The Extended Phenotype: The Long Reach of the Gene (Popular Science) (52 page)

If we look at a gene in any cell in a living organism and trace its history backwards in evolutionary time, the most recent few cell divisions of its
‘experience’ may be somatic, but once we reach a germ-line cell division in our backwards march, all previous ones in the gene’s history must be germ-line divisions. Germ-line cell divisions may be thought of as proceeding forwards in evolutionary time, while somatic cell divisions are proceeding sideways. Somatic cell divisions are used to make mortal tissues, organs and instruments whose ‘purpose’ is the promoting of germ-line cell divisions. The world is populated by genes which have survived in germ-lines as a consequence of aid that they received from their exact duplicates in somatic cells. Growth comes about through the propagation of dead-end somatic cells, while reproduction is the means of the propagation of germ-line cells.

Harper (1977) makes a distinction between reproduction and growth in plants, which will normally amount to the same as my distinction between germ-line and somatic cell division: ‘The distinction made here between “reproduction” and “growth” is that reproduction involves the formation of a new individual from a single cell: this is usually (though not always e.g. apomicts) a zygote. In this process a new individual is “reproduced” by the information that is coded in the cell. Growth, in contrast, results from the development of organized meristems’ (Harper 1977, p. 27 fn.). What matters here is whether there really is an important biological distinction between growth and reproduction which is not the same as the distinction between mitosis and meiosis + sex. Is there really a crucial difference between ‘reproducing’ to make two aphids on the one hand, and ‘growing’ to make one aphid twice as large on the other? Janzen would presumably say no. Harper would presumably say yes. I agree with Harper, but I would not have been able to justify my position until I had read J. T. Bonner’s (1974) inspiring book
On Development
. The justification is best made with the aid of thought experiments.

Imagine a primitive plant consisting of a flat, pad-like thallus, floating on the surface of the sea, absorbing nutrients through its lower surface and sunlight through its upper surface. Instead of ‘reproducing’ (i.e. sending off single-celled propagules to grow elsewhere), it simply grows at its margins, spreading into an ever larger circular green carpet, like a monstrous lily pad several miles across and still growing. Maybe older parts of the thallus eventually die, so that it consists of an expanding ring rather than a filled circle like a true lily pad. Perhaps also, from time to time, chunks of the thallus split off, like icefloes shearing away from the pack ice, and separate chunks drift to different parts of the ocean. Even if we assume this kind of fission, I shall show that it is not reproduction in an interesting sense.

Now consider a similar kind of plant which differs in one crucial respect. It stops growing when it attains a diameter of 1 foot, and reproduces instead. It manufactures single-celled propagules, either sexually or asexually, and sheds them into the air where they may be carried a long way on the wind. When one of these propagules lands on the water surface it becomes a new
thallus, which grows until it is 1 foot wide, then reproduces again. I shall call the two species G (for growth) and R (for reproduction) respectively.

Following the logic of Janzen’s paper, we should see a crucial difference between the two species only if the ‘reproduction’ of the second species, R, is sexual. If it is asexual, the propagules shed into the air being mitotic products genetically identical to the cells of the parent thallus, there is, for Janzen, no important difference between the two species. The separate ‘individuals’ in R are no more genetically distinct than different regions of the thallus in G might be. In either species, mutation can initiate new clones of cells. There is no particular reason why, in R, mutations should occur during propagule formation any more than during thallus growth. R is simply a more fragmented version of G, just as a clone of dandelions is like a fragmented tree. My purpose in making the thought experiment, however, was to disclose an important difference between the two hypothetical species, representing the difference between growth and reproduction, even when reproduction is asexual.

G just grows, while R grows and reproduces in alternation. Why is the distinction important? The answer cannot be a genetic one in any simple sense because, as we have seen, mutations are just as likely to initiate genetic change during growth-mitosis as during reproduction-mitosis. I suggest that the important distinction between the two species is that a lineage of R is capable of evolving complex adaptations in a way that G is not. The reasoning goes as follows.

Consider again the past history of a gene, in this case a gene sitting in a cell of R. It has had a history of passing repeatedly from one ‘vehicle’ to another similar vehicle. Each of its successive bodies began as a single-celled propagule, then grew through a fixed cycle, then passed the gene on into a new single-celled propagule and hence a new multicellular body. Its history has been a cyclical one, and now here is the point. Since each of this long series of successive bodies developed anew from single-celled beginnings, it is possible for successive bodies to develop slightly differently from their predecessors. Evolution of complex body structure with organs, say a complex apparatus for catching insects like a Venus fly trap, is only possible if there is a cyclically repeating developmental process to evolve. I shall return to this point in a moment.

Meanwhile, compare G. A gene sitting in a young cell at the growing margin of the huge thallus has a history which is not cyclical, or is cyclical only at the cellular level. The ancestor of the present cell was another cell, and the career of the two cells was very similar. Each cell of an R plant, by contrast, has a definite place in the growth sequence. It is either near the centre of the 1-foot thallus, or near the rim, or at some particular place in between. It can therefore differentiate to fill its special role in its appointed place in an organ of the plant. A cell of G has no such specific developmental
identity. All cells first appear at the growing margin, and later find themselves enclosed by other, younger cells. There is cyclicity only at the cellular level, which means that in G evolutionary change can take place only at the cellular level. Cells might improve on their predecessors in the cell lineage, developing more complex internal organelle structure, say. But the evolution of organs and adaptations at the multicellular level could not take place, because recurrent, cyclical development of whole groups of cells does not occur. It is, of course, true that in G the cells and their ancestors are in physical contact with other cells, and in this sense form a multicellular ‘structure’. But as far as putting together complex multicellular organs is concerned, they might just as well have been free-swimming protozoa.

