"The New Synthesis" of evolutionary biology began developing in the late 1930s & 40s, and continued through to the 50s.  It ostensibly brought together what was then known of genetics theory and practice, together with paleontology and systematics, into a single and coherent evolutionary canon.  A primary feature of the Synthesis period was the displacement of drift & non-adaptive variation, as a major part of evolutionary explanation, by natural selection & adaptive variation.  A second feature was the developing conflict between opposing views of how selection worked and what it produced - the "Classic-Balance Debate."  We have become introduced to this debate in the section on Dobzhansky above, but we shall have more to say in what follows.  In this section, our main task is to draw together the main strands of argument so as to bring us to the threshold of modern evolutionary thinking.

First, we should return to look more closely at the sort of empirical evidence that persuaded evolutionists to become "hardened" against genetic drift - to adopt a frankly selectionist and adaptationist view of variation and the evolutionary process.  Such a selectionist stance has dominated evolutionary thinking since the Synthesis until very recent times;  only in the last decade or two has the adaptationist view of variation and the evolutionary process been seriously questioned or challenged.  Following this, we shall return to some further consideration of the Classic-Balance views.

What, then, of the empirical base for the rising selectionist view?  We shall look at one primary case,  which concerns conspicuous polymorphism, a long-standing problem for evolutionists.  Until the times of the later Evolutionary Synthesis, such variation was uniformly regarded as selectively neutral - for if were not so, why would "the superior form" not replace the inferior?  The assertion of neutrality was a stimulus to the ardent selectionists in Britain who were at the time mustering under the banner of R.A. Fisher, E.B. Ford, and Ecological Genetics.

The second half of the century brought several compelling cases of natural selection to light;  this had enormous effects on general thinking

Cepaea is a widespread genus of land snail, and it shows a complex and prominent polymorphism in the colour and patterning of its shell.  Many other land snails showed similar polymorphisms, and they were all regarded as classic cases of neutral characters, showing off the effects of sampling error in small populations of an organism with low capacity for gene-dispersal.  These taxa were held up in the earlier (~1930s-40s) editions of all the classic texts in evolu-tionary biology as cases of neutral variation.  In the early 1950s, Arthur Cain and Philip Sheppard (a doctoral student of Ford's), both then working at Oxford, decided to show the world that such conspicuous variation could not possibly be neutral (ironically, Wright was also of this opinion - despite everyone's understanding that he believed such variation to reflect drift!)  In their now-classic work, Cain & Sheppard demonstrated that the shell-morph frequencies correlated clearly with major features of the habitat, that the correlation was of a form intelligible under a model of visual selection by birds (i.e. it showed selection for crypsis), and that such selection indeed took place (one of their main predators conveniently uses traditional large stones as "anvils" on which to smash the shells, and it can be shown that the samples of dead shells accumulated around these stones are non-random samples of the population at large, in the right direction as to maintain the local population morph-frequencies.)  In their conclusions of selection, they also made a strong, telling, point:  "all situations supposedly caused by drift should be re-investigated." (Note 1)  Their unstated suggestion was that it is too easy to conclude neutrality if you don't take the trouble to work hard so as to understand the organism on its own terms in its own habitat.

It was a hard-hitting point, one that still has great power, both rhetorical and practical.  Although much later work was conducted on Cepaea and other similar systems, much of it failed to show the same sort of simple and persuasive evidence of visual selection.  Certainly much of it did implicate selection of some sort, but the general persuasive power came from the earlier studies around Oxford.  The Cepaea work proved to become iconic - it became one of the selectionists' most important rallying points.  But can one move from a clear case of selection - from even a good number of cases - to the inductive conclusion that, in general, it is truly selection that drives the great mass of evolutionary phenomena?  In truth one cannot legitimately make this inference - after all, until naturalists explored Australia and South America, all swans were white;  now we must say that they are mostly white.  But it is much more straightforward to enumerate swan species than all instances of variation and character change...... The argument about the respective domains of explanatory power of chance on the one hand, and selection on the other, persists to this day.  However the answer may turn out, work such as that just sketched has, regardless, a very powerful message:  the mode and intensity of action of natural selection may not be obvious at first glance - it may take energy, persistence and ingenuity to find it out;  armchair conclusions of the sort:  "well, I fail to see how this character could be of selective significance" should be given little weight.  But, for the time being at least, it would also be unwise to take the view that "if only we look closely and imaginatively enough, we will be sure to find a selective agent at work," as an infallible global guide.  It was the perception of just such adaptationist fervour (which they felt to be inappropriate and unjustified) that drove Lewontin and Gould (Note 2) recently to mount their campaign against what they styled "naive adaptationist 'just-so-story' telling."  You will hear more about this business in a course in evolution, such as Zoology 441a;  suffice to say, while their diatribe against adaptationism has had the salutary effect of making adaptationists less glib and more careful, it has done little to dampen the adaptationist enthusiams, and for very good reason.

