The Extended Phenotype: The Long Reach of the Gene (Popular Science) (37 page)

Neither Eberhard nor Cosmides and Tooby explicitly justify or document the genes’-eye view of life: they simply
assume
it: ‘The recent shift towards viewing the gene as the unit of selection, coupled with a recognition of the different modes of genetic inheritance makes the concept of parasitism, symbiosis, conflict, cooperation, and coevolution—which were developed with reference to whole organisms—relevant to genes within an organism’ (Cosmides & Tooby). These papers have what I can only describe as the flavour of post-revolutionary normal science (Kuhn 1970).

The reader may remark that we have come thus far with scarcely a mention of ‘fitness’. This was deliberate. I have misgivings about the term, but I have been holding my fire. Several of the earlier chapters have been aimed, in their different ways, at exposing the weaknesses in the individual organism’s candidacy for the title of optimon, the unit for whose benefit adaptations may be said to work. ‘Fitness’, as it is normally used by ecologists and ethologists, is a verbal trick, a device contrived to make it possible to talk in terms of individuals, as opposed to true replicators, as beneficiaries of adaptation. The word is therefore a kind of verbal symbol of the position that I am trying to argue against. More than that, the word is actively confusing because it has been used in so many different ways. It is therefore fitting to end the critical section of the book with a discussion of fitness.

Herbert Spencer’s (1864) term ‘survival of the fittest’ was adopted by Darwin (1866) at the urging of Wallace (1866). Wallace’s argument makes fascinating reading today, and I cannot resist quoting him at some length:

My dear Darwin,—I have been so repeatedly struck by the utter inability of numbers of intelligent persons to see clearly, or at all, the self-acting and necessary effects of Natural Selection, that I am led to conclude that the term itself, and your mode of illustrating it, however clear and beautiful to many of us, are yet not the best adapted to impress it on the general naturalist public … in Janet’s recent work on the ‘Materialism of the Present Day’ … he considers your weak point to be that you do not see that ‘thought and direction are essential to the action of Natural Selection’. The same objection has been made a score of times by your chief opponents, and I have heard it as often stated myself in conversation. Now, I think this arises almost entirely from your choice of the term Natural Selection, and so constantly comparing it in its effects to man’s selection, and also to
your so frequently personifying nature as ‘selecting’, as ‘preferring’, as ‘seeking only the good of the species’, etc., etc. To the few this is as clear as daylight, and beautifully suggestive, but to many it is evidently a stumbling block. I wish, therefore, to suggest to you the possibility of entirely avoiding this source of misconception in your great work (if now not too late), and also in any future editions of the ‘Origin’, and I think it may be done without difficulty and very effectually by adopting Spencer’s term (which he generally uses in preference to Natural Selection), viz. ‘Survival of the Fittest’. This term is the plain expression of the fact; ‘Natural Selection’ is a metaphorical expression of it, and to a certain degree
indirect
and
incorrect
, since, even personifying Nature, she does not so much select special variations as exterminate the most unfavourable ones … [The Wallace-Darwin Correspondence].

It may seem hard to believe that anyone could have been misled in the way that Wallace indicates, but Young (1971) provides ample evidence confirming that Darwin’s contemporaries often were so misled. Even today the confusion is not unknown, and an analogous muddle arises over the catch-phrase ‘selfish gene’: ‘This is an ingenious theory but far-fetched. There is no reason for imputing the complex emotion of selfishness to molecules’ (Bethell 1978); ‘Genes cannot be selfish or unselfish, any more than atoms can be jealous, elephants abstract or biscuits teleological’ (Midgley 1979; see reply in Dawkins 1981).

Darwin (1866) was impressed by Wallace’s letter, which he found ‘as clear as daylight’, and he resolved to incorporate ‘survival of the fittest’ into his writings, although he cautioned that ‘the term Natural Selection has now been so largely used abroad and at home that I doubt whether it could be given up, and with all its faults I should be sorry to see the attempt made. Whether it will be rejected must now depend on the “survival of the fittest” …’ (Darwin clearly understood the ‘meme’ principle). ‘As in time the term must grow intelligible, the objections to its use will grow weaker and weaker. I doubt whether the use of any term would have made the subject intelligible to some minds … As for M. Janet, he is a metaphysician, and such gentlemen are so acute that I think they often misunderstand common folk.’

