The Extended Phenotype: The Long Reach of the Gene (Popular Science) (21 page)

I have made so much of the fragmenting effects of meiosis as a reason for not regarding sexually reproduced organisms as replicators, that it is tempting to see this as the only reason. If this were true, it should follow that asexually reproduced organisms are true replicators, and that where reproduction is asexual we could legitimately speak of adaptations as ‘for the good of the organism’. But the fragmenting effect of meiosis is not the only reason for denying that organisms are true replicators. There is a more fundamental reason, and it applies to asexual organisms as much as to sexual ones.

To regard an organism as a replicator, even an asexual organism like a female stick insect, is tantamount to a violation of the ‘central dogma’ of the non-inheritance of acquired characteristics. A stick insect looks like a replicator, in that we may lay out a sequence consisting of daughter, granddaughter, great-granddaughter, etc., in which each appears to be a replica of the preceding one in the series. But suppose a flaw or blemish appears somewhere in the chain, say a stick insect is unfortunate enough to lose a leg. The blemish may last for the whole of her lifetime, but it is not passed on to the next link in the chain. Errors that affect stick insects but not their genes are not perpetuated. Now lay out a parallel series consisting of daughter’s genome, granddaughter’s genome, great-granddaughter’s genome, etc. If a blemish appears somewhere along
this
series it will be passed on to all subsequent links in the chain. It may also be reflected in the bodies of all subsequent links in the chain, because in each generation there are causal arrows leading from genes to body. But there is no causal arrow leading from body to genes. No part of the stick insect’s phenotype is a replicator. Nor is her body as a whole. It is wrong to say that ‘just as genes can pass on their structure in gene lineages, organisms can pass on their structure in organism lineages’.

I am sorry if I am about to labour this argument, but I fear it was my failure to be clear about it before that led to an unnecessary disagreement
with Bateson, a disagreement which it is worth going to some trouble to sort out. Bateson (1978) made the point that genetic determinants of development are necessary but not sufficient. A gene may ‘program’ a particular bit of behaviour ‘without it being the only thing to do so’. He goes on:

Dawkins accepts all this but then reveals his uncertainty about which language he is using by immediately giving special status back to the gene as the programmer. Consider a case in which the ambient environmental temperature during development is crucial for the expression of a particular phenotype. If the temperature changes by a few degrees the survival machine is beaten by another one. Would not that give as much status to a necessary temperature value as to a necessary gene? The temperature value is also required for the expression of a particular phenotype. It is also stable (within limits) from one generation to the next. It may even be transmitted from one generation to the next if the survival machine makes a nest for its offspring. Indeed, using Dawkins’ own style of teleological argument one could claim that the bird is the nest’s way of making another nest [Bateson 1978].

I replied to Bateson, but did so too briefly, picking on the last remark about birds’ nests and saying, ‘A nest is not a true replicator because a [non-genetic] “mutation” which occurs in the construction of a nest, for example the accidental incorporation of a pine needle instead of the usual grass, is not perpetuated in future “generations of nests”. Similarly, protein molecules are not replicators, nor is messenger RNA’ (Dawkins 1978a). Bateson had taken the catchphrase about a bird being a gene’s way of making another gene, and inverted it, substituting ‘nest’ for ‘gene’. But the parallel is not a valid one. There is a causal arrow going from gene to bird, but none in the reverse direction. A changed gene may perpetuate itself better than its unmutated allele. A changed nest will do no such thing unless, of course, the change is due to a changed gene, in which case it is the gene that is perpetuated, not the nest. A nest, like a bird, is a gene’s way of making another gene.

Bateson is worried that I seem to give ‘special status’ to genetic determinants of behaviour. He fears that an emphasis on the gene as the entity for whose benefit organisms labour, rather than the other way around, leads to an undue emphasis on the importance of genetic as opposed to environmental determinants of development. The answer to this is that when we are talking about
development
it is appropriate to emphasize non-genetic as well as genetic factors. But when we are talking about units of selection a different emphasis is called for, an emphasis on the properties of replicators.
The special status of genetic factors rather than non-genetic factors is deserved for one reason only: genetic factors replicate themselves, blemishes and all, but non-genetic factors do not.