Molecular variation, on the other hand, seemed largely to be selectively neutral

One primary area of genetic variability where selectionist fervour has borne little fruit is that of molecular variation.  Virtually every enzyme and protein surveyed shows some Mendelian variability.  But although there are some diverse and important demonstrations that there are indeed selective factors that work on at least some of this variation, most would now agree that the great bulk of it seems to be selectively neutral, at least much of the time.  The same must be said of variation in DNA and RNA sequences.  So here is a largely-undisputed locus of action for random processes, and, because the frequencies of these variants seem largely to obey the dictates of chance, they can be used as highly informative sources of estimates of basic demographic parameters, such as population size, gene-flow, etc.  They may also be used to provide quantitative statements about the degrees of genetic differentiation among populations and taxa, and even statements about the times of separation among them.

With this, then, we have brought the arguments about the importance of selection vs. chance more or less up to the present.  There will be other remarks that bear on this same issue elsewhere in what remains below, but since they concern the matters of the extent, distribution, and evolutionary meaning of genetic variation (still the fundamental empirical issues), our attention must shift again to the Classic-Balance debate.

Until remerkably recently, poulation genetics theory has had little impact on the practice of evolutionary thinking;  all this was made worse by a continuing narrow empirical base

As we have seen, a highly-elaborated body of population genetics theory had developed by the time of the Modern Synthesis.  But it is remarkable just how little the thinking and practice of most evolutionists became informed by the full diversity of population genetics theory.  Also, we might note that, while some ideas did filter across and become incorporated, many others simply did not, and indeed still have not.  As Richard Lewontin could observe in 1974 (note 3):

 At this moment, theoretical population genetics plays a remarkably small role in the synthetic attempts of modern evolutionary geneticists to understand what they see.  I am constantly amazed at the rubbish that people write about their interpretations of the natural historical observations and experimental observations.  To this day they have not incorporated the insights of Fisher, Wright and Haldane..... into their thinking. ...There are prejudices, desires, and axes to be ground..

Of particular interest to what we might call 'general evolutionary biologists,' there were strongly-articulated theoretical views concerning how much variation there is in typical species of organism, how much of such variation is heritable, how much of it has to do with natural selection and adaptation, and how such variation is organized in space, particularly the relative amounts of variation within and among populations.   Fisher and Wright had worked out pretty thoroughly what the probable evolutionary consequences of given scenarios would be with respect to these matters, yet at the time (and until very recently), there was precious little firm empirical evidence with which to evaluate the relevance of the various models.  However, despite the inherent uncertainty about this fundamental set of issues, conceptualizations of many evolutionary phenomena and processes - such as subspecific differentiation and speciation processes - were quite profoundly influenced by what most folk in the trade thought they knew - what was familiar theory, and what, indeed, seemed intuitive - about variation within and among populations, and throughout whole species.

As we have noted, after drift became largely eclipsed by selection, the primary paradigm of the 40s was known as the Classic Model, due to Muller, which became opposed a little later by the Balance Model of Dobzhansky.  To anticipate:  the modern view is, as one might expect, somewhere in between, but it is much closer to Balance views in terms of the prevalence of allelic variation, if not in its conception of mechanism.  To recapitulate:  in a nutshell, the Classic view was that most genetic mutations are deleterious on their appearance, most of the time, and therefore natural selection primarily has a 'purifying' role in removing such mutants.  This renders the population largely genetically uniform at most gene loci for what was known as "the wild-type" allele.  On those rare occasions when beneficial mutants arise, they rapidly replace the wild-type allele, at least locally, and during the replacement phase the populations will show transient genetic polymorphism.  By such a process, populations gradually, and uniformly, accumulate genetic adaptations to their respective environments.

The classic & balance views had important implications about the meanings of variation

Corollaries of this "classic" conception are:  while most variation within most local populations must necessarily be either non-heritable or non-adaptive (selectively neutral - the old "fluctuations"), that shown among populations of widespread species is largely genetically-based, representing adaptation to local conditions (the local wild-types);  such regional differentiation (often recognised in subspecific epithets or racial designations) is seen as the stuff of larger-scale evolutionary change - the generation of new species.  By contrast, the Balance view was that dynamically stable genetic polymorphism is abundant and widespread at all levels of species populations - there was no such thing as the 'wild-type' - this was seen as a figment of the Classic view's imagination.  Selection dynamics were not seen as being simply directional and 'purifying,' but rather 'balancing,' actively maintaining much variation.  Most local intra-population variation was therefore seen as of adaptive significance - neutral variation and drift was an explanation rarely required.  Geographic variation was seen as largely representing shifting genetic balances, according to local environmental exigencies.

The "classic" conception of populations may be traced back to an interpretation of Fisher's "Fundamental Theorem of Natural Selection" (see section 3)  That theorem speaks of directional, adaptational, evolutionary progress..  The picture it lends is seemingly consonant with Darwin's view of things;  thus the Classic conceptualizations of nature found an easy niche in the minds of many evolutionary thinkers when they turned to contemplate natural populations.  It is ironic that Fisher's other big contributions, balanced polymorphism and the evolution of dominance, initially had a much more marginal influence.  Doubly ironic because the grinding of Fisher's selection engine removes genetic variation - the very conundrum which Darwin (and others since) wrestled with for so long.

