The Extended Phenotype: The Long Reach of the Gene (Popular Science) (38 page)

The concept of fitness has the power to confuse even distinguished biologists. Consider the following misunderstanding of Waddington (1957) by Emerson (1960). Waddington had used the word ‘survival’ in the sense of reproductive survival or fitness[3]: ‘… survival does not, of course, mean the bodily endurance of a single individual … that individual “survives” best which leaves most offspring’. Emerson quotes this, then goes on: ‘Critical data on this contention are difficult to find, and it is likely that much new investigation is needed before the point is either verified or refuted.’ For once, the ritual lip-service to the need for more research is utterly inappropriate. When we are talking about matters of definition, empirical research cannot help us. Waddington was clearly
defining
survival in a special sense (the sense of fitness[3]), not making a proposition of fact subject to empirical verification or falsification. Yet Emerson apparently thought Waddington was making the provocative statement that those individuals with the highest capacity to survive tend also to be the individuals with the largest number of offspring. His failure to grasp the technical concept of fitness[3], is indicated by another quotation from the same paper: ‘It would be extremely difficult to explain the evolution of the uterus and mammary glands in mammals … as the result of natural selection of the fittest individual.’ In accordance with the influential Chicago-based school of thought of which he was a leader (Allee, Emerson
et al
. 1949), Emerson used this as an argument in favour of group selection. Mammary glands and uteruses were, for him, adaptations for the continuation of the species.

Workers who correctly use the concept of fitness[3] admit that it can be measured only as a crude approximation. If it is measured as the number of children born it neglects juvenile mortality and fails to account for parental care. If it is measured as number of offspring reaching reproductive age it neglects variation in reproductive success of the grown offspring. If it is measured as number of grandchildren it neglects … and so on
ad infinitum
. Ideally we might count the relative number of descendants alive after some very large number of generations. But such an ‘ideal’ measure has the curious property that, if carried to its logical conclusion, it can take only two values; it is an all-or-none measure. If we look far enough into the future, either I shall have no descendants at all, or all persons alive will be my descendants (Fisher 1930a). If I am descended from a particular individual male who lived a million years ago, it is virtually certain that you are descended from him too. The fitness of any particular long-dead individual, as measured in present-day descendants, is either zero or total. Williams would presumably say that if this is a problem it is so only for people that
wish to measure the
actual
reproductive success of particular individuals. If, on the other hand, we are interested in qualities that tend, on average, to make individuals
likely
to end up in the set of ancestors, the problem does not arise. In any case a more biologically interesting shortcoming of the concept of fitness[3] has led to the development of two newer usages of the technical term fitness.

Hamilton (1964a,b), in a pair of papers which we can now see to have marked a turning point in the history of evolutionary theory, made us aware of an important deficiency in classical fitness[3], the measure based on the reproductive success of an organism. The reason reproductive success matters, as opposed to mere individual survival, is that reproductive success is a measure of success in passing on genes. The organisms we see around us are descended from ancestors, and they have inherited some of the attributes that made those individuals ancestors as opposed to non-ancestors. If an organism exists it contains the genes of a long line of successful ancestors. The fitness[3] of an organism is its success as an ancestor, or, according to taste, its capacity for success as an ancestor. But Hamilton grasped the central importance of what, previously, had been only glancingly referred to in stray sentences of Fisher (1930a) and Haldane (1955). This is that natural selection will favour organs and behaviour that cause the individual’s genes to be passed on, whether or not the individual is, himself, an ancestor. An individual that assists his brother to be an ancestor may thereby ensure the survival in the gene-pool of the genes ‘for’ brotherly assistance. Hamilton saw that parental care is really only a special case of caring for close relatives with a high probability of containing the genes for caring. Classical fitness[3], reproductive success, was too narrow. It had to be broadened to
inclusive fitness
, which will here be called fitness[4].