What neither Wallace nor Darwin could have foreseen was that ‘survival of the fittest’ was destined to generate more serious confusion than ‘natural selection’ ever had. A familiar example is the attempt, rediscovered with almost pathetic eagerness by successive generations of amateur (and even professional) philosophers (‘so acute that they misunderstand common folk’?), to demonstrate that the theory of natural selection is a worthless tautology (an amusing variant is that it is unfalsifiable and therefore false!).
In fact the illusion of tautology stems entirely from the phrase ‘survival of the fittest’, and not from the theory itself at all. The argument is a remarkable example of the elevation of words above their station, in which respect it resembles St Anselm’s ontological proof of the existence of God. Like God, natural selection is too big a theory to be proved or disproved by word-games. God and natural selection are, after all, the only two workable theories we have of why we exist.

Briefly, the tautology idea is this. Natural selection is defined as the survival of the fittest, and the fittest are defined as those that survive. Therefore the whole of Darwinism is an unfalsifiable tautology and we don’t have to worry our heads about it any more. Fortunately, several authoritative replies to this whimsical little conceit are available (Maynard Smith 1969; Stebbins 1977; Alexander 1980), and I need not labour my own. I will, however, chalk up the tautology idea on my list of muddles attributable to the concept of fitness.

It is, as I have said, a purpose of this chapter to show that fitness is a very difficult concept, and that there might be something to be said for doing without it whenever we can. One way I shall do this is to show that the word has been used by biologists in at least five different senses. The first and oldest meaning is the one closest to everyday usage.

When Spencer, Wallace and Darwin originally used the term ‘fitness’, the charge of tautology would not have occurred to anyone. I shall call this original usage fitness[1]. It did not have a precise technical meaning, and the fittest were not
defined
as those that survive. Fitness meant, roughly, the capacity to survive and reproduce, but it was not defined and measured as precisely synonymous with reproductive success. It had a range of specific meanings, depending upon the particular aspect of life that one was examining. If the subject of attention was efficiency in grinding vegetable food, the fittest individuals were those with the hardest teeth or the most powerful jaw muscles. In different contexts the fittest individuals would be taken to mean those with the keenest eyes, the strongest leg muscles, the sharpest ears, the swiftest reflexes. These capacities and abilities, along with countless others, were supposed to improve over the generations, and natural selection effected that improvement. ‘Survival of the fittest’ was a general characterization of these particular improvements. There is nothing tautological about that.

It was only later that fitness was adopted as a technical term. Biologists thought they needed a word for that hypothetical quantity that tends to be maximized as a result of natural selection. They could have chosen ‘selective potential’, or ‘survivability’, or ‘
W
’ but in fact they lit upon ‘fitness’. They did the equivalent of recognizing that the definition they were seeking must
be ‘whatever it takes to make the survival of the fittest into a tautology’. They redefined fitness accordingly.

But the tautology is not a property of Darwinism itself, merely of the catchphrase we sometimes use to describe it. If I say that a train travelling at an average velocity of 120 m.p.h. will reach its destination in half the time it takes a train travelling at 60 m.p.h., the fact that I have uttered a tautology does not prevent the trains from running, nor does it stop us asking meaningful questions about what makes one train faster than the other: does it have a larger engine, superior fuel, a more streamlined shape, or what? The concept of velocity is
defined
in such a way as to make statements such as the one above tautologically true. It is this that makes the concept of velocity useful. As Maynard Smith (1969) witheringly put it: ‘Of course Darwinism contains tautological features: any scientific theory containing two lines of algebra does so.’ And when Hamilton (1975a), speaking of ‘survival of the fittest’, said that ‘accusations of tautology seem hardly fair on this small phrase itself’, he was putting it mildly. Given the purpose for which fitness was redefined, ‘survival of the fittest’
had
to become a tautology.

