The Extended Phenotype: The Long Reach of the Gene (Popular Science) (51 page)

I am grateful to Dr J. P. Hailman for not withholding from me the sarcastic reaction of a colleague to the paper that was a brief trial-run for this book (Dawkins 1978a): ‘Richard Dawkins has rediscovered the organism.’ The irony was not lost on me, but there are wheels within wheels. We agree that there is something special about the individual organism as a level in the hierarchy of life, but it is not something obvious, to be accepted without question. My hope is that this book has revealed that there is a second side to the Necker Cube. But Necker Cubes have a habit of flipping back again to their original orientation, and then continuing to alternate. Whatever it is that is special about the individual organism as a unit of life, we should at least see it more clearly for having viewed the other side of the Necker Cube, for having trained our eyes to see through body walls into the world of replicators, and out and beyond to their extended phenotypes.

So, what is it that is special about the individual organism? Given that life can be viewed as consisting of replicators with their extended phenotypic tools of survival, why in practice have replicators chosen to group themselves together by the hundreds of thousands in cells, and why have they influenced those cells to clone themselves by the millions of billions in organisms?

One kind of answer is suggested by the logic of complex systems. Simon (1962) has written a stimulating essay on ‘The architecture of complexity’, which suggests (using a parable of two watchmakers called Tempus and Hora, which has become well known), a general functional reason why complex organization of any kind, biological or artificial, tends to be organized into nested hierarchies of repeated subunits. I have developed his argument in the ethological context, concluding that the evolution of statistically ‘improbable assemblies proceeds more rapidly if there is a succession of intermediate stable sub-assemblies. Since the argument can be applied to each sub-assembly, it follows that highly complex systems which exist in the world are likely to have a hierarchical architecture’ (Dawkins 1976b). In the present context the hierarchy consists of genes within cells and cells within organisms. Margulis (1981) makes a persuasive and fascinating case for an old idea that the hierarchy contains yet another intermediate level: eukaryotic ‘cells’ are themselves, in a sense, multi-cellular clusters, symbiotic unions of entities such as mitochondria, plastids and cilia, which are homologous to, and descended from, prokaryotic cells. I will not pursue the matter further here. Simon’s point is a very general one, and we need a more specific answer to the question of why replicators
chose to organize their phenotypes into functional units, especially at the two levels of the cell and the multicellular organism.

In order to ask questions about why the world is the way it is, we have to imagine how it might have been. We invent possible worlds in which life might have been organized differently, and ask what would have happened if it had been. What instructive alternatives to the way life is, then, can we imagine? First, in order to see why replicating molecules ganged up in cells, we imagine a world in which there are replicating molecules floating freely in the sea. There are different varieties of replicator, and they are competing with each other for space and for the chemical resources needed to build copies of themselves, but they are not grouped together in chromosomes or nuclei. Each solitary replicator exerts phenotypic power to make copies of itself, and selection favours those with the most effective phenotypic power. It is easy to believe that this form of life would not be evolutionarily stable. It would be invaded by mutant replicators that ‘gang up’. Certain replicators would have chemical effects that complement those of other replicators, complement them in the sense that when the two chemical effects are put together replication of both is facilitated (Model 2 in the previous chapter). I have already used the example of genes coding for enzymes that catalyse successive stages of a biochemical chain reaction. The same principle may be applied to larger groups of mutually complementary replicating molecules Indeed, earthly biochemistry suggests that the minimal unit of replication, except possibly in the food-rich environment of a total parasite, is about fifty cistrons (Margulis 1981). It makes no difference to the argument whether new genes arise by duplication of old ones and remain close together, or whether previously independent genes positively come together. We can still discuss the evolutionary stability of the state of being ‘ganged up’.

