Adaptation and Evolutionary Theory
Robert N. Brandon
There is virtually universal disagreement among students of evolution as to the meaning of adaptation. (Lewontin, 1957)
Much of past and current disagreement on adaptation centers about the , definition of the concept and its application to particular examples: these argu- ments would lessen greatly ifprecise definitions for adaptations were available. (Bock and von Wahlert, 1965)
The development of a predictive theory [of evolution] depends on being able to specify when a population is in better or worse evolutionary state. For this purpose an objective definition of adaptedness is necessary. (Slobodkin, 1968)
The conception of adaptation was not introduced adequate definition of relative adaptedness. As we into biology in 1859, Rather what Darwin did will see such analysis cannot be divorced from an was to offer a radically new type of explanation analysis of the structure of evolutionary theory. of adaptations and in so doing he altered the The other major aim of this paper is to expose conception. As the above quotes indicate we have this structure, to show how it differs from the not in the last century sufficiently delimited this standard philosophical models of scientific the- conception and it is important to do so. ories, and to defend this differentiating feature In this paper we will analyse and, I hope, (and hence to show the inadequacy of certain clarify one aspect of the conception of adaptation. views about the structure of scientific theories One of the aims of this paper is a theoretically which purport to be con~plete).
Reprinted from Robert Brandon, Studies in the History and Philosophy of Science, Vol. 9, Adaptation and Evolutionary Theory, pp. 9, 181-206. Copyright 1978, with permission from Elsevier. I owe a debt of gratitude to all those who read earlier versions of this paper and helped me improve it. Where possible I have tried to footnote contributions. Here I want to give special thanks to Ernst Mayr and Paul Ziff whose comments and criticisms have had pervasive effects on the evolution of this paper. 104 ROBERT N. BRANDON
A note on defining is needed. Definitions are occurrence in nature is controversial. One could often thought to be of two kinds, descriptive and speak of an abstract theory of evolution which stipulative. (See, for example, I-Iempel (1966), covers natural selection, group selection and even chapter 7.) Descriptive definitions simply describe the selection of tin cans in junk yards. But most the meaning of terms already in use; stipulative of the interesting problems don't arise at this level definitions assign, by stipulation, special mean- of generality. In this paper we will be primarily ing to a term (either newly coined or previously concerned with natural selection, i.e. with intra- existing). According to this view the project of specific intraenvironmental selection. Thus we will defining a term is either purely descriptive or be concerned with the adaptedness of individual purely stipulative. This view is mistaken. The organisms, not with the adaptedness of populations. project at hand calls for neither pure linguistic Let me illustrate the confusion that results analysis nor pure stipulation; it is much more com- from the failure to relate adaptedness to the plex. Briefly, we examine the conceptual network proper level of selection. One of the more prom- of evolutionary biology. We find that according inent definitions of relative adaptedness is due to evolutionary theory there is a biological prop- to Thoday.' Basically it says: a is better adapted erty, adaptedness, which some organisms have than b if and only if a is more likely than b to more of than others. Those having more of it, have offspring surviving 10' (or some other large or those better adapted, tend to leave more off- number) years from now. Either the long-range spring. And this is the mechanism of evolution. probability of offspring corresponds to the short- The project calls for conceptual analysis but range probability of offspring or it does not. such analysis is sterile unless it is coupled with (Corresponds means: a's long-range probability an examination of the biological property which of offspring is greater than b's long-range prob- is the object of the conception. Any definition ability of offspring if and only if a's short- which fails to fit the conceptual network must range probability of offspring is greater than b's be rejected, as must any which fails to apply to short-range probability of offspring.) If it does the property. The project calls for an element correspond then we should stick to the more of stipulation but our stipulatory freedom is easily measurable short-range probability. If not, constrained both by theoretical and conceptual then since natural selection is not foresighted, i.e. requirements and, one hopes, by the real world. it operates only on the differential adaptedness A note on the restricted scope of this paper is of present organisms to present environments, the also needed. Biologists talk about the adaptecl- long-range probability of offspring is irrelevant to ness of individual organisms and of populations. natural selection. Selection occurs at the level of individuals and, Why has Thoday's definition been so favorably presumably, at higher levels. That is, there is received? Because the long-range probability intrapopulational selection and interpop~~lational of descendants is important to selection at or selection. It is vital that we keep these levels above the species level. For instance, one plaus- separate and that we see the relation between ible explanation of the predominance of sexual selection and adaptation.' Selection at the level of reproduction over asexual modes of reproduction individual organisms has as its cause differences is that the long-range chances of survival are in individual adaptedness and its effect is adap- greater for populations having sex (see Maynard tions for individual organisms. We will follow Smith, 1975, pp. 185ff). But if one is interested standard practice in calling selection at this level in selection at the population level then the natural selection. Any benefit to the population relevant notion of adaptedness would be that from natural selection is purely fortuitous. One which applies to populations. Until recently even must distinguish between a group of adapted biologists have failed to distinguish intra- and organisms and an adapted group of organisms. inter-populational selection. Thoday's definition, For instance, a herd of fleet gazelles is not neces- not being selection relative, lends itself to this sarily a fleet herd of gazelles. Similarly group confusion. To keep matters as clear as possible we selection will have as its cause differences in group will only be concerned with natural selection and adaptedness and as its effect group adaptations. with that notion of adaptation which properly The theory of group selection is quite clear; its relates to it. ADAPTATION AND EVOLUTIONARY THEORY 105
