1962; Williams 1966; Lewontin 1970a; Leigh 1977; Dawkins 1978a; Alexander & Borgia 1978; Wright 1980) and of philosophy (Hull 1980a,b; Wimsatt in preparation). At first sight it seems a rather uselessly theological argument. Hull, indeed, explicitly regards it as ‘metaphysical’ (though none the worse for that). I must justify my interest in it. Why does it matter what we consider to be the unit of selection? There are various reasons, but I shall give only one. I agree with Williams (1966), Curio (1973) and others that there is a need to develop a serious science of adaptation—teleonomy as Pittendrigh (1958) called it. The central theoretical problem of teleonomy will be that of the nature of the entity for whose benefit adaptations may be said to exist. Are they for the benefit of the individual organism, for the benefit of the group or species of which it is a member, or for the benefit of some smaller unit inside the individual organism? As already emphasized in Chapter 3, this really matters. Adaptations for the good of a group will look quite different from adaptations for the good of an individual.

  Gould (1977b) sets out what, at first sight, appears to be the issue:

  The identification of individuals as the unit of selection is a central theme in Darwin’s thought … Individuals are the unit of selection; the ‘struggle for existence’ is a matter among individuals … In the last fifteen years challenges to Darwin’s focus on individuals have come from above and from below. From above, Scottish biologist V. C. Wynne-Edwards raised orthodox hackles fifteen years ago by arguing that groups, not individuals, are units of selection, at least for the evolution of social behaviour. From below, English biologist Richard Dawkins has recently raised my hackles with his claim that genes themselves are units of selection, and individuals merely their temporary receptacles.

  Gould is invoking the idea of a hierarchy of levels in the organization of life. He sees himself as perched on an intermediate rung of a ladder, with group selectionists above and gene selectionists below. The present chapter and the next will show that this kind of analysis is false. There is, of course, a hierarchy of levels of biological organization (see next chapter), but Gould is applying it incorrectly. The conventional dispute between group selection and individual selection is different in category from the apparent dispute between individual selection and gene selection. It is wrong to think of the three as arranged on a single-dimensional ladder, such that words like ‘above’ and ‘below’ have transitive meaning. I shall show that the well-aired dispute between group and individual is concerned with what I shall call ‘vehicle selection’ and can be regarded as a factual biological dispute about units of natural selection. The attack ‘from below’, on the other hand, is really an argument about what we ought to mean when we talk about a unit of natural selection.

  To anticipate the conclusion of these two chapters, there are two ways in which we can characterize natural selection. Both are correct; they simply focus on different aspects of the same process. Evolution is the external and visible manifestation of the differential survival of alternative replicators (Dawkins 1978a). Genes are replicators; organisms and groups of organisms are best not regarded as replicators; they are vehicles in which replicators travel about. Replicator selection is the process by which some replicators survive at the expense of other replicators. Vehicle selection is the process by which some vehicles are more successful than other vehicles in ensuring the survival of their replicators. The controversy about group selection versus individual selection is a controversy about the rival claims of two suggested kinds of vehicle. The controversy about gene selection versus individual (or group) selection is a controversy about whether, when we talk about a unit of selection, we ought to mean a vehicle at all, or a replicator. Much the same point has been realized by the philosopher D. L. Hull (1980a,b), but after some thought I prefer to persist with my own terminology rather than adopt his ‘interactors’ and ‘evolvors’.

  I define a replicator as anything in the universe of which copies are made. Examples are a DNA molecule, and a sheet of paper that is xeroxed. Replicators may be classified in two ways. They may be ‘active’ or ‘passive’, and, cutting across this classification, they may be ‘germ-line’ or ‘dead-end’ replicators.

  An active replicator is any replicator whose nature has some influence over its probability of being copied. For example a DNA molecule, via protein synthesis, exerts phenotypic effects which influence whether it is copied: this is what natural selection is all about. A passive replicator is a replicator whose nature has no influence over its probability of being copied. A xeroxed sheet of paper at first sight seems to be an example, but some might argue that its nature does influence whether it is copied, and therefore that it is active: humans are more likely to xerox some sheets of paper than others, because of what is written on them, and these copies are, in their turn, relatively likely to be copied again. A section of DNA that is never transcribed might be a genuine example of a passive replicator (but see Chapter 9 on ‘selfish DNA’).