Let us grant with both hands that the temperature in the nest housing a developing bird is important both for its immediate survival and for the way it develops and therefore for its long-term success as an adult. The immediate effects of gene products on the biochemical springs of development may, indeed, closely resemble the effects of temperature changes (Waddington 1957). We could even imagine the enzyme products of genes as little Bunsen burners, selectively applied at crucial nodes of the branching biochemical tree of embryonic causation, controlling development by selective control of biochemical reaction rates. An embryologist rightly sees no fundamental distinction between genetic and environmental causal factors, and he correctly regards each as necessary but not sufficient. Bateson was putting the embryologist’s point of view, and no ethologist is better qualified to do so. But I was not talking embryology. I was not concerned with the rival claims of determinants of development. I was talking about replicators surviving in evolutionary time, and Bateson certainly agrees that neither a nest, nor the temperature inside it, nor the bird that built it, are replicators. We can quickly see that they are not replicators by experimentally altering one of them. The change may wreak havoc on the animal, on its development and its chances of survival,
but the change will not be passed on to the next generation
. Now make a similar mutilation (mutation) to a gene in the germ-line: the change may or may not affect the bird’s development and its survival, but it
can
be passed on to the next generation; it can be replicated.

As is so often the case, an apparent disagreement turns out to be due to mutual misunderstanding. I thought that Bateson was denying proper respect to the Immortal Replicator. Bateson thought that I was denying proper respect to the Great Nexus of complex causal factors interacting in development. In fact, each of us was laying legitimate stress on considerations which are important for two different major fields of biology, the study of development and the study of natural selection.

An organism, then, is not a replicator, not even (despite Lewontin 1970a—see Dawkins 1982) a crude replicator with poor copying fidelity. It is therefore better not to speak of adaptations as being for the good of the organism. What about larger units, groups of organisms, species, communities of species, etc.? Some of these larger groupings are clearly subject to a version of the ‘internal fragmentation destroys copying fidelity’ argument. The fragmenting agent in this case is not the recombining effects of meiosis, but immigration and emigration, the destruction of the integrity of groups by the movement of individuals into and out of them. As I have put it before, they are like clouds in the sky or dust-storms in the desert. They are temporary aggregations or federations. They are not stable through
evolutionary time. Populations may last a long while, but they are constantly blending with other populations and so losing their identity. They are also subject to evolutionary change from within. A population is not a discrete enough entity to be a unit of natural selection, not stable and unitary enough to be ‘selected’ in preference to another population. But, just as the ‘fragmentation’ argument applied only to a subset of organisms, sexual ones, so it also applies only to a subset at the group level. It applies to groups capable of interbreeding, but it does not apply to reproductively isolated species.

Let us, then, examine whether species behave sufficiently like coherent entities, multiplying and giving rise to other species, to deserve to be called replicators. Note that that is not the same as Ghiselin’s (1974b) logical claim that species are ‘individuals’ (see also Hull 1976). Organisms, too, are individuals in Ghiselin’s sense, and I hope I have established that organisms are not replicators. Do species, or, to be more precise, do reproductively isolated gene-pools, really answer to the definition of replicators?

It is important to remember that mere immortality is not a sufficient qualification. A lineage, such as a sequence of parents and offspring from the long-unchanged brachiopod genus
Lingula
, is unending in the same sense, and to the same extent, as a lineage of genes. Indeed, for this example we perhaps need not have chosen a ‘living fossil’ like
Lingula
. Even a rapidly evolving lineage can, in a sense, be treated as an entity which is either extinct or extant at any moment in geological time. Now, certain kinds of lineage may be more likely to go extinct than others, and we may be able to discern statistical laws of extinction. For example, lineages whose females reproduce asexually may be systematically more or less likely to go extinct than lineages whose females stick to sex (Williams 1975; Maynard Smith 1978a). It has been suggested that ammonite and bivalve lineages with a high rate of evolving larger size (i.e. with a high rate of obeying Cope’s Rule) are more likely to go extinct than more slowly evolving lineages (Hallam 1975). Leigh (1977) makes some excellent points about differential lineage extinction, and its relationship to lower levels of selection: ‘… those species are favored where selection within populations works more nearly for the good of the species’. Selection ‘… favors species that have, for whatever reason, evolved genetic systems where a gene’s selective advantage more nearly matches its contribution to fitness’. Hull (1980a,b) is particularly clear about the logical status of the lineage, and about its distinction from the replicator and the interactor (Hull’s name for what I am calling the ‘vehicle’).