1. The Role of the Concept of Relative that there is variation, (I), and that some of the Adaptedness in Evolutionary Theory traits which vary are heritable, (2), it follows that the variation within a species tends to be preserved. The following three statements are crucial coin- (Of course this tendency can be counterbalanced ponents of the Darwinian (or neo-Darwinian) by other factors.) theory of evol~tion:~ When (3) holds, when there are differences in reproductive rates, it follows from (1) and (2) 1. Variation: There is (significant) variation in that the variation status quo is disrupted, that is, morphological, physiological and behavioral that there are changes in the patterns of variation traits among members of a species. within the species. For our purposes we can count 2. Heredity: Some traits are heritable so that such changes as evolution. (For a fuller explica- individuals resemble their relations more tion of the concept of evolution see Brandon, than they resemble unrelated individuals and, 1978.) Thus when (1)-(3) hold evolution occurs. in particular, offspring resemble their parents. We have seen that (1) is in a sense trivial and 3. Differential Fitness: Different variants (or requires no explanation. We have also seen that different types of organisms) leave different (2) is non-trivial and is to be explained by mod- numbers of offspring in immediate or re- ern theories of genetics, but that this explanation mote generations. is not essential to Darwinian theory. In contrast, the distinguishing feature of a Darwinian theory When the conditions described above are of evolution is its explanation of (3).4 The focus satisfied organic evolution occurs. A thorough of this paper is the conception used for such examination into the history of our awareness explanations. of these conditions would be interesting and The distinguishing feature of a Darwinian worthwhile but will not be attempted here (see theory of evolution is explaining evolutionary Mayr, 1977). Suffice it to say that in Darwin's time change by a theory of natural selection. Of course, each was a non-trivial statement. In what follows that is not the only possible sort of explanation we will examine them predominantly from our of evolution. 111 his own time Darwin convinced own point of view. the majority of the scientific comn~unitythat Ignoring the parenthetical 'significant' (1) evolution has and does occur but hardly anyone could not help but be true. The uniqueness bought his natural-selection-explanation of it. of complex material systems is now taken for (For an excellent source book on the reception granted; and so we expect variation among of Darwin's theory see Hull, 1973.) The alternat- individuals of a species. Their similarity needs ives of Darwin's day, e.g. divine intervention and explaining not their variation. (1) becomes less the unfolding of some predetermined plan, are no empty from our point of view when 'significant' longer scientifically acceptable. But there is one is added. What sort of variation is significant? That present day alternative we should consider. which can lead to adaptive evolutionary changes. It is not surprising that in finite populations Though the world is such that individuals must of unique individuals some variants leave more be unique the recognition of this fact is of fairly offspring than others. We would expect such recent origins and is necessary for an evolution- differences in reproductive success simply from ary world view. chance. And if there are chance differences in Unlike (I), (2) is not at all trivial. There is no reproductive success between two types of nletaphysical necessity in offspring resembling organisms (or similarity classes of organisms) we their parents. (2) can now be derived from our expect one type ultimately to predominate by modern theories of genetics; in Darwin's time it what statisticians call random walk. If we can was an observation common to naturalists and explain (3) and so the occurrence of evolution in animal breeders. Darwin's theories of heredity terms of chance is the hypothesis of natural were notoriously muddled but fortunately a cor- selection necessary? rect theory of genetics is not a prerequisite for a It is becoming the received view in the philo- Darwinian theory of evolution (see Mayr, 1977, sophy of science that hypotheses are not evaluated p. 325). What is important to note is that given in isolation but rather in comparison with rival 106 ROBERT N. BRANDON hypotheses. This view is, I think, for the most part do not directly observe long term evolutionary correct but not entirely; some hypotheses we change. What we observe and try to explain are reject as unacceptable without comparison with the products of such change. Presumably any specific alternatives. Unacceptable hypotheses are complex feature of an organism is the product of those that violate deeper-seated beliefs, theories long term evolutionary change. On the one hand or metaphysics. Similarly some forms of explana- some complex features of organisms, such as the tion are unacceptable in that no investigation eye of a human, are so obviously useful to their into the particular phenomenon is required to possessor that we cannot believe that this useful- reject them. We reject them without considering ness plays no part in explaining their existence. any particular alternative explanation simply That is, given Darwinian theory and the obvious because we believe there must be a better altern- usefulness of sight we have a better alternative ative. For example, accepting Darwinian theory to the chance-explanation. On the other hand we reject the explanation that bees make honey there are features whose usefulness is unclear for in order to provide food for bears without exam- which we still reject chance-explanations because ining bees, bears or honey. (An acceptable form of their high degree of complexity and con- of explanation is not one which is necessarily stancy. Complexity and constancy are not made correct or even accepted; it simply is one which likely 011 the hypothesis of evolution by random is not unacceptable.) sampling. A good example is lateral lines in fish. The theory of evolution by chance or by This organ is structurally complex and shows random walk has been developed in recent years a structural constancy within taxa, yet until and is often called the theory of non-Darwinian recently it was not known how the lateral line was evolution, or better, the neutrality theory of useful to its possessor. In this case the rejection evolution (see King and Jukes, 1969). We cannot of a chance-explanation was good policy; studies give it the discussion it deserves but it is worth eventually showed that the lateral line is a sense pointing out that explanation in terms of chance organ of audition. (This example is taken from is an acceptable form of explaining short term G. C. Williams, 1966, pp. 10-11.) evolutionary change but not of any interesting sort One can contrast the lateral line in fish with the of long term evolutionary change. (The truth of tailless condition of Manx cats. This feature is this hinges on what counts as interesting. I will not even constant within the species and a non- not try to delimit interesting long term evolu- existent tail is hardly complex. (Actually what is tionary change; suffice it to say that any seemingly relevant concerning complexity is that the historical directed change is interesting.) process leading from tailed to tailless is most The neutrality theory supposes that certain probably not complex.) Furthermore legend has alternative alleles (and so certain protein molecules it that Manx cats originated on the Isle of Man coded by them) are functionally equivalent, i.e. in what would be a small isolated population; are selectively neutral. Given this supposition thus increasing the probable role of chance. The the neutrality theory predicts (and so is able to tailless condition of Manx cats may have evolved explain) the sorts of changes in frequencies of these by natural selection but for all we know the best alleles expected by a process of random sampling explanation