The phenomena of adaptation, both the process of adaptation and the products thereof, are central to, if not definitive of, biology.  The explanatory problem of adaptation was a major part of Darwin’s revolutionary project.  Prior to Darwin, the only systematic explanation of design in nature was a designer. (Although Lamarckian explanations of ontogenetic adaptation and transmission were thought by Darwin and others to be responsible for a small fraction of adaptive structures in biology.)  Darwin’s theory of evolution by natural selection changed all of that.  This paper focuses exclusively on that theory.  I will not consider extensions of that theory to culture, nor analogues to human artifacts.  We will see that Darwin’s theory of evolution by natural selection underwrites a thoroughly naturalistic account of functions in the biological world and the extensions of this to the cultural and artifactual domains are both tempting and perfectly reasonable, but due to space limitations I leave that for others.

1.  The Theory of Evolution by Natural Selection.   Consider a simple case of evolution by natural selection.  In a population of annual plants there is variation in the height of the plants.    Let us say the mean value is 1 meter (other statistical properties of the distribution will not be relevant in this simple example).  Taller plants out reproduce shorter plants, i.e., reproduction output is a (probabilistic) increasing function of height.  The ecological reason for this in our scenario is that the taller plants are out-competing the shorter plants for sunlight because they are growing close together in dense stands and so the taller ones shade the shorter ones.  But, let us note now, that the same result, talls out reproducing shorts, could occur for any number of ecological reasons.  This is a point to which we shall return.  Finally, height is, to some degree, heritable in this population, i.e., taller than average plants tend to produce taller than average offspring and similarly for shorter than average plants.

Although my description of heritability above is mechanism neutral, and the process of evolution requires no particular mechanism of heritability, let us suppose that in our plants multiple genes at multiple loci control height.  Statistically, though there will be exceptions, taller than average plants will have different alleles than shorter plants and these different genes will be passed on to their offspring.   Thus the offspring of tall parents will tend to have “tall” alleles and offspring of short parents will have “short” alleles.  Has evolution thus occurred?  I would say no.  We could take a purely genetic point of view and think of evolution as change in allele frequencies over generational time—but notice that is not how we started our account.  We started with a phenotypic description.   And, I claim, we need to complete a full generational cycle to give an evolutionary account, thus we have one further step—namely the development of these genotypes into mature plants with heights.  Then we have a 2^nd generation height distribution which, given all that has been said, will differ from the previous generation in that its mean will be greater than 1 meter.  How much greater depends on quantitative aspects of the account that have not been specified—the strength of selection and the degree of heritability.    But the points we are interested in are not dependent on making this simple example quantitative.

From this example it is easy to extract what have come to be know as “Darwin’s Three Conditions”.  These conditions are necessary, but not sufficient, for evolution by natural selection.  The conditions are:

1.      Variation.  There is variation in phenotypic traits among members of a population.

2.      Inheritance.  These traits are heritable to some degree, meaning that offspring are more like their parents with respect to the traits than they are like the population mean.

3.      Differential reproductive success.  Different variants leave different numbers of offspring in succeeding generations. (Lewontin 1978, Brandon 1990)

I will not dwell on the necessity of these conditions, since I think this has been explained adequately elsewhere and is fairly obvious, but for our purposes I need to make one point about the lack of sufficiency. 

In finite populations, and, of course, all biological populations are finite; in the absence of selection, differential reproduction is still expected.  Take two coins fresh off the mint, as close to physically identical as can be.  Toss them both 100 times.  It is highly likely that one will yield more heads than the other.  Similarly, in the absence of selection, drift will occur.  So change—in gene frequencies, or in phenotypic distributions—is by no means indicative of selection.  We need more than change to invoke selection.  What we need is differential adaptedness.  Or, more specifically, differential adaptedness to a common selective environment.

The Darwinian explanation of 3 is the Principle of Natural Selection.  I have stated this principle as follows:

PNS:  If a is better adapted than b in environment E then (probably) a will have greater reproductive success than b in E.  (Brandon 1990)

For this to be an explanatory law relative adaptedness needs to appropriately defined.  For instance, if we were to define relative adaptedness in terms of actualized reproductive success, then the PNS would be a tautology and explanatorily empty.  Elsewhere I have argued for the propensity interpretation of adaptedness (also known as the propensity interpretation of fitness), arguing that such an interpretation renders the PNS explanatory (see Brandon 1978, 1990,

Mills and Beatty 1979, Brandon and Beatty 1984).  I will simply assume the correctness of that interpretation in the discussion that follows.

2. Adaptation and Environment.  The PNS compares entities a and b in a common environment E.  Why? And what does this mean?