To redefine fitness in a special technical sense might have done no harm, other than to give some earnest philosophers a field day, but unfortunately its exact technical meaning has varied widely, and this has had the more serious effect of confusing some biologists too. The most precise and unexceptionable of the various technical meanings is that adopted by population geneticists.

For population geneticists, fitness is an operational measure, exactly defined in terms of a measurement procedure. The word is applied not really to a whole individual organism but to a genotype, usually at a single locus. The fitness
W
of a genotype, say
Aa
, may be defined as 1 –
s
, where
s
is the coefficient of selection against the genotype (Falconer 1960). It may be regarded as a measure of the number of offspring that a typical individual of genotype
Aa
is expected to bring up to reproductive age, when all other variation is averaged out. It is usually expressed relative to the corresponding fitness of one particular genotype at the locus, which is arbitrarily defined as 1. Then there is said to be selection, at that locus, in favour of genotypes with higher fitness, relative to genotypes with lower fitness. I shall call this special population geneticists’ meaning of the term fitness[2]. When we say that brown-eyed individuals are fitter than blue-eyed individuals we are talking about fitness[2]. We assume that all other variation among the individuals is averaged out, and we are, in effect, applying the word fitness to two genotypes at a single locus.

But while population geneticists are interested directly in changes in genotype frequencies and gene frequencies, ethologists and ecologists look at whole organisms as integrated systems that appear to be maximizing something. Fitness[3], or ‘classical fitness’, is a property of an individual organism, often expressed as the product of survival and fecundity. It is a measure of the individual’s reproductive success, or its success in passing its genes on to future generations. For instance, as mentioned in
Chapter 7
, Clutton-Brock
et al
. (1982) are conducting a long-term study of a red deer population on the island of Rhum, and part of their aim is to compare the lifetime reproductive successes or fitness[3] of identified individual stags and hinds.

Notice the difference between the fitness[3] of an individual and the fitness[2] of a genotype. The measured fitness[2] of the brown-eyed genotype will contribute to the fitness[3] of an individual who happens to have brown eyes, but so will the fitness[2] of his genotype at all other loci. Thus the fitness[2] of a genotype at a locus can be regarded as an average of the fitness[3]s of all individuals possessing that genotype. And the fitness[3] of an individual can be regarded as influenced by the fitness[2] of his genotype, averaged over all his loci (Falconer 1960).

It is easy to measure the fitness[2] of a genotype at a locus, because each genotype,
AA, Aa
, etc., occurs a countable number of times in successive generations in a population. But the same is not true of the fitness[3] of an organism. You can’t count the number of times an organism occurs in successive generations, because he only occurs once, ever. The fitness[3] of an organism is often measured as the number of his offspring reared to adulthood, but there is some dispute over the usefulness of this. One problem is raised by Williams (1966) criticizing Medawar (1960) who had said: ‘The genetical usage of “fitness” is an extreme attenuation of the ordinary usage: it is, in effect, a system of pricing the endowments of organisms in the currency of offspring, i.e., in terms of net reproductive performance. It is a genetic valuation of goods, not a statement about their nature or quality.’ Williams is worried that this is a retrospective definition, suitable for particular individuals who have existed. It suggests a posthumous evaluation of particular animals as ancestors, not a way of evaluating the qualities that can be expected to make for success in general. ‘My main criticism of Medawar’s statement is that it focuses attention on the rather trivial problem of the degree to which an organism actually achieves reproductive survival. The central biological problem is not survival as such, but design for survival’ (Williams 1966, p. 158). Williams is, in a sense, hankering after the pre-tautological virtues of fitness[1], and there is much to be said in his favour. But the fact is that fitness[3] has become widely used by biologists in
the sense described by Medawar. Medawar’s passage was addressed to laymen and was surely an attempt to enable them to follow standard biological terminology while avoiding the otherwise inevitable confusion with common-usage ‘athletic’ fitness.