of it is the explanation in terms of in different situations. As Ayala (1974) points chance. out these predictions differ both qualitatively It is important to keep in mind the possibility and quantitatively from those given by the selec- of evolution by random walk for it is important tionist theory. (Ayala presents data on different that Darwinian explanations be testably different species of Drosophila which tend to corroborate (at least in principle) from chance-explanations. the natural selectionist hypothesis and refute What is the Darwinian explanation of (3)? The the neutrality hypothesis.) Whether evolution by conventional wisdom is that Darwin explained random walk is a common or rare phenomenon (3) by his postulate of the 'struggle for existence' we cannot reject a priori a chance-explanation of (or in Spencer's words, which Darwin later short term evolutionary change. used, 'the survival of the fittest') and that this The situation is different for interesting long explanation, or this discovery of the mechanism term evolutionary phenomena. Of course we of evolution, was Darwin's greatest contribution. ADAPTATION AND EVOLUTIONARY THEORY 107
How does 'the struggle for existence' or 'the Certainly if (D) is a true law then the Darwinian survival of the fittest' explain (3)?Following cur- explanation is acceptable. Darwin seems to pre- rent practice let us define the reproductive success suppose (D) but it is not to be found stated or the Darwinian fitness of an organism in terms explicitly in the Origin. Nor is it to be found in of its actual genetic contribution to the next modern evolutionary works. But if one exam- generation. I will not try to make this definition ines work in modern evolutionary biology - the precise and con~plete.The genetic contribution to theorizing done, the inferences made, the expla- the next generation can usefully be identified with nations offered - one finds that (D) or soinetl~ing the number of sufficiently similar offspring when like (D) is required as the foundation of evolu- 'sufficiently similar' is sufficiently explicated. tionary theory. I take it that this conclusion will This would disallow, for example, sterile offspring be so ui~controversialthat it need not be further from counting towards Darwinian fitness. There supported by examining examples of evolution- are two options: either let the Darwinian fitness ary reasoning. But later in this paper we will of an individual equal its actual number of give some examples to show how (D) is to be sufficiently similar offspring or let the Darwinian employed. fitness of an individual equal the mean number Pl~ilosopl~ersof science talk about laws more of sufficiently similar offspring of members of often than they display actual examples of them. the similarity class to which it belongs. In either I11 particular many people have discussed whether case Darwinian fitness is defined in terms of or not 'the survival of the fittest' is a tautology numbers of actual offspring. I should point out without displaying son~etl~ingother than that that most biologists use the words 'fitness' and phrase which might be a tautology. (As for ex- 'adaptedness' interchangeably. In this paper 'fitness' ample J. J. C. Smart, 1963, p. 59.) The phrase itself, will only be used to refer to Darwinian fitness. not being a declarative sentence, could not be a Adaptedness, as we will see, cannot be identified tautology. An exception is Mary Willia~ns.~She has with Darwinian fitness. (3) says that Darwinian attempted to give a 'precise, concise and testable' fitness is correlated with certain morpl~ological, version of that phrase, and so has attempted to physiological or behavioral traits. Why is there this give a precise, concise and testable version of the correlation? Why is there differential fitness? fundamental law of evolutionary theory. Darwin's answer, which he arrived at after read- William defines the clan of a set Q as the ing Malthus' Essay on P~pulation,~was that since members of Q plus all their descendants. 011 a phy- in each generation more individuals are pro- logenetic tree the clan of Q would be those nodes duced than can survive to reproduce there is a which are in Q plus all nodes after them which struggle for existence. In this 'struggle' (which in are on a branch which passes through one of the its broadest sense is a struggle of the organism with original nodes. A subclan is either a whole clan its environment not just with other individuals, or a clan with one or more branches removed. see Darwin, 1859, p, 62) certain traits will render A Darwinian subclan is a subclan which is held an organism better adapted to its environment together by cohesive forces so that it acts as a unit than conspecifics with certain other traits. The with respect to selection (this crucial concept is better adapted individuals will tend to be fitter not defined by Williams; she takes it as primitive). i.e. produce more offspring) than the less well Informally Williams' version of the fundamental adapted. Why are those who happen to be the law of evolutionary theory states that for any fittest in fact the fittest? The Darwinian answer is: subclan Dl of any Darwinian subclan D, They are (for the most part) better adapted to their environment. If Dl is superior in fitness to the rest of D for sufficiently many generations . then the What does this explanation presuppose? It . . proportion of D, in D will increase during these seems to presuppose the following as a law of generations. (1970, p. 362) nature: (D) is a 'law'7 about properties of individual (D) If a is better adapted than b in environ- organisn~s;Williams' version is a law about ment E then (probably) a will have more properties of sets of organisms. Which is (sufficientlysimilar) offspring than b in E fundamental? Some properties of sets (notable 108 ROBERT N. BRANDON exceptions being set-theoretic properties such of the concept will satisfy all four desiderata. In as cardinality) are a function of the properties the final section I will attempt to draw the of the sets' members. In particular, as Williams ramifications of this result. herself points out (1973, p. 528), the fitness of a clan is to be identified with the average fitness (a) Independence of the members of the clan. Thus the property of individuals (or more precisely the property of The relational concept of adaptation is to explain individuals in some environment) -what we will differential fitness. To do so (D) must not be a call adaptedness, what Williams calls fitness - is tautology. Clearly if (D) is to be a scientific law fundamental. Likewise (D) is fundamental in rather than a tautology the relational concept of that Williams' law can be derived from it and the adaptation cannot be defined in terms of actual laws of population genetics but not vice versa. reproductive values. That is, we cannot define it Perhaps the only way of testing (D) is to apply it as follows: to fairly large populations and so to test some- a is better adapted than b in E iff a has more thing like Williams' law, but this does not change offspring than b in B our conclusion. (D) is required as the foundation of evolutionary theory. ('iff' is shorthand for 'if and only if'.) Most biologists treat 'fitness' and 'adaptedness' as synonymous and many define relational fitness 2. Four Desiderata of Definitions ill just this way. (See Stern, 1970, p. 47 where he of Relative Adaptedness quotes Simpson, Waddington, Lerner and ~a~r' to this effect. Stern approves of this definition.) We have seen the role the relational concept of They thus