The Extended Phenotype: The Long Reach of the Gene (Popular Science) (20 page)

But there is a more interesting reason for rejecting the concept of the selfish nucleotide, in favour of some larger replicating entity. The whole purpose of our search for a ‘unit of selection’ is to discover a suitable actor to play the leading role in our metaphors of purpose. We look at an adaptation and want to say, ‘It is for the good of …’. Our quest in this chapter is for the right way to complete that sentence. It is widely admitted that serious error follows from the uncritical assumption that adaptations are for the good of the species. I hope I shall be able to show, in this book, that yet other theoretical dangers, albeit lesser ones, attend the assumption that adaptations are for the good of the individual organism. I am suggesting here that, since we must speak of adaptations as being for the good of something, the correct something is the active, germ-line replicator. And while it may not be strictly wrong to say that an adaptation is for the good of the nucleotide, i.e. the smallest replicator responsible for the phenotypic differences concerned in the evolutionary change, it is not helpful to do so.

We are going to use the metaphor of power. An active replicator is a chunk of genome that, when compared to its alleles, exerts phenotypic power over its world, such that its frequency increases or decreases relative to that of its alleles. While it is undoubtedly meaningful to speak of a single nucleotide as exerting power in this sense, it is much more useful, since the nucleotide only exerts a given type of power when embedded in a larger unit, to treat the larger unit as exerting power and hence altering the frequency of its copies. It might be thought that the same argument could be used to justify treating an even larger unit, such as the whole genome, as the unit that exerts the power. This is not so, at least for sexual genomes.

We reject the whole sexual genome as a candidate replicator, because of its high risk of being fragmented at meiosis. The single nucleotide does not suffer from this problem but, as we have just seen, it raises another problem. It cannot be said to have a phenotypic effect except in the context of the other nucleotides that surround it in its cistron. It is meaningless to speak of the phenotypic effect of adenine. But it is entirely sensible to speak of the phenotypic effect of substituting adenine for cytosine at a named locus within a named cistron. The case of a cistron within a genome is not analogous.
Unlike a nucleotide, a cistron is large enough to have a consistent phenotypic effect, relatively, though not completely, independently of where it lies on the chromosome (but not regardless of what other genes share its genome). For a cistron, its sequential context
vis-à-vis
other cistrons is not overwhelmingly important in determining its phenotypic effect in comparison with its alleles. For a
nucleotide’s
phenotypic effect, on the other hand, its sequential context is everything.

Bateson (1981) expresses the following misgiving about ‘replicator selection’.

A winning character is defined in
relation
to another one while genetic replicators are thought about in
absolute
and atomistic terms. The difficulty is brought home if you ask yourself, what exactly is Dawkins’ replicator? You might answer: ‘That bit of genetic material making the difference between the winning and losing characters.’ You would have stated that a replicator must be defined in relation to something else. Alternatively, your reply might be: ‘A replicator consists of all the genes required for the expression of the surviving character’. In that case you are saddled with a complex and unwieldy concept. Either way your answer would show how misleading it is to think of replicators as the atoms of evolution.

I certainly would join Bateson in rejecting the second of his two alternative answers, the unwieldly one. The first of his alternatives, on the other hand, expresses exactly my position, and I do not share Bateson’s misgivings about it. For my purposes a genetic replicator is defined by reference to its alleles, but this is not a weakness of the concept. Or, if it is deemed to be a weakness, it is a weakness that afflicts the whole science of population genetics, not just the particular idea of genetic units of selection. It is a fundamental truth, though it is not always realized, that
whenever
a geneticist studies a gene ‘for’ any phenotypic character, he is always referring to a
difference
between two alleles. This is a recurring theme throughout this book.