  A germ-line replicator (which may be active or passive) is a replicator that is potentially the ancestor of an indefinitely long line of descendant replicators. A gene in a gamete is a germ-line replicator. So is a gene in one of the germ-line cells of a body, a direct mitotic ancestor of a gamete. So is any gene in Amoeba proteus. So is an RNA molecule in one of Orgel’s (1979) test-tubes. A dead-end replicator (which also may be active or passive) is a replicator which may be copied a finite number of times, giving rise to a short chain of descendants, but
which is definitely not the potential ancestor of an indefinitely long line of descendants. Most of the DNA molecules in our bodies are dead-end replicators. They may be the ancestors of a few dozen generations of mitotic replication, but they will definitely not be long-term ancestors.

  A DNA molecule in the germ-line of an individual who happens to die young, or who otherwise fails to reproduce, should not be called a dead-end replicator. Such germ-lines are, as it turns out, terminal. They fail in what may metaphorically be called their aspiration to immortality. Differential failure of this kind is what we mean by natural selection. But whether it succeeds in practice or not, any germ-line replicator is potentially immortal. It ‘aspires’ to immortality but in practice is in danger of failing. All the DNA molecules in fully sterile social insect workers, however, are true dead-end replicators. They do not even aspire to replicate indefinitely. Workers lack a germ-line, not as a matter of misfortune but as a matter of design. In this respect they resemble human liver cells rather than the spermatogonia of a human who happens to be celibate. There may be awkward intermediate cases, for instance the ‘sterile’ worker who becomes facultatively fertile if her mother dies, and the Streptocarpus leaf which is not expected to propagate a new plant but which can do so if planted as a cutting. But this is getting theological: let us not worry precisely how many angels can dance on a pin’s head.

  As I said, the active/passive distinction cuts across the germ-line/dead-end distinction. All four combinations are conceivable. Particular interest attaches to one of the four, the active germ-line replicator, for it is, I suggest, the ‘optimon’, the unit for whose benefit adaptations exist. The reason active germ-line replicators are important units is that, wherever in the universe they may be found, they are likely to become the basis for natural selection and hence evolution. If replicators exist that are active, variants of them with certain phenotypic effects tend to out-replicate those with other phenotypic effects. If they are also germ-line replicators, these changes in relative frequency can have long-term, evolutionary impact. The world tends automatically to become populated by germ-line replicators whose active phenotypic effects are such as to ensure their successful replication. It is these phenotypic effects that we see as adaptations to survival. When we ask whose survival they are adapted to ensure, the fundamental answer has to be not the group, nor the individual organism, but the relevant replicators themselves.

  I have previously summed up the qualities of a successful replicator ‘in a slogan reminiscent of the French Revolution: Longevity, Fecundity, Fidelity’ (Dawkins 1978a). Hull (1980b) explains the point clearly.

  Replicators need not last forever. They need only last long enough to produce additional replicators [fecundity] that retain their structure largely intact [fidelity]. The relevant longevity concerns the retention of structure through descent. Some entities, though structurally similar, are not copies because they are not related by descent. For example, although atoms of gold are structurally similar, they are not copies of one another because atoms of gold do not give rise to other atoms of gold. Conversely, a large molecule can break down into successively smaller molecules as its quaternary, tertiary, and secondary bonds are severed. Although descent is present, these successively smaller molecules cannot count as copies because they lack the requisite structural similarity.

  A replicator may be said to ‘benefit’ from anything that increases the number of its descendant (‘germ-line’) copies. To the extent that active germ-line replicators benefit from the survival of the bodies in which they sit, we may expect to see adaptations that can be interpreted as for bodily survival. A large number of adaptations are of this type. To the extent that active germ-line replicators benefit from the survival of bodies other than those in which they sit, we may expect to see ‘altruism’, parental care, etc. To the extent that active germ-line replicators benefit from the survival of the group of individuals in which they sit, over and above the two effects just mentioned, we may expect to see adaptations for the preservation of the group. But all these adaptations will exist, fundamentally, through differential replicator survival. The basic beneficiary of any adaptation is the active germ-line replicator, the optimon.

  It is important not to forget the ‘germ-line’ proviso in the specification of the optimon. This is the point of Hull’s gold atom analogy. Krebs (1977) and I (Dawkins 1979a) have previously criticized Barash (1977) for suggesting that sterile worker insects care for other workers because they share genes with them. I would not harp on this again, had the error not been repeated twice recently in print (Barash 1978; Kirk 1980). It would be more correct to say that workers care for their reproductive siblings who carry germ-line copies of the caring genes. If they care for other workers, it is because those other workers are likely to work on behalf of the same reproductives (to whom they also are kin), not because the workers are kin to each other. Worker genes may be active, but they are dead-end, not germ-line replicators.