Ganging up of genes together into cells, then, is easily understood, but why did cells gang together into multicellular clones? In this case it might be thought that we do not have to invent thought experiments, because unicellular, or acellular, organisms abound on our world. These, however, are all small, and it may be useful to imagine a possible world in which there exist large and complex unicellular or mononucleate organisms. Could there be a form of life in which one single set of genes, enthroned in a single central nucleus, directed the biochemistry of a macroscopic body with complex organs, either a single gigantic ‘cell’, or a multicellular body in which all but one of the cells lacked their own private copies of the genome? I think such a form of life could only exist if its embryology followed principles very different from those with which we are familiar. In the embryologies that we know, only a minority of genes are ‘turned on’ in any one type of differentiating tissue at any one time (Gurdon 1974). It is admittedly a weak argument at this stage, but if there were only one set of genes in the entire body, it is not easy to see how the appropriate gene products could be
conveyed to the various parts of the differentiating body at the appropriate times.

But why does there have to be a
complete
set of genes in every cell of a developing body? It is surely easy to imagine a form of life in which parts of the genome are hived off during differentiation, so that a given type of tissue, liver tissue or kidney tissue say, has only the genes that it needs. Only the germ-line cells, it would seem, really need to preserve the entire genome. It may be that the reason is simply that there is no easy way, physically, to hive off parts of the genome. It is not, after all, as though the genes needed in any particular differentiated region of the developing body are all segregated on one chromosome. We could, I suppose, now ask ourselves why
this
had to be the case. Given that it
is
the case, full division of the entire genome at every cell division may simply be the easiest and most economical way of doing things. However, in the light of my parable (
Chapter 9
) of the rosy-spectacled Martian and the need for cynicism, the reader may be tempted to speculate further. Could it be that the total, rather than partial, duplication of the genome in mitosis is an adaptation by some genes to keep themselves in a position to oversee and thwart would-be outlaws among their colleagues? Personally I doubt it, not because the idea is inherently farfetched but because it is hard to see how a gene in the liver, say, could stand to gain from being an outlaw and manipulating the liver in a way that would be to the detriment of genes in the kidney or the spleen. Following the logic of the chapter on parasites, the interests of ‘liver genes’ and ‘kidney genes’ would overlap because they share the same germ-line and the same gametic route out of the present body.

I have not provided a rigorous definition of the organism. It is, indeed, arguable that the organism is a concept of dubious utility, precisely because it is so difficult to define satisfactorily. From the immunological or genetic points of view, a pair of monozygotic twins would have to count as a single organism, yet clearly they would not so qualify from the point of view of the physiologist, the ethologist, or Huxley’s indivisibility criterion. What is ‘the individual’ in a colonial siphonophore or bryozoan? Botanists have good reason to be less fond of the phrase ‘individual organism’ than zoologists are: ‘The individual fruit fly, flour beetle, rabbit, flatworm or elephant is a population at the cellular but not at any higher level. Starvation does not change the number of legs, hearts or livers of an animal but the effect of stress on a plant is to alter both the rate of formation of new leaves and the rate of death of old ones: a plant may react to stress by varying the number of its parts’ (Harper 1977, pp. 20–21). To Harper, as a plant population biologist, the leaf may be a more salient ‘individual’ than ‘the plant’, since the plant is a straggling, vague entity for whom reproduction may be hard to distinguish from what a zoologist would happily call ‘growth’. Harper feels obliged to coin two new terms for different kinds of ‘individual’ in botany. ‘The
“ramet” is the unit of clonal growth, the module that may often follow an independent existence if severed from the parent plant.’ Sometimes, as in strawberries, the ramet is the unit that we ordinarily call a ‘plant’. In other cases such as white clover the ramet may be the single leaf. The ‘genet’, on the other hand, is the unit which springs from one single-celled zygote, the ‘individual’ in the sense of a zoologist whose animals reproduce sexually.

Janzen (1977) faces up to the same difficulty, suggesting that a clone of dandelions should be regarded as one ‘evolutionary individual’ (Harper’s genet), equivalent to a single tree although spread out along the ground rather than raised up in the air on a trunk, and although divided up into separate physical ‘plants’ (Harper’s ramets). According to this view, there may be as few as four individual dandelions competing with each other for the territory of the whole of North America. Janzen sees a clone of aphids in the same way. His paper has no literature citations at all, but the view is not a new one. It goes back at least as far as 1854, when T. H. Huxley ‘treated each life cycle as an individual, with all the products from sexual event to sexual event being a single unit. He even treated an asexual lineage of aphids as an individual’ (Ghiselin 1981). There is merit in this way of thinking, but I shall show that it leaves out something important.