To prove the pudding, let me show how easy it is to use the gene as a conceptual unit of selection, while admitting that it is only defined by comparison with its alleles. It is now accepted that a particular major gene for dark coloration in the peppered moth
Biston betularia
has increased in frequency in industrial areas because it produces phenotypes that are superior in industrial areas (Kettlewell 1973). At the same time, we have to admit that this gene is only one of thousands that are necessary in order for the dark coloration to show itself. A moth cannot have dark wings unless it has wings, and it cannot have wings unless it has hundreds of genes and hundreds of equally necessary environmental factors. But this is all
irrelevant. The
difference
between the
carbonaria
and the
typica
phenotype can still be due to a difference at one locus, even though the phenotypes themselves could not exist without the participation of thousands of genes. And it is the same difference that is the basis of the natural selection. Both geneticists
and
natural selection are concerned with differences! However complex the genetic basis of features that all members of a species have
in common
, natural selection is concerned with differences. Evolutionary change is a limited set of substitutions at identifiable loci.

Further difficulties will be dealt with in the next chapter. Meanwhile, I end this chapter with a small diversion which may be helpful in illustrating the replicator or ‘gene’s-eye’ view of evolution. An appealing aspect of the view appears if we look backwards in time. The replicators in frequent existence today constitute a relatively successful subset of those that have existed in the past. A given replicator in me could, in theory, be traced backwards through a straight line of ancestors. These ancestors, and the environments that they provided for the replicator, can be regarded as the replicator’s ‘past experience’.

The past experience of autosomal genetic fragments in a species is, statistically speaking, similar. It consists of an ensemble of typical species bodies, approximately 50 per cent male and 50 per cent female bodies, bodies which grew through a wide spectrum of ages at least up to reproductive age; and it includes a good random shuffling of ‘companion’ genes at other loci. The genes that exist today tend to be the ones that are good at surviving in that statistical ensemble of bodies, and in company with that statistical ensemble of companion genes. As we shall see, it is selection in favour of the qualities needed for survival
in company
with other, similarly selected, genes, that gives rise to the appearance of ‘coadapted genomes’. I shall show in
Chapter 13
that this is a much more illuminating interpretation of the phenomenon of coadaptation than its alternative, that ‘the coadapted genome is the true unit of selection’.

Probably no two genes in an organism have identical past experiences, though a linked pair may come close, and, mutants aside, all the genes on a Y chromosome have travelled together through the same set of bodies for a large number of generations. But the exact nature of a gene’s past experience is of less interest than the generalizations one can make about the past experiences of all genes that exist today. For instance, however variable the set of my ancestors may be, they all had in common that they survived at least to reproductive age, they copulated heterosexually and were fertile. The same generalization cannot be made about the historical set of bodies that were not my ancestors. The bodies that provided the past experience of existing genes are a non-random subset of all the bodies that have ever existed.

The genes that exist today reflect the set of environments that they have
experienced in the past. This includes the internal environments provided by the bodies the genes have inhabited, and also external environments, desert, forest, seashore, predators, parasites, social companions, etc. This is, of course, not because the environments have imprinted their qualities on the genes—that would be Lamarckism (see
Chapter 9
)—but because the genes that exist today are a selected set, and the qualities that made them survive reflect the qualities of the environments in which they survived.