Differential lineage extinction, though technically a form of selection, is not enough in itself to generate progressive evolutionary change. Lineages may be ‘survivors’, but this does not make them replicators. Grains of sand
are survivors. Hard grains, made of quartz or diamond, will last longer than soft grains made of chalk. But nobody has ever invoked hardness selection among sand grains as the basis for an evolutionary progression. The reason, fundamentally, is that grains of sand do not multiply. One grain may survive a long time, but it does not multiply and make copies of itself. Do species, or other groups of organisms, multiply? Do they replicate?

Alexander and Borgia (1978) assert that they do, and that they are therefore true replicators: ‘Species give rise to species; species multiply.’ The best case I can make for regarding species, or rather their gene-pools, as multiplying replicators arises from the theory of ‘species selection’ associated with the palaeontological idea of ‘punctuated equilibria’ (Eldredge & Gould 1972; Stanley 1975, 1979; Gould & Eldredge 1977; Gould 1977c, 1980a,b; Levinton & Simon 1980). I will take some time to discuss this body of theory, since ‘species selection’ is very relevant to this chapter. Another reason for taking the time is that I regard the suggestions of Eldredge and Gould as of great interest to biology generally, but I am anxious that they should not be oversold as more revolutionary than they actually are. Gould and Eldredge (1977, p. 117) are themselves conscious of this danger, though for different reasons.

My fear stems from the growing influence of a vigilant corps of lay critics of Darwinism, either religious fundamentalists or Shavian/Koestlerian Lamarckists who, for reasons that have nothing to do with science, eagerly seize upon anything that, with imperfect understanding, can be made to sound anti-Darwinian. Journalists are often only too ready to pander to the unpopularity of Darwinism in some lay circles. One of Britain’s least disreputable daily newspapers (
The Guardian
, 21 November 1978) served up a journalistically garbled but still just recognizable version of the Eldredge/Gould theory in a leading article, as evidence that all is not well with Darwinism. Predictably, this elicited some uncomprehending fundamentalist glee in the letter columns of the paper, some of it from disquietingly influential sources, and the public could well have been left with the impression that even ‘the scientists’ themselves now have doubts about Darwinism. Dr Gould informs me that
The Guardian
did not favour him with a reply to his letter of protest. Another British newspaper,
The Sunday Times
(8 March 1981), in a much longer article called ‘The new clues that challenge Darwin’, sensationally exaggerated the difference between the Eldredge/Gould theory and other versions of Darwinism. The British Broadcasting Corporation also got in on the act around the same time, in two separate programmes made by rival production teams. They were called
The Trouble with Evolution
and
Did Darwin get it Wrong?
, and they differed hardly at all except that one had Eldredge and the other had Gould! The second programme actually went to the lengths of digging up some
fundamentalists to comment on the Eldredge/Gould theory: not surprisingly, the ill-understood appearance of dissension within the ranks of Darwinists was meat and drink to them.

Journalistic standards are not unknown in learned periodicals too.
Science
(Vol. 210, pp. 883–887, 1980) reported on a recent conference on macroevolution under the dramatic heading, ‘Evolutionary theory under fire’, and with the equally sensational subtitle, ‘An historic conference in Chicago challenges the four-decade long dominance of the Modern Synthesis’ (see criticisms by Futuyma
et al
. 1981). As Maynard Smith is quoted as saying at the same conference, ‘You are in danger of preventing understanding by suggesting that there is intellectual antagonism where none exists’ (see also Maynard Smith 1981). In the face of all the ballyhoo, I am anxious to be very clear about, to quote one of their own section headings, exactly ‘What Eldredge and Gould Did Not (And Did) Say’.