It is sometimes supposed that the inclusive fitness of an individual is his own fitness[3] plus half the fitnesses[3] of each brother plus one-eighth of the fitness[3] of each cousin, etc. (e.g. Bygott
et al
. 1979). Barash (1980) explicitly defines it as ‘the sum of individual fitness (reproductive success) and the reproductive success of an individual’s relatives, with each relative devalued in proportion as it is more distantly related’. This would not be a sensible measure to try to use, and, as West-Eberhard (1975) emphasizes, it is not the measure Hamilton offered us. The reason it would not be sensible can be stated in various ways. One way of putting it is that it allows children to be counted many times, as though they had many existences (Grafen 1979). Then again, if a child is born to one of a set of brothers, the inclusive fitness of all the other brothers would, according to this view, immediately rise an equal notch, regardless whether any of them lifted a finger to feed the
infant. Indeed the inclusive fitness of another brother yet unborn would theoretically be increased by the birth of his elder nephew. Further, this later brother could be aborted shortly after conception and still, according to this erroneous view, enjoy a massive ‘inclusive fitness’ through the descendants of his elder brothers. To push to the
reductio ad absurdum
, he needn’t even bother to be conceived, yet still have a high ‘inclusive fitness’!

Hamilton clearly saw this fallacy, and therefore his concept of inclusive fitness was more subtle. The inclusive fitness of an organism is not a property of himself, but a property of his actions or effects. Inclusive fitness is calculated from an individual’s own reproductive success plus his
effects
on the reproductive success of his relatives, each one weighed by the appropriate coefficient of relatedness. Therefore, for instance, if my brother emigrates to Australia, so I can have no effect, one way or the other, on his reproductive success, my inclusive fitness does not go up each time he has a child!

Now ‘effects’ of putative causes can only be measured by comparison with other putative causes, or by comparison with their absence. We cannot, then, think of the effects of individual A on the survival and reproduction of his relatives in any absolute sense. We could compare the effects of his choosing to perform act X rather than act Y. Or we could take the effects of his lifetime’s set of deeds and compare them with a hypothetical lifetime of total inaction—as though he had never been conceived. It is this latter usage that is normally meant by the inclusive fitness of an individual organism.

The point is that inclusive fitness is not an absolute property of an organism in the same way as classical fitness[3] could in theory be, if measured in certain ways. Inclusive fitness is a property of a triple consisting of an organism of interest, an act or set of acts of interest, and an alternative set of acts for comparison. We aspire to measure, then, not the absolute inclusive fitness of the organism I, but the effect on I’s inclusive fitness of his doing act X in comparison with his doing act Y. If ‘act’ X is taken to be I’s entire life story, Y may be taken as equivalent to a hypothetical world in which I did not exist. An organism’s inclusive fitness, then, is defined so that it is not affected by the reproductive success of relatives on another continent whom he never meets and whom he has no way of affecting.

The mistaken view that the inclusive fitness of an organism is a weighted sum of the reproductive successes of all its relatives everywhere, who have ever lived, and who will ever live, is extremely common. Although Hamilton is not responsible for the errors of his followers, this may be one reason why many people have so much difficulty dealing with the concept of inclusive fitness, and it may provide a reason for abandoning the concept at some time in the future. There is yet a fifth meaning of fitness, which was designed to avoid this particular difficulty of inclusive fitness, but which has difficulties of its own.

Fitness[5] is ‘personal fitness’ in the sense of Orlove (1975, 1979). It can be thought of as a kind of backwards way of looking at inclusive fitness. Where inclusive fitness[4] focuses on the effects the individual of interest has on the fitness[3] of his relatives, personal fitness[5] focuses on the effects that the individual’s relatives have on his fitness[3]. The fitness[3] of an individual is some measure of the number of his offspring or descendants. But Hamilton’s logic has shown us that we may expect an individual to end up with more offspring then he could rear himself, because his relatives contribute towards rearing some of his offspring. An animal’s fitness[5] may be briefly characterized as ‘the same as his fitness[3] but don’t forget that this must include the extra offspring he gets as a result of help from his relatives’

The advantage, in practice, of using personal fitness[5] over inclusive fitness[4] is that we end up simply counting offspring, and there is no risk of a given child’s being mistakenly counted many times over. A given child is a part of the fitness[5] of his parents only. He potentially corresponds to a term in the inclusive fitness[4] of an indefinite number of uncles, aunts, cousins, etc., leading to a danger of his being counted several times (Grafen 1979; Hines & Maynard Smith 1979).

Inclusive fitness[4] when properly used, and personal fitness[5], give equivalent results. Both are major theoretical achievements and the inventor of either of them would deserve lasting honour. It is entirely characteristic that Hamilton himself quietly invented both in the same paper, switching from one to another with a swiftness that bewildered at least one later author (Cassidy 1978, p. 581). Hamilton’s (1964a) name for fitness[5] was ‘neighbour-modulated fitness’. He considered that its use, though correct, would be unwieldy, and for this reason he introduced inclusive fitness[4] as a more manageable alternative approach. Maynard Smith (1982) agrees that inclusive fitness[4] is often easier to use than neighbour-modulated fitness[5], and he illustrates the point by working through a particular hypothetical example using both methods in turn.