The basic idea behind the PNS is to localize the adaptive differences in the organisms (or whatever entities we are talking about—for now let us focus on organisms).  The contrast would be the following:  suppose we take two genetically identical seeds and plant them into two pots, one containing fertile soil which we water regularly and place in a well lit location.  The other pot contains soil mixed with arsenic that we place in a dark closet and never water.  Now the plant in the first pot grows well and produces many seeds, the second dies shortly after germination.  Do we say the first plant was better adapted than (or fitter than) the second?  No.  That would be to confuse a within-environment comparison of two different organisms with a comparison of two different environments.  Now if I change the case and use two different genotypes to start with but keep everything else the same then I have just succeeded in constructing a worthless experiment.  Again, almost certainly, the plant in pot one will do well and produce many seeds and the plant in pot two will die before producing any seeds.  In the language of experimental design, I would have confounded genotype and environment, and so would not have any meaningful interpretation of the result.  To meaningfully compare genotypes, I must do so in a common environment.  That idea is the foundation of the long-standing practice in biology of “common garden experiments” which are attempts to compare different organisms within a common environment.

But all of this sounds epistemological, and I am not here interested in making an epistemological point.  Rather I want to argue that ontologically, evolution by natural selection works by comparing organisms within common selective environments.  The point cannot be made fully here, but two facts are pertinent.  First, only differences localized within organisms have the possibility of being heritable in the normal sense.  This point is more complicated that it might seem.  Good and bad luck can be transmitted across the generations, for instance, if a plant lands in a bad habitat that is large relative to its range of seed dispersal, then that bad luck will be transmitted to its offspring.  Suppose another genotype in the same species had the good fortune to land in a good habitat that is again large relative to its dispersal range.  This second genotype will increase relative to the first over generational time.  But this case this is not natural selection; rather it is a form of genetic drift, based on a chance distribution event.  There is no differential adaptedness involved. (For further discussion of habitat choice vs. chance distribution see Brandon 1990, pp. 60-64.) 

Second, cumulative adaptive evolution, requires the existence, indeed the persistence, of common selective environments.  More on this shortly.

What is a selective environment?  How are they individuated?  The concept of fitness or adaptedness has received much attention from philosophers and biologists alike.  But adaptation, as I have just argued, is always to an environment.  One cannot meaningfully speak of adaptation simpliciter.  Thus the concept of the environment is the dual to the concept of adaptation.  As such it should have received equal attention from philosophers and biologists, but until quite recently it received none at all.  The result was not just a lack of conceptual clarity, but completely misguided experimental research programs (see Antonovics, Ellstrand and Brandon 1988 and Brandon and Antonovics 1996).  Fortunately progress has been made.

Interestingly, the problem is strictly analogous to the reference class problem in probability theory, and the approach I have taken draws directly on Wes Salmon’s solution to the reference class problem in terms of homogeneous reference classes (Salmon 1984).    I have argued that a selective environment is homogenous with respect to types (genotypes or phenotypes) T₁, T₂, …T_n if and only if the relative adaptedness values of those types are constant in that region.  (I am intentionally using the vague term ‘region’ here.  We might wish to apply this to a spatial transect, a temporal slice or even something else.)   First, notice that this notion is explicitly comparative and relative.  One must have at least 2 types to compare in order to have a selective environment; otherwise there is no relative adaptedness (only absolute).  And the scale of environmental homogeneity and heterogeneity for one set of genotypes may differ dramatically from that of a different set.

The idea just articulated is radically different from more tradition ways of thinking of the environment.  The above conception takes an “organism-centric” point of view.  That is, we look at the environment not through our eyes, not by guessing what might be of relevance to the organisms, but by using the organisms as our measuring instruments (Antonovics et al. 1988).   We put the organisms out in the environment, see how they do relative to each other, and repeat.  As long as we keep getting the same pattern we have the same selective environment, a change in relative performance, indicates a change in selective environment.  

This conception of the selective environment has two primary virtues.  One it is operational  (see e.g., Brandon and Antonovics 1996).  Two it is this notion, rather than the more simple-minded notion of heterogeneity of the external environment, that is relevant to the important areas of population genetic theory in which the notion of environmental heterogeneity has been invoked—e.g., the evolution of sex and the maintenance of genetic polymorphisms.