deprive evolutionary theory of its adaptedness is to play in a Darwinian theory of explanatory power. evolution: It is the explanatory concept in what To avoid turning (D) into a tautology it seems I have called the fundamental law of evolu- we must also avoid defining relative adaptedness tionary theory. Philosophers have not been able in terms of probable reproductive values. That is, to come up with a set of necessary and jointly the following definition also seems to render (D) sufficient conditions for scientific lawhood, but a tautology: there is wide agreement on some necessary con- a is better adapted than b in E iff a will prob- ditions. In particular laws of the empirical sciences ably have more offspring than b in E are to be empirically testable universal state- merits. It is also highly desirable, whether or not (See Munson, 1971, p. 211 for a definition of this definitionally necessary, that laws be empirically form; but he substitutes survival for reproductive correct or at least nearly true. One cannot just look values.) Actually things are not as simple as they at the surface logic of a statement in order to seem to be. Whether or not the above definition determine whether or not it is a scientific law (as makes (D) tautologous depends 011 the inter- done in Ruse, 1975). To determine whether (D) pretation of probability being used. More will is a scientific law we will have to look deeply into be said about this, but for the moment we may the conception of adaptation. My strategy is to try conclude the obvious: If the relational concept to construct a definition of relative adaptedness of adaptation is to play its explanatory role in that makes (D) a respectable scientific law. In evolutionary theory it must be defined so that this section I will argue that from any definition (D) does not become a tautology. We will call (construction, explication) of this concept we this requirement the condition of independence would want the following: (a) independence from actual reproductive values. from actual reproductive values; (b) generality; (c) episteinological applicability; and (d) empir- (b) Generality ical correctness. After arguing for the above desiderata I will show how current definitions As stated earlier we are primarily interested in fail to satisfy all four and then I will produce a intraspecific selection and so for the set of ordered general argument showing that no explication triple
There may be many features of organisn~s, will also fail (d)." We want our definition of such as strength, beauty or even longevity, which relative adaptedness to fit the facts of natural we will be disappointed to find out are not selection. We cannot accept a definition which invariably selected. In fact quite often there is no renders (D) false. selection for higher fec~ndity.~The best adapted To summarize, our strategy is to construct may not always be the strongest or the most a definition of relative adaptedness that makes beautiful or even the most prolific. But natural (D) a respectable scientific law (from the rece- selection, rather than personal or collective taste, ived point of view of philosophy of science). must be the ultimate crilerion against which we Requirement (a) is that (D) cannot be a tautology. test our explication of adaptedi~ess.~~If we define Requirement (b) is that (D) must be general, i.e. natural selection in terms of relative adaptedness universally applicable througl~outthe biosphere. (as we will, see below p. 111) then those selected Requirement (c) is that (D) not be so vague or will by definition be the better adapted. Yet it so obscure that we have 110 idea how to apply does not follow that those organisms with higher it to particular cases (or that (D) be testable). reproductive values will by definition be better And requirement (d) is that (D) must not be false adapted. (If it did then (D) would be tautologous.) (or more precisely, that (D) must be nontautol- We must allow that some instances of differential ogously true). reproduction are not instances of natural selection. If natural selection is to be defined in terms of relative adaptedness how can we use it to test the 3. Current Definitions and the empirical correctness of our definition of rel- Possibility of Satisfying the Four ative adaptedness? Suppose for a certain species Desiderata of organisms we pick out 2 similarity classes of members ofitthis species, A and B. (For our pur- Let us now examine current approaches to the poses these classes should be formed on the basis problem of defining relative adaptedness in the of the functional or epigenetical similarity of the light of the four desiderata discussed above. As genotypes of the members, see Brandon, 1978.) I said earlier the simplest approach is perhaps Suppose further that by our definition of relative the most popular: a is better adapted than b in adaptedness all members of A are better adapted E iff a has more offspring than b in E. Besides than any member of B to their mutual environ- making (D) a tautology and so stripping the ment. Our theory of natural selection, of which concept of its explanatory power this approach (D) is a major component, tells us that in statist- totally ignores the fact that natural selection is a ically large populations (where chance differences statistical phenomenon. Differential fitness may in fitness are cancelled out) A's will have a higher be correlated with certain differences in traits average reproductive rate than B's. If repeated but the correlation is not expected to be perfect. observations (either in the lab or in the field) show For example, in a certain population of moths that A's do in fact outreproduce B's then our darker winged individuals may on average definition of relative adaptedness fits these facts produce more offspring than lighter winged of natural selection and so is corroborated; if not individuals but this certainly does not imply that then it is on its way to being falsified (of course for every pair of moths the darker winged one no one observation would falsify it). will have a greater number of offspring than the It should be clear that any definition that fails lighter winged one. Appreciating that natural selec- to satisfy the condition of independence from tion is a statistical rather than a deterministic actual reproductive values will fail to be testable process has led some theorists to suggest a more in the way described above. Yet it is important sophisticated approach to our problem (see Mayr, to note that once we accept some theory of 1963, pp. 182-184). adaptedness, that is, some theory of what it is for This more sophisticated approach would an organism to be adapted to its environment, we define relative adaptedness in terms of the statist- can criticize a definition failing (a) as empirically ical probability of reproductive success. How is incorrect. In fact, as we will see, on any decent this probability to be determined? Suppose we theory of adaptedness any definition failing (a) separate the members of a population (of n~oths, ADAPTATION AND EVOLUTIONARY THEORY 111 for example) into similarity classes formed on the than the shepherds? To put the question another basis of the functional or epigenetical similarity way, do we count this differential reproduction of their genotypes. To fix ideas let us say that as natural selection? we form two such classes and that the members Biologists usually define natural selection simply of one are all darker winged than any of the as differential reproduction (of genes, genotypes members of the other (this difference being