In order to put together a complex multicellular organ you need a complex developmental sequence. A complex developmental sequence has to have evolved from an earlier developmental sequence which was slightly less complex. There has to be an evolutionary progression of developmental sequences, each one in the series being a slight improvement on its predecessor. G does not have a recurring developmental sequence other than the high-frequency cycle of development at the single-cell level. Therefore it cannot evolve multicellular differentiation and organ-level complexity. To the extent that it can be said to have a multicellular developmental process at all, that development continues non-cyclically through geological time: the species makes no separation between the growth time-scale and the would-be evolution time-scale. The only high-frequency developmental cycle available to it is the cell cycle. R, on the other hand, has a multicellular developmental cycle which is fast compared with evolutionary time. Therefore, as the ages succeed, later developmental cycles can be different from earlier developmental cycles, and multicellular complexity can evolve. We are moving towards a definition of the organism as the unit which is initiated by a new act of
reproduction
via a single-celled developmental ‘bottleneck’.

The importance of the difference between growth and reproduction is that each act of reproduction involves a new developmental cycle. Growth simply involves swelling of the existing body. When an aphid gives rise to a new aphid by parthenogenetic reproduction the new aphid, if it is a mutant, may be radically different from its predecessor. When an aphid grows to twice its original size, on the other hand, all its organs and complex structures simply swell. It might be said that somatic mutations could occur within cell lineages of the growing giant aphid. True, but a mutation within a somatic cell line in a heart, say, cannot radically re-organize the structure of the heart. To switch the example to vertebrates, if the present heart is two-chambered, with one auricle feeding one ventricle, new mutations in the mitotic cells at the growing margin of the heart are very unlikely to achieve radical restructuring of the heart so that it comes to have four chambers with
a pulmonary circulation kept separate from the rest. In order to put together new complexity, new developmental beginnings are required. A new embryo must start from scratch, without any heart at all. Then a mutation can act on sensitive key points in early development to bring about a new fundamental architecture of the heart. Developmental recycling allows a return ‘back to the drawing board’ (see below) in every generation.

We began this chapter by wondering why replicators have ganged up into large, multicellular clones called organisms, and we initially gave a rather unsatisfactory answer. A more satisfying answer is now starting to emerge. An organism is the physical unit associated with one single life cycle. Replicators that gang up in multicellular organisms achieve a regularly recycling life history, and complex adaptations to aid their preservation, as they progress through evolutionary time.

Some animals have a life cycle involving more than one distinct body. A butterfly is utterly different from the caterpillar which preceded it. It is hard to imagine a butterfly growing from a caterpillar by slow, within-organ change: caterpillar organ growing into corresponding butterfly organ. Instead, what happens is that the complex organ structure of the caterpillar is largely broken down and the tissues of the caterpillar are used as fuel for the development of a whole new body. The new butterfly body does not quite restart from a single cell, but the principle is the same. It develops a radically new bodily structure from simple, relatively undifferentiated imaginal discs. There is a partial return to the drawing board.

Returning to the growth/reproduction distinction itself, Janzen was not actually wrong. Distinctions can be unimportant for some purposes, while they remain important for other purposes. For discussing certain kinds of ecological or economic questions, there may be no important distinction between growth and asexual reproduction. A sisterhood of aphids may indeed be analogous to a single bear. But for other purposes, for discussing the evolutionary putting together of complex organization, the distinction is crucial. A certain type of ecologist may gain illumination from comparing a field full of dandelions with a single tree. But for other purposes it is important to understand the differences, and to see the single dandelion ramet as analogous to the tree.

But Janzen’s position is, in any case, a minority one. A more typical biologist might think it perverse of Janzen to regard asexual reproduction in aphids as growth, and equally perverse of Harper and me to regard vegetative propagation by multicellular runners, as growth and not reproduction. Our decision is based on the assumption that the runner is a multicellular meristem rather than a single-celled propagule, but why should we regard this as an important point? Again, the answer may be seen in a thought experiment involving two hypothetical species of plants, in this case strawberry-like plants called M and S (Dawkins in press).

Both the hypothetical strawberry-like species propagate vegetatively, by runner. In both there is a population of what appear to be distinct and recognizable ‘plants’ connected by a network of runners. In both species, each ‘plant’ (i.e. ramet) can give rise to more than one daughter plant, so that we have the possibility of exponential growth of the ‘population’ (or growth of the ‘body’ depending on your point of view). Even though there is no sex, there can be evolution since mutations will sometimes occur in the mitotic cell divisions (Whitham & Slobodchikoff in press). Now comes the crucial difference between the two species. In species M (for many, or multicellular, or meristem), the runner is a broad-fronted multicellular meristem. This means that two cells in any one ‘plant’ may be the mitotic descendants of two different cells in the parent plant. In terms of mitotic descent, a cell may therefore be a closer cousin of a cell in another ‘plant’ than it is of another cell in its own plant. If mutation has introduced genetic heterogeneity into the cell population, this means that individual plants may be genetic mosaics, with some cells having closer genetic relatives in other plants than in their own. We will see the consequences of this for evolution in a moment. Meanwhile we turn to the other hypothetical species.

Species S (for single) is exactly like M, except that each runner culminates in a single apical cell. This cell acts as the basal mitotic ancestor of all the cells of the new daughter plant. This means that all cells in a given plant are closer cousins to each other than they are to any cells in other plants. If mutation introduces genetic heterogeneity into the population of cells, there will be relatively few mosaic plants. Rather, each plant will tend to be a genetically uniform clone, but it may differ genetically from some other plants, while being genetically identical to yet other plants. There will be a true population of
plants
, each one of which has a genotype characteristic of all its cells. It is therefore possible to conceive of selection, in the sense which I have called ‘vehicle selection’, acting at the level of the whole plant. Some whole plants may be better than others, because of their superior genotypes.