Finally, let me return to a point mention earlier in this section.  Some (e.g. Sterely and Kitcher 1988) have complained that my notion of selective environment is not really relevant to evolutionary biology because it is too narrow—that if applied literally it would break up the biological world at much too fine a scale to be useful for the purposes of evolutionary biology.  My reply is that the existence of stable adaptations—whether at the phenotypic level or genetic level—very strongly implies the long term persistence of selectively homogenous environments, or at least homogenous with respect to trait variants in question.  Otherwise there is no explanation of the long-term persistence of the trait.  Turtles-with-folding-necks is a good evolutionary trick.  It has persisted for tens of millions of years (a interesting and complicated story, see Rosenzweig and McCord 1991).  The PAX6 gene has persisted in more or less the form we see in fruit flies, zebra fish, mice and humans for 400 million years or so.  The only way to account for this impressive long-term stability is very strong stabilizing selection, meaning that any variant off the standard gets strongly selected against.

3. Adaptation and Function.  The Darwinian theory of evolution by natural selection that we have sketched above underwrites a thoroughly naturalistic account of functions in the biological world.  But the account has a number of complications that must be recognized in order to properly apply it.

We have already pointed to one serious epistemological problem in applying this theory—change, increase or decrease in frequency is by no means sufficient to indicate that selection has occurred.  Drift is constantly changing frequencies in natural populations (Brandon 2006).  Differentiating selection from drift raises both interesting conceptual and methodological problems (on the former see Millstein 2002 and Brandon 2005).  Space limitations preclude any detailed discussion of that here.  But it is worth pointing out that a great deal of practical methodological progress has been made on that point, especially at the molecular level (see, e.g., Bamshad and Wooding 2003).   We will focus on a problem that remains even after we have a clear separation of drift from selection.  As mentioned above, the PAX6 gene is highly conserved across a broad swath of animal phylogeny.  Given the constancy of mutation, the only explanation of this stasis is very strong stabilizing selection. Thus the presence of PAX6 in the form that it has across the broad phylogenetic distribution it has is due, without any doubt, to selection.

Consider the other example mentioned above, turtles that can flex their necks (by bending their necks sideways—Pleurodira—or in an S-curve—Cyrptodira) gradually replaced straight necked turtles (Amphichelydia) four or five times in different regions of the globe, as long ago as the Cretaceous in Eurasia and as recently as the Pleistocene in Australia (Rosenzweig and McCord 1991).  The consistency with which this happened strongly implicates selection on this particular trait.  That is, the bending neck is adaptively superior to the phylogenetically prior character state of a straight neck.

In both cases we can be confident selection has occurred, and that we know the “target” of selection (thus to use the language of Sober 1984, there has been selection for PAX6 not merely selection of, likewise for the bending necks of turtles).   And so if an adaptation is a product of the process of evolution by natural selection (Brandon 1978, 1990), then these things are adaptations.  And so, I claim, they have functions.  Their functions are their effects that make them adaptively superior to the trait variants with which they compete.  But knowing that they are adaptations, does not automatically allow us to identify their function.

To do that, we must have the ecological explanation of the adaptive superiority of the trait variant in question relative to its competition and relative to the relevant selective environment.   That ecological understanding does not follow either directly or indirectly from the statistical methods used to detect selection.  Thus, especially at the molecular level, it is quite possible to know that something is an adaptation, and so that it has a function, while being quite ignorant of its function. 

Neither of the two cases I have discussed are such cases, though the PAX6 was one where there was initial misunderstanding of its function.   When it was initially discovered that a mouse PAX6 gene could induce and ectopic eye in a fruit fly two erroneous conclusions were drawn: first that the fly eye and the mammalian eye were homologues—which is certainly false; and second, that the function of PAX6 was to induce eye development.  The latter is not flatly false, but incomplete, like saying that the function of a refrigerator is to chill Champagne.   That is an incomplete description of the function of a refrigerator.  Likewise PAX6 turns out to be a general purpose developmental regulatory gene that is involved in much more than eye development (see Brandon 2005 For discussion and references).  Now we know its function much more fully.

The turtle case is one where we have a very plausible ecological explanation of adaptive superiority of bending necks—it allows turtles to retract their heads under their shells for protection from predators.  Although we are dealing with selection in the distant past in many different habitats, the assumption is that predation was a constant problem and, everything else being equal, a bending neck is therefore superior to a non-bending one.  Thus the function of the bending neck is to provide protection for the turtle’s head from predators.  (See Brandon 1990, chap. 5 for a discussion of the general difficulties of constructing the necessary ecological explanations to support attributions of function.)

4.   The Necessity of a Hierarchical Point of View.  Strictly speaking, this section is unnecessary, given a correct ecological account of selection.  But it is worth being explicit on the point that the only possibly adequate general account of selection and adaptation must be hierarchical.  A single level account, for example, a purely genic account, could not possibly account for adaptations in nature.  Although this refutes some philosophical positions, once understood, there can be no residual controversy.