the or phenotypes). But this is due to carelessness result of genetic differences between members not lack of understanding. Most biologists would of the two classes). Further suppose that these agree that the above case is not an instance of classes are epistemically homogeneous with respect natural selection but rather a case of chance to reproduction; i.e. no other division of this differences in fitness. (Not that it could not be class of moths that we can make (based on our natural selection, but nothing in the story indic- knowledge) will be statistically more relevant to ates that it is. We can elaborate the story in reproduction, except divisions based tautologously ways that make it clear that it is not a case of 011 actual reproduction. We can now determine natural selection. For instance, the only food the probability of reproductive success of any source for dogs on our island might be animals individual as a simple function of the average whose size and ferocity would make it relatively reproductiye success of the members of the easier for the larger shepherds to eat than the similarity class to which it belongs. And so the bassets. Furthermore lightning might be a rare reproductive success of the individual is statist- phenomenon and indifferent between bassets ically determined by the functional properties of and shepherds.) How then shall we characterize its genotype. natural selection?The concept must be defined in This approach, which we will call the statist- terms of the as yet undefined notion of adapted- ical approach, fits some existing paradigms of ness. Natural selection is not just differential statistical explanation (see Salmon, 1970), but, reproduction but rather is differential reproduc- as 1 will show, it fails not only desideratum (a) tion which is due to the adaptive superiority of but also (d). The statistical approach is most those who leave more offspring. closely related to the frequentist interpretation Even without a definition of relative adapted- of probability which identifies the probability of ness we can be confident that cases like the an event with its relative frequency 'in the long basset-shepherd case are not instances of natural run'. The leading proponents of this interpre- selection. Given that natural selection is a statis- tation have been Richard von Mises and Hans tical phenomenon it should not be surprising Reichenbach. In what follows I am only criti- that in small populations Darwinian fitness is cizing the application of this interpretation of not always correlated with adaptedness. Yet the probability to defining relative adaptedness. This, statistical approach to defining relative adapted- of course, does not constitute a general criticism ness cannot recognize this. According to our of that interpretation. In the next section I will story the basset-shepherd case is unique; no such suggest a definition using a rival conception of population of dogs has ever been nor will ever probability. be on this island nor on any sufficiently similar Since the statistical approach uses actual repro- island. Thus our four dogs exhaust the data ductive values its empirical correctness cannot available for the statistical approach. So according be tested by prediction and observation. It can to the statistical approach the bassets are better only be tested against certain general theoretical adapted to the island environment than the principles. Consider the following case. Four shepherds. Yet by ecological analysis, in which dogs are on an island; two German shepherds one we determine what it takes for a dog to survive of each sex and two basset hounds one of each and reproduce on our island, we conclude that sex. Both bitches go into heat, basset mounts the shepherds are better adapted to the island basset and German shepherd mounts German than the bassets. This conflict raises questions shepherd. While copulating the shepherds are concerning the empirical correctness of the fatally struck by lightning. The bassets, on the other statistical approach. hand, raise a nice family. Are the bassets there- If the basset-shepherd case were just an ad fore better adapted to the island environment hoc counter-example dreamed up to refute the 112 ROBERT N. BRANDON statistical approach then. perhaps we should population of dogs. Here differential fitness is ignore it. But statistically small populations are not explained (some might worry over how this is uncomnion in nature and they are of consider- an explanation - 1 can't concern myself with that able evolutionary significance (especially for here) in terms of a chance process and small speciation by what Mayr calls the founder principle, population size. Thus if evolutionists are to explain see Mettles and Gregg, 1969, pp. 130-135; and what they want to explain, if they are to have Mayr, 1963). When applied to small populations the sort of explanatory theory they want, some the statistical approach will quite predictably other approach to the problem of adaptation is conflict with our best analyses of the organism- needed. environment relation, and so we are led to Early in this paper we were led to distinguish conclude that this approach which renders (D) a adaptedness from Darwinian fitness. As we have tautology is also empirically incorrect. (It should seen from the basset-shepherd example, in small be clear that defining the relative adaptedness of populations the two do not always coincide. Are an individual in terms of its actual reproductive there other types of cases where the two do not success is likewise empirically incorrect.) c~jncide?I can think of only three candidates Let me criticize tlie statistical approach in a for such cases: cases of artificial selection, cases slightly different way to show the connection of domestication such as in modern man where between its empirical incorrectness and its selection seems to have been relaxed and cases explanatory failure. The role in evolutionary tlie- of sexual selection. But none of these types of ory of the relational concept of adaptation is cases are ones where the correlation of fitness to explain differential fitness. The question is: and adaptedness should not be expected and it Why are those features which happen to be highly is important to see why this is so. I will focus correlated with reproductive success in fact my attention on artificial selection; what is said highly correlated with reproductive success? The about it can easily be applied to the other two types Darwinian answer is: Organisms having these of cases by analogy. features are (for the most part) better adapted Artificial selection quite often results in orgaii- to their environment than their conspecifics isms which could not survive in their 'natural' lacking them. This higher degree of adaptedness habitat. Organisms which under 'natural' con- causes the fitter organisms to be fitter and is the ditions would be the fittest are prevented from explanation of their higher fitness. The idea breeding while other organisms, less fit under behind the statistical approach to defining relat- 'natural' conditions, are allowed to breed. By ive adaptedness is that high statistical correlations such a process we end up with chickens without between certain features and Darwinian fitness feathers, dogs so small they can fit in your hand will indeed be causal connections and so will and fruit flies with legs where they should have explain differential fitness. Yet we have seen that antennae. Such cases, it could be claimed, are clear there are conceptually clear-cut types of cases cases where