The underpinnings of the Classic viewpoint became incorporated into a pervasive view of nature, the most important here being that geographic differentiation was generally and implicitly assumed to be reflective of genetic differentiation, of adaptational significance, and representative of the early stages of more substantial evolutionary change (speciation) - that is, subspecies, recognised and named on the basis of patterns in geographic variation, were seen as proto-species.  Much research into geographic variation up until recent times has been largely embedded in such assumptions, but many inferences were (and are still) simply not justified by the evidences usually presented - it is a matter for empirical investigation whether, and how much, geographic differentiation is even heritable, let alone of adaptive significance, or potentially of long-term importance.  Evolutionary biologists have only recently begun direct investigation (note 4) of this fundamental issue.

Another important underpinning of the Classic view was, as we have seen, the concept of genetic load:  since intra-populational variation is "bad" (insofar as it is due to deleterious genetic mutations which must be 'weeded out'  by natural selection), then populations showing such variation pay a selection penalty.  The more variation, the greater the load.  This concept has obvious disciplinary (and, as noted above, historical) associations with the notions of dysgenics, and eugenics.

The new evidence provided to us, from the late 60s onwards, by a diversity of molecular methods, has served to demonstrate conclusively the near-ubiquity of genetically-based variation at all levels of species populations, from the familial to the global.  It has also shown us that there is generally much more genetic variation within, than among, populations, for many sorts of characteristic;  that the geographic patterns shown by different sorts of character (say morphological or molecular) can be greatly different from one another;  that the historical processes that would seem to lie behind these different patterns may also be radically distinct, and therefore possibly of greatly-differing significance.

This all should not be seen as an unalloyed triumph of the Balance view, however, since we must recall that heterozygote advantage itself seems to be rare in nature (though we do now know of many good examples.  On the other hand, there is an expanding empirical base for the view that much variability in natural populations represents a dynamical balance of fitness differences among genotypes which can depend on complex arrays of factors such as:  mosaics of micro-habitat differences which give a spatial mosaic of genotypic fitnesses; population density- or genotype frequency-dependent fitness; age-group or life stage-dependent fitness.  Finally, we must note that some workers interpret the new molecular data as evidence for what has been called the neo-classical view:  that while molecular variation is indeed abundant, most is neutral, and therefore subject to drift dynamics, but that other kinds of variation largely follow classic (variation-removing) selection processes.

In its basic tenet of the "wild-type," though, the classic view seems to have been refuted.  Nevertheless, much of its associated evolutionary world-view (see previous page) has lived on, largely unquestioned and unexamined, at least explicitly.  However, recently, some evolutionary biologists began directly questioning (again!) the assumption of a genetic base to all variation (whether within or among populations), and the concomitant supposition (as they saw it) that all this variation is a reflection of the action of natural selection, generating adaptations.  After all, it was true (and remains so) that remarkably little empirical evidence bears directly on this matter.

Thus the question of heritability came sharply into focus:  how much of this variation really is heritable?  for if it isn't heritable it can't be part of a direct evolutionary adaptation, as such.  Thus there was a spate of studies into the heritability of variation, and, less than 20 years ago, biologists began to undertake experiments directly addressing the matter of the basis of inter-population differences.  These experiments involve such things as large-scale reciprocal cross fostering (note 4) and common-garden rearing experiments.  What they found out is that there is, indeed, often evidence of at least some genetic basis to some of the geographic differentiation, at least in some sorts of characteristics;  thus, those geographic patterns are probably some reflection of the action of natural selection.  Now we are in a position to assert that is is so, in at least some few cases;  before, it was an assumption, with only reasonable-seeming theory as its basis.

But, once again, we face the question:  is it a legitimate and reliable inductive inference that this is, much of the time, generally the case?  Can it become part of our assumed base of knowledge?  Can it become what now "seems reasonable?"  Perhaps so - and indeed, there is a wealth of examples of selection in wild populations (note 5) - but if history is any guide atall, we should be on our toes, mindful of the likelihood of empirical surprises;  after all, the empirical world has dealt us a good many in the last 130 years, and this has served to keep the pendulum of explanation swinging among the poles of historical contingency, chance events and selective change.
 

Note 1  Cain, A.J. and P.M. Sheppard  1950  Heredity  4:  275-294.  Return to text

Note 2   Gould, S.J. and R.C. Lewontin  1979  The spandrels of San Marco and the Panglossian paradigm:  A critique of the adaptationist program.  Proc. Roy. Soc. Lond.  B  207:  581-598.  Return

Note 3   at the AAAS conference, the proceedings of which were published in 1980 as:  "The Evolutionary Synthesis:  Perspectives on the Unification of Biology," edited by Ernst Mayr & William Provine and published by Harvard University Press.  Return

Note 4   See for example James, F.  1983 Environmental component of morphological differentiation in birds.  Science 221:  184-186.  Return

Note 5   Endler, J.  1986  Natural Selection in the Wild.  Princeton Monographs in Population Biology #21.  Princeton Univ. Press.  Return