Ironically, looking back at the discovery of one of the first genuine cases of genic selection nicely illustrates this point.  When Doolittle and Sapienza (1980) and Orgel and Crick (1980) first discovered what we now know to be the common phenomena of repetitive genomic sequences they were initially puzzled.   They asked how the organism could benefit from these repetitive sequences.  No plausible answer emerged.  In the words of Doolittle and Sapienza, they had to reject the “phenotypic paradigm” in order to finally understand this phenomenon.  Benefit to the organism was not the issue.  Why?  Because the process that produced these repetitive sequences was not a selection process among organisms.  Rather, the process was a within-cellular process of a bit of DNA copying itself and inserting that copy elsewhere in the genome, thus out-competing bits of DNA not doing that or doing that at a slower rate.  In other words, this was another, lower, level of selection, to be understood in terms of what benefits accrue to the entities competing at that level.  Organismic benefit is irrelevant (in the first instance—of course, selection can, and often does occur simultaneously at multiple levels).

What is good for a sequence of DNA, may, or may not, be good for the organism in which it is housed.  Genuine genic selection is indifferent to organismic benefit.  The classic case of meiotic drive in mice, is one where what is good at the genic level is clearly deleterious at the organismic level  (males homozygous for the t-allele are sterile).  There is always a potential for conflict of interest among different levels of selection (e.g., cell lineage in cancer vs. organism).  Any adequate theory of adaptation must recognize this.  And so must be hierarchical.

5. Summary.  Modern evolutionary biology does provide a naturalistic account of adaptation and function.  That account has been briefly outlined here.  The process of adaptation is simply the process of evolution by natural selection.  The products of that process, we label adaptations.  That concept, then, is explicitly historical.  To say something is an adaptation is to say something about its causal history; just as to label a mountain volcanic is to say something about its causal history.   Adaptations are adaptations to specific environments and they are adaptations in virtue of specific effects that made the trait variant in question adaptively superior to the variants with which it has competed.  These effects can be referred to as the function of the adaptation.  Given that there are conflicts of interests among different levels of biological organization, the theory of adaptation must be explicitly hierarchical.

Conceptually I think this is reasonably clear.  But as we have seen, there are considerable difficulties lurking in the details.

Robert Brandon

References

Antonovics, J., Ellstrand, N. C. and Brandon, R. N. (1988) Genetic variation and environmental variation: Expectations and experiments. In Plant Evolutionary Biology, (ed. by L. D. Gottlieb and S. K. Jain), pp. 275-303.  Chapman and Hall.

Bamshad, M. and Wooding, S. P. (2003) Signatures of natural selection in the human genome. Nature Reviews Genetics 4: 99-111.

Brandon, R. N. (1978) Adaptation and evolutionary theory.  Studies in History and Philosophy of Science 9: 181-206.

Brandon, R. N. (1990) Adaptation and Environment.  Princeton University Press.

Brandon, R. N. (2005)  Evolutionary modules: Conceptual analyses and empirical     hypotheses,"  in Modularity: Understanding the Development and Evolution of Natural Complex Systems (ed. by W. Callebaut), pp. 51-60.  The MIT Press.

Brandon, R. N.  (2005) The difference between selection and drift: A reply to Millstein.  Biology and Philosophy 20: 153-170.

Brandon, R. N. (2006), The principle of drift: Biology’s first law.  Journal of Philosophy Vol. CIII, 7: 319-335.

Brandon, R. N. and Antonovics, J.  (1996)  The coevolution of organism and environment.  In R. Brandon, Concepts and Methods in Evolutionary Biology.  Cambridge University Press.

Brandon, R. N. and Beatty, J. (1984)  The propensity interpretation of ‘fitness’: No interpretation is no substitute. Philosophy of Science 51: 342-347.

Doolittle, W. F. and Sapienza, C. (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601-603.

Lewontin, R. C. (1978) Adaptation  Scientific American 239: 212-230.

Mills, S. K. and Beatty, J. (1979)  The propensity interpretation of fitness. Philosophy of Science 46: 263-286.

Millstein, R. (2002)  Are random drift and natural selection conceptually distinct? Biology and Philosophy 17: 33-53.

Orgel, L. E. and Crick, F. H. C. (1980) Selfish DNA: The ultimate parasite.  Nature 284: 604-607.

Rosenzweig, M. L. and McCord, R. D.  (1991)  Incumbent replacement: evidence for long-term evolutionary progress.  Paleobiology 17: 202-213.

Salmon, W.  (1984), Scientific Explanation and the Causal Structure of the World.  Princeton University Press.

Sober, E.  (1984) The Nature of Selection. MIT Press.

Sterelny, K. and Kitcher, P. (1988)  The return of the gene. Journal of Philosophy 85 (7): 339-361.