Darwinian fitness does not coincide (involving small populations) where the high with adaptedness. But how could one argue for statistical correlation is not a causal connection this claim? (in any interesting sense) and so cannot be used to Suppose we are following the relative frequency explain differential fitness. In our basset-shepherd of a segregating genetic entity, say a chroino- case certain distinctively basset features (such as some inversion in a population of fruit flies. We shortness and color of coat) are perfectly corre- divide this population into two genetically ident- laled with fitness. Yet our bassets are fitter than ical subpopulations, leave one sub-population in our shepherds not because they are shorter or are its original habitat and move tlie other to some a certain color, but rather because the shepherds new and different habitat. After a few generations were in the wrong place at the wrong time. In our we observe that the frequency of this chromosome case it's not that shepherds are characteristically inversion has changed in tlie moved population in the wrong place at the wrong time but just that (while remaining tlie same in the control they happened to be once. Due to small popula- population). Are we to conclude that this change tion size once is enough and so an essentially in frequency is the result of some divergence random process has radically altered our island between fitness and adaptedness, since some flies ADAPTATION AND EVOLUTIONARY THEORY 113 which would have been less fit in the original more sophisticated statistical approach fail both environment have had a higher relative fitness in desiderata (a) and (d). This failure, especially the the new environment? Obviously not. Whatever failure to meet (a), is fairly apparent and is pre- adaptedness is it has something to do with the sumably due to the neglect of theorists to formulate organism-environment relation. With a change in desiderata concerning the concept of relative environment a change in relative adaptedness is adaptation. However there is the novel approach not unexpected. Man is often thought of as the by Walter Bock and Gerd vo11 Wal~lert(1965) zenith of evolution yet he can hardly get by in his which might be taken as an attempt to meet fishy ancestors' environment. (a)-(d); at least it does not obviously fail them. Artificial selection is just a human induced Bock and von Wahlert argue that a measure change in environment. I presume that it is true of adaptedness should be expressed in terms of that a fly with leg-like antennae would not be as energy requirements. First they point out that well adapted to his ancestral home as many of the energy available to an organism at any given his more normal relatives. But is he not much time (from both internal and external sources) is better adapted than his normal relatives to the limited and that there is interindividual variation laboratory where the experimenter is selecting in the amount of energy available to organisms for an extra set of legs? In this environment he is (as well as intraindividual variation over the lifc- much better able to survive and reproduce than span of an individual). Next they point out that his more normal colleagues. The flies are living for an organism to maintain the proper relation and breeding in the laboratory; what would be to its environment (i.e. to stay alive) it must their relative adaptedness in the wild is irrelevant expend energy. The amount of energy expended to an assessment of their relative adaptedness will vary depending, for example, on whether in the lab. the organism is resting or escaping predation. Since To argue that in cases of artificial selection an organism must expend energy to live and fitness and adaptedness do not coincide is clearly reproduce and since its available energy is limited to ignore the environment in which the selection it is advantageous, they argue, for the organism is taking place; in particular it is to ignore the to minimize the amount of energy required to experimenter's or breeder's part in this environ- maintain successfully its ecological niche (p. 287). ment, But that is no more justified than ignoring Thus the following definition is suggested by the part of predators in the prey's environment their work: and is a bit of ai~tl~ropocentricism.To objective a is better adapted than b in E iff a requires less biologists experimenters and breeders are no energy to maintain successfully its niche in Ethan different than those English birds who for bun- does b, dreds of years have steadfastly selected against i.e. eaten) moths not cryptically colored. There are a number of problems with this Thus artificial selection is just a type of natural definition. First we must ask whether it really meets selection. This point will have a crucial role to requirement (a). Stern (1970, p. 48) suggests that play in an argument later in this paper so I it does not. He asks what it means to success- should make it clear that it is not a quibble over fully maintain a niche. He quotes Bock and von words. How would we reply to one who says Wahlert as follows: 'The relative factor of survival that by 'natural selection' he means all cases of or the relative number of progeny left which is selection excluding those involving man? To this usual when comparing the adaptedness of indi- we should reply that the concept he has defined viduals is accounted for by the relative nature is not as useful for theoretical purposes as the more of the term "successful" ' (Bock and von Wahlert, inclusive concept we have defined. He can try to p. 287). This, according to Stern, 'is tantamount use words however he wants, but he can't justify to admitting that their criterion is really subser- an anthropocentric point of view towards the vient to reproduction, and that success in adap- concept of adaptedness. tation is still to be measured by more conventional We have seen that the simplest approach to means. That a niche will be maintained more defining relative adaptedness, which does so successfully if less energy is required is clearly in terms of actual reproductive values, and the only an unsupported conclusion, not a matter of 114 ROBERT N. BRANDON definition.' (Stern, p. 48). But here Stern misses Rather let us grant for the sake of argument the point. Bock and von Wal~lertclearly assert that it is applicable and ask whether or not it is that 'unsupported conclusion'. They say, 'The less empirically correct. energy used, the more successfully. . . the niche I have already outlined how to test the will be maintained.' (p. 287). If they are right then empirical correctness of a definition of relative differences in fitness can and will be explained in adaptedness (see above, pp. 110-1 11). In brief, terms of differences in energy requirements. It we take paradigmatic cases of natural selection remains for us to ask whether they are right. and see if the definition fits the case. In the well We may not be able to answer this question. known case of melanism in English moths we Although their definition of relative adaptedness would check to see if darker winged moths seems to be applicable (i.e. it seems to satisfy required on average less energy than lighter winged desideratum (c)) it may not be. We can turn to moths. I have raised doubts whether the Bock Bock and von Waldert for suggestions on how their and von Wahlert definition is so testable and definition is to be applied to particular cases. since I can't overcome the problems raised for its Unfortunately they do not discuss intraspecific testability I can't