Notice that both these fitnesses, like ‘classical’ fitness[3], are firmly tied to the idea of the individual organism as ‘maximizing agent’. It is only partly facetiously that I have characterized inclusive fitness as ‘that property of an individual organism which will appear to be maximized when what is really being maximized is gene survival’ (Dawkins 1978a). (One might generalize this principle to other ‘vehicles’. A group selectionist might define his own version of inclusive fitness as ‘that property of a
group
which will appear to be maximized when what is really being maximized is gene survival’!)

Historically, indeed, I see the concept of inclusive fitness as the instrument of a brilliant last-ditch rescue attempt, an attempt to save the individual organism as the level at which we think about natural selection. The underlying spirit of Hamilton’s (1964) papers on inclusive fitness is gene
selectionist. The brief note of 1963 which preceded them is explicitly so: ‘Despite the principle of “survival of the fittest” the ultimate criterion that determines whether
G
will spread is not whether the behavior is to the benefit of the behaver but whether it is to the benefit of the gene
G
…’ Together with Williams (1966), Hamilton could fairly be regarded as one of the fathers of gene selectionism in modern behavioural and ecological studies:

A gene is being favored in natural selection if the aggregate of its replicas forms an increasing fraction of the total gene pool. We are going to be concerned with genes supposed to affect the social behavior of their bearers, so let us try to make the argument more vivid by attributing to the genes, temporarily, intelligence and a certain freedom of choice. Imagine that a gene is considering the problem of increasing the number of its replicas and imagine that it can choose between causing purely self-interested behavior by its bearer A (leading to more reproduction by A) and causing ‘disinterested’ behavior that benefits in some way a relative, B [Hamilton 1972].

Having made use of his intelligent gene model, Hamilton later explicitly abandons it in favour of the inclusive fitness effect of an
individual
on the propagation of copies of his genes. It is part of the thesis of this book that he might have done better to have stuck by his ‘intelligent gene’ model. If individual organisms can be assumed to work for the aggregate benefit of all their genes, it doesn’t matter whether we think in terms of genes working to ensure their survival, or of individuals working to maximize their inclusive fitness. I suspect that Hamilton felt more comfortable with the individual as the agent of biological striving, or perhaps he surmised that most of his colleagues were not yet ready to abandon the individual as agent. But, of all the brilliant theoretical achievements of Hamilton and his followers, which have been expressed in terms of inclusive fitness[4] (or personal fitness[5]), I cannot think of any that could not have been more simply derived in terms of Hamilton’s ‘intelligent gene’, manipulating bodies for its own ends (Charnov 1977).

Individual-level thinking is superficially attractive because individuals, unlike genes, have nervous systems and limbs which render them capable of working in obvious ways to maximize something. It is therefore natural to ask what quantity, in theory, they might be expected to maximize, and inclusive fitness is the answer. But what makes this so dangerous is that it, too, is really a metaphor. Individuals do not consciously strive to maximize anything; they behave
as if
maximizing something. It is exactly the same ‘as if’ logic that we apply to ‘intelligent genes’. Genes manipulate the world as if
striving to maximize their own survival. They do not really ‘strive’, but my point is that in this respect they do not differ from individuals. Neither individuals nor genes really strive to maximize anything. Or, rather, individuals may strive for something, but it will be a morsel of food, an attractive female, or a desirable territory, not inclusive fitness. To the extent that it is useful for us to think of individuals working as if to maximize fitness, we may, with precisely the same licence, think of genes as if they were striving to maximize their survival. The difference is that the quantity the genes may be thought of as maximizing (survival of replicas) is a great deal simpler and easier to deal with in models than the quantity individuals may be thought of as maximizing (fitness). I repeat that if we think about individual animals maximizing something, there is a serious danger of our confusing ourselves, since we may forget whether we are using ‘as if’ language or whether we are talking about the animals consciously striving for some goal. Since no sane biologist could imagine DNA molecules consciously striving for anything, the danger of this confusion ought not to exist when we talk of genes as maximizing agents.