  No copying process is infallible. It is no part of the definition of a replicator that its copies must all be perfect. It is fundamental to the idea of a replicator that when a mistake or ‘mutation’ does occur it is passed on to future copies: the mutation brings into existence a new kind of replicator which ‘breeds true’ until there is a further mutation. When a sheet of paper is xeroxed, a blemish may appear on the copy which was not present on the original. If the xerox copy itself is now copied, the blemish is incorporated into the second copy (which may also introduce a new blemish of its own). The important principle is that in a chain of replicators errors are cumulative.

  I have previously used the word ‘gene’ in the same sense as I would now use ‘genetic replicator’, to refer to a genetic fragment which, for all that it serves as a unit of selection, does not have rigidly fixed boundaries. This has not met with uniform approval. The eminent molecular biologist Gunther Stent (1977) wrote that ‘One of the great triumphs of 20th century biology was the eventual unambiguous identification of the Mendelian hereditary factor, or gene … as that unit of genetic material … in which the amino acid sequence of a particular protein is encoded.’ Stent therefore violently objected to my adopting the equivalent of Williams’s (1966) definition of a gene as ‘that which segregates and recombines with appreciable frequency’, describing it as a ‘heinous terminological sin’.

  Such motherly protectiveness towards a rather recently usurped technical term is not universal among molecular biologists, for one of the greatest of them has recently written that ‘the theory of the “selfish gene” will have to be extended to any stretch of DNA’ (Crick 1979). And, as we saw at the beginning of this chapter, another molecular biologist of the first rank, Seymour Benzer (1957), recognized the shortcomings of the traditional gene concept, but rather than grab the traditional word gene itself for one particular molecular usage, he chose the more modest course of coining a useful set of new terms—muton, recon and cistron, to which we may add the optimon. Benzer recognized that all three of his units had claims to be regarded as equivalent to the gene of the earlier literature. Stent’s uncompromising elevation of the cistron to the honour is arbitrary, though admittedly it is quite common. A more balanced view was given by the lamented W. T. Keeton (1980): ‘It may seem strange that geneticists continue to employ different definitions of the gene for different purposes. The fact is that, at the present stage of knowledge, one definition is more useful in one context and another in another context; a rigid terminology would only hamper the formulation of current ideas and research aims.’ Lewontin (1970b), too, gets it right when he says that ‘it is only the chromosomes that obey Mendel’s Law of Independent Assortment, and only the nucleotide base that is indivisible. The codons and the genes [cistrons] lie in between, being neither unitary nor independent in their behavior at meiosis.’

  But let us not become worked up over terminology. Meanings of words are important, but not important enough to justify the ill-feeling they sometimes provoke, as i
n the present case of Stent (and also as in Stent’s passionate and apparently sincere denunciation of my following the standard modern fashion of redefining ‘selfishness’ and ‘altruism’ in non-subjective senses—see Dawkins, 1981, for a reply to a similar criticism). I am happy to replace ‘gene’ with ‘genetic replicator’ where there is any doubt.

  Heinous terminological sins aside, Stent makes the more important point that my unit is not precisely delimited in the way that the cistron is. Well, perhaps I should say ‘in the way that the cistron once seemed to be’, for the recent discovery of ‘embedded’ cistrons in virus ΦX174, and of ‘exons’ surrounding ‘introns’ must be causing a little discomfort to anyone who likes his units rigid. Crick (1979) expresses the sense of novelty well: ‘In the last 2 years there has been a mini-revolution in molecular genetics. When I came to California, in September 1976, I had no idea that a typical gene might be split into several pieces and I doubt if anyone else had.’ Crick significantly adds a footnote to the word gene: ‘Throughout this article I have deliberately used the word “gene” in a loose sense since at this time any precise definition would be premature.’ My unit of selection, whether I called it gene (Dawkins 1976a) or replicator (1978a) never had any pretensions to unitariness anyway. For the purposes for which it was defined, unitariness is not an important consideration, although I readily see that it might be important for other purposes.

  The word replicator is purposely defined in a general way, so that it does not even have to refer to DNA. I am, indeed, quite sympathetic towards the idea that human culture provides a new milieu in which an entirely different kind of replicator selection can go on. In the next chapter we shall look briefly at this matter, and also at the claims of species gene-pools to be regarded as replicators in a large-scale selection process governing ‘macroevolutionary’ trends. But in the rest of this chapter we shall be concerned only with genetic fragments, and ‘replicator’ will be used as an abbreviation for ‘genetic replicator’.