subject it to this case-study type comparisons; but from their discussion of com- of test. But if it is testable (or epistemologically paring the energy requirements of sparrows vs applicable) it can, I will argue, be shown to be woodpeckers for clinging to vertical surfaces we empirically incorrect. can reconstruct how they would make such a coin- Suppose we have in our laboratory a popula- parison (see Bock and von Wahlert, pp. 287 ff.). tion of genetically diverse individuals whose They would determine the amount of energy diversity is phenotypically expressed in an easily expended in clinging to a vertical surface by recognizable manner. By Bock's and von Wahlert's measuring the amount of oxygen consumed. definition some variants are better adapted than Thus for two woodpeckers they would determine others. I, as a perverse Popperian, prevent the which is better adapted to clinging to vertical so-called 'better adapted' from breeding while surfaces by measuring their oxygen consuinp- allowing the so-called 'less well adapted' to tion while clinging to some surface. One would breed. I do this in a large population over a be better adapted than the other if it used less number of generations. Since artificial selection oxyged than the other. Recall that we want to is just a type of natural selection we have here a explain differential reproductive success. One case of natural selection which does not fit could test the hypothesis that if one woodpecker Bock's and von Wahlert's definition. If more requires less energy to cling to a vertical surface falsifying cases are wanted we can produce them. than another then it (probably) will have more And so, it seems, if Bock's and von Wahlert's offspring than the other. But it is not likely to be definition is episteinologically applicable it is true. Even for woodpeckers there is more to life not empirically correct. Clearly this argument than hanging on trees. What seems to be needed applies not only to the Bock and von Wahlert is a determination of all the activities necessary definition but to all definitions which meet for survival and reproduction in a particular desiderata (a)-(c), environment. We would then compare the rel- This argument is not conclusive. When we ative adaptedness of two organisms by comparing begin to select for the so-called 'less well adapted' their energy requirements for these activities. we change the environment of the organisms. It But would not these activities have to be is open for the theorist whose definition we are weighted according to their importance? How criticizing to claim that our change of environ- would they be weighted? And isn't it possible, ment has reversed his estimations of adaptedness, and even fairly frequent, that one organism can adaptedness being environment relative. This bypass some 'necessary activity' because of some doesn't deter us; again we try to refute the difference from his conspecifics in morphology, implications of the definition. But what if our most physiology or behavior? These questions lead me perverse efforts fail to contradict the proposed to believe that the Bock and von Wahlert defin- definition? Here I think we must conclude that ition is in fact not epistemologically applicable empirical correctness has been purchased at the i.e. it fails (c)) but I will not pursue this further. price of epistemological applicability. (Consider ADAPTATION AND EVOLUTIONARY THEORY 115 how one would try to defend the Bock and von 4. A Suggested Definition Wal~lertdefinition against such countercases.) That is, the definition has become so vague and The attempt has been to construct a definition malleable as to make (D) unfalsifiable. My claim of relative adaptedness that renders (D) an is that for any proposed definition of relative explanatory law. Accepting the received view of adaptedness satisfying desiderata (a)-(c) I can philosophy of science I pointed out that for (D) produce cases showing that it fails (d) (i.e. is to be an explanatory law it must be nontautolog- empirically incorrect) and that to resist falsifica- ous, general, testable and true. I argued that for tion by artificial selection is to give up (c) (i.e. is (D) to be such the definition of relative adapted- to cease being episteinologically applicable or ness must satisfy desiderata (a)-(d). Finally I testable). To exhaustively prove this would be to showed that no definition of relative adaptedness take every possible definition of relative adapted- can satisfy (a)-(d). In the light of these conclu- ness and produce the relevant countercases. It is sions I will now suggest what I take to be the best not surprising that I can't do this. But I do hope possible definition of relative adaptedness. my argument is convincing. Recall our desiderata. Apparently we will have I'm sure some will feel that this argument to give up at least one of them. We should retain from artificial selection is a cheap victory. If we (a) and (d); tautologies and false statements could find a definition of relative adaptedness explain little (one should note that giving up that truly applied to all organisms in 'natural' (a) would also entail giving up (d)). As we will environments wouldn't we be justified in ignoring see there is a trade-off between desiderata (b) and counterexamples produced by artificial selection? (c) and my suggested definition will, in a sense, That is a difficult theoretical question but we preserve both. can say this: Such a definition would represent a First I will suggest a non-technical definition of tremendous advance in our knowledge of ecology relative adaptedness and then a more technical and would be welcomed. But artificial selection version. The non-technical version follows: is as much a natural phenomenon as predation, a is better adapted than b in E iff a is bet- starvation, mate selection, etc. The argument (RA) ter able to survive and reproduce in E than is b. from artificial selection should, if nothing else, decrease the plausibility of the possibility of such This definition avoids tautology, that is, it is a definition. Naturalists are well aware that nat- independent of actual reproductive values. (We ural selection is an opportunistic process, often can confidently assert that a particular Mercedes- leading to evolutionary dead ends and extinction. Benz 450 SEL is able to do 150 mph while Are not some 'natural' cases of selection just as knowing that it never has and never will go that bizarre as our concocted cases? fast.) It is also a general definition and it is The point emphasized in the argument from empirically correct (insofar as this makes sense, artificial selection is this: The environments in at least it is not empirically incorrect). But how which organisms find themselves competing are are we to apply it to particular situations? I think radically different from each other, and at least it is clear that as it stands (RA) is not episteino- practically speaking there is no way to specify all logically applicable. So this suggested definition' possible environments. Thus there is conflict has the effect of preserving (a), (b) and (d) at the between desiderata (c) and (d).To make (D) test- expense of (c), and given that we cannot have all able is to expose (D) to falsification from some four, (RA)'s obvious failure of (c) is a virtue. radically new ecological situation. And to protect It is an unpretentious definition; it wears its (D) from such falsification is to make it so general epistemological inapplicability on its sleeve. that it ceases to be applicable. This point should We can construct a more technical (and more be accepted even by those who fail to subsume pretentious) definition. Earlier I criticized what I artificial selection under natural selection. Having called the statistical approach to defining relative given good reasons to doubt that any definition adaptedness. This approach identified adaptedness of relative adaptedness will satisfy (a)-(d) the with the statistical mean of observed reproduct- question should be: Is there any reason to sup- ive rates. As pointed out then it is not too dis- pose such a definition possible? I've found none. torting to call the interpretation of probability used 116 ROBERT N. BRANDON