One way to re-express the Huxley/Janzen argument is as follows. The germ-line of a typical organism, say a human, goes through a sequence of perhaps a few dozen mitotic divisions between each meiosis. Employing
Chapter 5’s
‘backwards’ way of looking at the ‘past experience of a gene’, any given gene in a living human has a history of cell divisions as follows: meiosis mitosis mitosis … mitosis meiosis. In every successive body, in parallel with the mitotic division of the germ-line, other mitotic divisions have furnished the germ-line with a large clone of ‘helper’ cells, grouped together into a body in which the germ-line is housed. In every generation the germ-line is funnelled down into a one-celled ‘bottleneck’ (a gamete followed by a zygote), then it fans out into a many-celled body, then it is funnelled down into a new bottleneck, etc. (Bonner 1974).

The many-celled body is a machine for the production of single-celled propagules. Large bodies, like elephants, are best seen as heavy plant and machinery, a temporary resource drain, invested in so as to improve later propagule production (Southwood 1976). In a sense the germ-line would ‘like’ to reduce capital investment in heavy machinery, reduce the number of cell divisions in the growth part of the cycle, so as to reduce the interval between recurrence of the reproduction part of the cycle. But this recurrence interval has an optimal length which is different for different ways of life. Genes that caused elephants to reproduce when too young and small would propagate themselves less efficiently than alleles tending to produce an optimal recurrence interval. The optimal recurrence interval for genes that happen to find themselves in elephant gene-pools is much longer than the
optimal recurrence interval for genes in mouse gene-pools. In the elephant case, more capital investment is required to be laid down before returns on investment are sought. A protozoan largely dispenses with the growth phase of the cycle altogether, and its cell divisions are all ‘reproductive’ cell divisions.

It follows from this way of looking at organisms that the end product, the ‘goal’ of the growth phase of the cycle, is reproduction. The mitotic cell divisions which put together an elephant are all directed to the end of finally propagating viable gametes which succeed in perpetuating the germ-line. Now, holding this in mind, look at aphids. During the summer, asexual females go through repeated generations of asexual reproduction culminating in a single sexual generation which restarts the cycle. Clearly, by analogy with the elephant, it is easy to follow Janzen in seeing the summer asexual generations as all directed towards the final end of sexual reproduction in autumn. Asexual reproduction, according to this view, is not really reproduction at all. It is growth, just like the growth of a single elephant’s body. For Janzen the whole clone of female aphids is a single evolutionary individual because it is the product of a single sexual fusion. It is an unusual individual in that it happens to be split up into a number of physically separate units, but so what? Each of those physical units contains its own fragment of germ-line, but then so does the left ovary and the right ovary of a female elephant. The fragments of germ-line in the aphid case are separated by thin air, while the two ovaries of an elephant are separated by guts but, again, so what?

Persuasive as this line of argument is, I have already mentioned that I think it misses an important point. It is right to regard most mitotic cell divisions as ‘growth’, ‘aimed’ at the final goal of reproduction, and it is right to regard the individual organism as the product of one reproductive event, but Janzen is wrong to equate the reproduction/growth distinction with the sexual/asexual distinction. There is, to be sure, an important distinction lurking here, but it is not the distinction between sex and non-sex, nor is it the distinction between meiosis and mitosis.

The distinction that I wish to emphasize is that between germ-line cell division (reproduction), and somatic or ‘dead-end’ cell division (growth). A germ-line cell division is one where the genes being duplicated have a chance of being the ancestors of an indefinitely long line of descendants, where the genes are, in fact, true germ-line replicators in the sense of
Chapter 5
. A germ-line cell division may be a mitosis or a meiosis. If we simply look at a cell division under a microscope, there may be no way of telling whether it is a germ-line division or not. Both germ-line and somatic cell divisions may be mitoses of identical appearance.