I said that a gene’s experience consists of time spent in approximately 50 per cent male and 50 per cent female bodies, but this is not, of course, true of genes on sex chromosomes. In mammals, assuming no Y-chromosome crossing-over, a gene on a Y chromosome has experienced only male bodies, and a gene on an X chromosome has spent two-thirds of its history in female bodies and one-third in male bodies. In birds, Y-chromosome genes have experienced only female bodies, and in particular cases such as cuckoos we can say something further. Female
Cuculus canorus
are divided into ‘gentes’, each gens parasitizing a different species of host (Lack 1968). Apparently each female learns the qualities of her own foster parents and their nest, and returns when adult to parasitize the same species. Males do not seem to discriminate as to gens in their choice of mate, and therefore they act as vehicles for gene flow between gentes. Of the genes in a female cuckoo, therefore, those on autosomes and the X chromosome have probably had recent experience of all gentes in the population, and been ‘reared’ by foster parents belonging to all the species parasitized by the cuckoo population. But the Y chromosome, uniquely, is confined for long sequences of generations to one gens and one foster species. Of all the genes sitting in a robin’s nest, one subset—robin genes and cuckoo Y-chromosome genes (and robin flea genes)—has sat in robins’ nests for many generations back. Another subset—cuckoo autosomal and X-chromosome genes—has experienced a mixture of nests. Of course the first subset share only part of their experience, a long series of robin nests. In other aspects of their experience, cuckoo Y-chromosome genes will have more in common with other cuckoo genes than with robin genes. But as far as certain particular selection pressures found in nests are concerned, cuckoo Y-chromosome genes have more in common with robin genes than with cuckoo autosome genes. It is natural, then, that cuckoo Y chromosomes should have evolved to reflect their peculiar experience, while other cuckoo genes simultaneously evolved to reflect their more general experience—a kind of incipient intragenomic ‘speciation’ at the chromosomal level. It is, indeed, widely assumed for this reason that genes for foster species-specific egg mimicry must be carried on the Y chromosome, while genes for general parasitic adaptations might be carried on any chromosome.

I am not sure whether the fact has significance, but this backwards way of looking shows X chromosomes, too, to have a peculiar history. A gene on an
autosome in a female cuckoo is as likely to have come from the father as from the mother, in which latter case it experiences the same host species for two generations running. A gene on an X chromosome in a female cuckoo is bound to have come from the father, and therefore is not especially likely to experience the same host species two generations running. A statistical ‘runs test’ on the sequence of foster species experienced by an autosomal gene would therefore reveal a slight runs effect, greater than that for a gene on an X chromosome, and much less than that for a gene on a Y chromosome.

In any animal, an inverted portion of chromosome may resemble a Y chromosome in being unable to cross over. The ‘experience’ of any part of the ‘inversion supergene’ therefore repeatedly includes the other parts of the supergene and their phenotypic consequences. A habitat selection gene anywhere in such a supergene, say a gene that makes individuals choose dry microclimates, would then provide a consistent habitat ‘experience’ for successive generations of the whole supergene. Thus a given gene may ‘experience’ consistently dry habitats for the same kind of reason as a gene on a cuckoo’s Y chromosome consistently experiences meadow-pipit nests. This will provide a consistent selection pressure bearing upon that locus, favouring alleles that are adapted to a dry habitat in the same way as alleles for mimicking meadow-pipit eggs are favoured in Y chromosomes of female cuckoos of the meadow-pipit gens. This particular inversion supergene will tend to be found for generations in dry habitats, even though the rest of the genome may be randomly shuffled over the whole range of habitats available to the species. Many different loci on the inverted portion of chromosome may therefore come to be adapted to a dry climate, and again something akin to intragenomic incipient speciation may go on. I find this backwards way of looking at the past ‘experience’ of genetic replicators helpful.

Germ-line replicators, then, are units that actually survive or fail to survive, the difference constituting natural selection. Active replicators have some effect on the world, which influences their chances of surviving. It is the effects on the world of successful active germ-line replicators that we see as adaptations. Fragments of DNA qualify as active germ-line replicators. Where there is sexual reproduction, these fragments must not be defined too large if they are to retain the property of self-duplication. And they must not be defined too small if they are to be usefully regarded as active.

If there were sex but no crossing-over, each chromosome would be a replicator, and we should speak of adaptations as being for the good of the chromosome. If there is no sex we can, by the same token, treat the entire genome of an asexual organism as a replicator. But the organism itself is
not
a replicator. This is for two quite distinct reasons which should not be confused with each other. The first reason follows from the arguments developed in this chapter, and applies only where there is sexual reproduction and meiosis: meiosis and sexual fusion see to it that not even our genomes are
replicators, so we ourselves are not replicators either. The second reason applies to asexual as well as sexual reproduction. It will be explained in the next chapter, which goes on to discuss what organisms, and also groups of organisms,
are
, given that they are not replicators.