in this approach the frequentist interpretation. success of organisms in environments independ- There are other interpretations of probability. ent of observations of their actual reproductive Some, for instance the logical and subjective success. For example, given the characteristics of interpretations (associated with Carnap and de a certain island environment and the particular Finetti respectively), are here irrelevant. But the characteristics of some basset hounds and German approach, best expounded by Hacking (1965) shepherds such theories should be able to pre- (also see Popper, 1959), on which probabilities are dict the relative reproductive success of each deduced from theory rather than identified with even without any relevant statistics. Clearly such observed frequencies is relevant. predictions are falsifiable (as falsifiable as any In discussing the basset-shepherd case I said that statistical hypothesis), but do we have any reason observed reproductive rates can conflict with to expect them to be successful? There are few, estimations of adaptedness based on ecological if any, outstanding examples of such success in analysis. Suppose our ecological theories to be so the corpus of biological science. On the other well developed that for any given environment and hand, there seems to be no theoretical obstacle to organism we could deduce the distribution of successful predictions of this sort. probabilities of the number of offspring left by that The informal definition of relative adaptedness organism (in the next generation). That is, from suggested above, (M),satisfied desiderata (a), our theories we deduce for each organism 0 (b), and (d) but not (c). How does (RA') fare on and environment E a range of possible numbers our desiderata? Given the proper interpretation of sufficiently similar offspring, Qy, Qy, . . . , of probability it satisfies (a). On this interpre- Qvand for each QyL our theory associates a tation the probability of reproductive success (or number P(QC";) which is the probability (or expected genetic contribution to future genera- chance or propensity) of 0 leaving Q, sufficiently tions) is some biological property of the organ- similar offspring in E, Given all this we define ism and its environment (just as the probability the adaptedness 0 in E (symbolized as A(0, E)) of heads for a coin is a physical property of the as follows: coin and the tossing device). The organism in its environment has this property even if it is struck by lightning prior to leaving any offspring (just as the chance of heads may be '12 for a coin That is, the, adaptednessi ' of 0 in E equals the even if it is unique and is melted before it is expected value of its genetic contribution to ever tossed). Thus (RA') is independent of actual the next generation. (The units of value are reproductive values. The occurence of 'probably' arbitrary. All that matters here are the ordinal in (D) may be confusing but (RA') does not relations among the numbers associated with turn (D) into a tautology.13 (RA') clearly satisfies each pair
As sliowii by Laclc (1954). This 111ust be quite C, G, EIelnpel, Pl~ilosop/~yof Natural Sctence, s~lrprisingto those wit11 only a s~lperficial~111del- (Ei~glewoodCliffs: Preiitice-Hall, 1966). standiiig of evol~~tioi~.For exainple l'opper (1972, D. L. 13~111, Darwiri and his Critics (Canlbridge: p, 271) tllii~lcsit is 'one of the cot~iitlessdiffic~llties Harvard Ui~iversityPress, 1973). of Darwi~i'stheory' that i~at~~ralselectioi~ s110~11d EI. B. D. ICettlewell, 'Selectioi~ Experiiileiits on do aiiytliiiig otlles t11ai1 increase fec~~iidity. Iiid~~strialMelaiiisil~ ill the Lepidoptera,' Heredity 9 T11e explaiiatioil is really quite siinple: Iilcreased (1955)) 323-342. fec~~iidityoften res~~ltsin a decreased i~~~nlbesof 13. B. D. IZettlewell, 'F~lrtlier Selectioi~Experi~ne~its offspring s~lrvivii~giii the next gei~eration.See oil Ii~d~~strialMelai~isill ill tile Lepidoptefi~,' Willian~s(1966, c11p. 6) for disc~~ssion. Heredity 10 (1956), 287-301, To soille ~~iifainiliarwith tlle problen~of adapta- J. L. 1Zing and T, H. J~~lces,'Non-Darwiniai~ Lion this tnay not be obvio~~s.Rather tllan Ieargue Evol~ltion,'Science 164, 788-798. tlie geiiesally accepted I refer the reader to Stern D. Lack, 'The Evol~~tioiiof Reprod~~ctiveRates,' (1970) wllicll is a good introduction into t11e Evolution as a Process, J. S. 13uxley, A. C. Hardy aiid relevanf. literat~ue. E. B, Ford (eds.) (Loi~don:Alleii & Uilwiii, 1954), See below pp. 110-111, Of course one inigl~t pp. 143-156. wonder 11ow a defiiiitioi~could fail bot11 (a) and R. C. Lewontin, 'The Adaptations of Pop~~lationsto (d), or 11ow a ta~ltology c0~11d be e~npirically Varying Ei~vironinents,'Symposium of Quantitative incorrect, It can be in just this sense: gzven ail ade- Biology 22 (1957), 395-408, quate tlieory of adaptediiess we 11ave a iiotion of R, C. Lewontiii, 'T11e Coiicept of Evol~~tioil,' adaptedness wl~iclldiffers from aiiy ilotion failing International Encyclopedia of the Soczal Sciences (a) (i,e, aiiy noti011 wliicll identifies adaptedness (New Yorlc: Macinillaii, 19681, pp, 202-210. wit11 act~lalreproductive success). These two R. C. Lewoiitiil, 'The Units of Selectioii,' Annual iiotions will not be extei~sio~~allyeq~~ivaleilt. So, Reivew of Systen~aticsand Ecology 1 (1970), 1-18. fro111 the standpoi~ltof OLI~theory, the defiiiitioi~ R. C. Lewoi~tiii, 'Adattaineiito,' Enciclopedia Biaudi wllicl~fails (a) will also fail (d). (Toriiio, Italy, 1977). Tlie inove to this sort of defii~itioilwas s~~ggested T. R, Maltllus, An Essay on the Principle of Pop~~lation. to tne by Hilary P~~tnarn. Loi~doi~(1798). (D) becomes soinetlli~~glilze an instance of J, Maynard Sii~itl~,The Theory of Evolution 3rd edii. wllal Hacluilg calls the Law of Lilcelil~oodand is (Middlesex: Pei~g~~iilBoolzs Ltd, 1975). a~ialogousto the followii~g:If the cllaiice of l~eads E. Mayr, 'Ca~~seaiid Effect ill Biology,' Science 134 for coin a is '12 and the cl~anceof heads for b is (1961), 1501-1506. '/.I the11 (probably) wllei~both coins ale tossed a E. Mayr, Animal Species and Evolution (Caii~bridge: sn~alliiu~nber of tinles a will laiid 011 heads illore Harvard U~~iversityPress, 1963). than b will. E. Mayr, 'Darwin aiid Nat~~ralSelectioii,' Am, Scient. 65 (19771, 321-327. L, E, Mettler and T. G. Gregg, Population Genetics arid Evolution (Englewood Cliffs: Preiltice-Hall, 1969). Bibliography R. MLI~ISOII,'Biological Adaptation,' Philosopl~y of Science 38 (1971), 200-215. F. J. Ayala, 'Biological Evol~~tioil:Natural Selection or IZ. R. Popper, 'The Propei~sity Iiiterpretatioii of Randon1 WallZoology 23 (19741, 536-544. Evolutioilary Theory,' Science 130 (1959), 477-482. 1. Haclung, Logic of Statistical Inference (Cainbridge: L. B. Slobodlcin, 'Toward a Predictive Theory of Cali~bridgeUiiiversity Press, 1965). Evolutioi~,' Population Biology and Evolution, 120 1ZOBERT N. BRANDON
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