Time: Stealth Attack On Evolution

I just lucked on to an article by Provine addressing exactly the question we are discussing. According to Provine, in 1942 Ernst Mayr was a “beanbagger” on his own account (italics=internal quote of Mayr):

Mayr understood this point perfectly in Systematics and the Origin of Species, but faced a major problem. He did not know much recent genetics. His primary source for the genetics of speciation in his 1942 book came from Genetics and the Origin of Species, in which Dobzhansky had relied heavily upon Sewall Wright’s insights into genetics and evolution (PROVINE 1986, Chaps. 10–11). Mayr assumed that most speciation took place after geographical isolation was firmly in place, even if only temporarily:

Naturalists have known for a long time that island populations tend to have aberrant characteristics. WRIGHT (1931)(1932, and elsewhere) found the theoretical basis for this by showing that in small populations the accidental elimination of genes may be a more successful process than selection. Furthermore, recessive mutations have a much better chance to become homozygous than in a large panmictic population. It is therefore very important to learn something about the actual size of distributional islands and of their populations (MAYR 1942, p. 234).

Mayr then offered examples of small isolated populations of cave animals, lizards, fish, birds, and mice, all of which exhibited aberrant characteristics. His analysis of these examples again drew upon the work of Wright:

An exact determination of the size of an isolated population is of importance, in view of Sewall Wright’s work on gene loss in small populations. Owing to “accidents of sampling,” small populations have a trend toward genetic homogeneity or at least toward a much-reduced variability. This is quite apparent in taxonomic work, although only a few systematists have taken the trouble to make careful measurements and to work out the coefficients of variation (MAYR 1942, p. 235).

Why, exactly, did population size have consequences for the speciation process?

The calculations of SEWALL WRIGHT (1931)(1932, and elsewhere) indicate that effective populations have to be rather small, in the order of several hundred individuals or less, before they can be expected to approach genetic homogeneity due to accidental gene loss. If the population size is larger (thousands to tens of thousands of individuals), there still may be rapid evolution owing to mutation pressure (in the absence of appreciable selection), but the population will remain much more variable. If the size of the effective breeding population is still greater, approaching panmixia in varying degrees, evolution will be slowed down considerably. The consequence of this consideration is that evolution should proceed more rapidly in small populations than in large ones, and this is exactly what we find (MAYR 1942, p. 236).

Mayr did not actually read Wright’s articles at this time, but relied upon Dobzhansky’s writing for Wright’s views. Thus he saw Wright basically as a random drifter, whereas Wright’s “shifting balance” theory clearly emphasized strong gene interaction and subdivided larger populations, not just small isolated ones (PROVINE 1986, Chap. 9). Mayr relied upon Dobzhansky’s distilled version of Wright’s theoretical formulations for analyzing reduced variability and increased rate of evolution in relatively small, geographically isolated populations. According to Mayr, however, random genetic drift was not the only way to produce reduced variability in isolated populations:

The reduced variability of small populations is not always due to accidental gene loss, but sometimes to the fact that the entire population was started by a single pair or by a single fertilized female. These “founders” of the population carried with them only a very small proportion of the variability of the parent population. This “founder” principle sometimes explains even the uniformity of rather large populations, particularly if they are well isolated and near the borders of the range of the species (MAYR 1942, p. 237).

This was the first statement of the founder principle.

Mayr also relied upon Wright’s calculations of effective population size, usually much smaller than a mere count of individuals in a natural population. In these passages, Mayr was attempting to explain the mechanisms of geographical speciation. He and other naturalists had observed that island populations exhibited characters different from those of mainland organisms, and he concluded that the speciation process was accelerated by the isolation of relatively small populations. Mayr argued that evolution was faster in small populations than in large ones because inbreeding led to random genetic drift, accidental gene loss, and consequent increase of homozygosis and decrease of genotypic and phenotypic variability in the small populations. These mechanisms caused rapid, divergent evolution in the small populations. “The potentiality for rapid divergent evolution in small populations explains also why we have on islands so many dwarf or giant races, or races with peculiar color characters (albinism, melanism), or with peculiar structures (long bills in birds), or other peculiar characters (loss of special male plumage in birds)” (MAYR 1942, p. 236).

Over the next 10 years Mayr became a critic of “beanbag genetics”, apparently because he came to see the co-adaptedness of alleles as very important. But it appears that the effect of small population sizes remained important:

Mayr’s article, “Change of genetic environment and evolution,” begins where he left off in Systematics and the Origin of Species. Mayr was particularly impressed by Wallace’s emphasis upon the high degree of integration and coadaptation of the genome. In the 1954 article, Mayr again emphasized “the conspicuous difference of most peripherally isolated populations of species.” But whereas in 1942 he left only a vague connection between the aberrant characteristics of these isolated populations and random genetic drift, he now argued that

… for such a striking dissimilarity of peripherally isolated populations two reasons are usually cited: difference of physical and biotic environment or genetic drift. It seems to me that neither of these factors nor a combination of the two can provide a full explanation, even though both may be involved (MAYR 1954, p. 158).

The answer to such aberrant characteristics, Mayr suggested, lay in understanding that the selective value of a single allele depended greatly upon the overall genetic environment.

The genome of an individual was a highly interactive, coadapted gene complex, Mayr argued. More importantly, the individuals in an entire species shared significant portions of that coadapted gene complex, which resisted changes: “Such a well-integrated, coadapted gene-complex constitutes an evolutionary unit in spite of its intrinsic variability. Any disharmonious gene or gene-combination which attempts to become incorporated in such a gene-complex will be discriminated against by selection” (MAYR 1954, p. 165).

Therefore, the major problem was to discover how it was possible to overcome the inertia of such a coadapted gene complex. One way was to send the gene-complex through a founder population (italics are Mayr’s):

One of the obvious effects of the sudden reduction of population size in the founder population will be a strong increase in the frequency of homozygotes. As a consequence, homozygotes will be much more exposed to selection and those genes will be favored which are specially viable in the homozygous condition. Thus, the “soloist” is now the favorite rather than the “good mixer.” We come thus to the important conclusion that the mere change of the genetic environment may change the selective value of a gene very considerably. Isolating a few individuals (the “founders”) from a variable population which is situated in the midst of the stream of genes which flows ceaselessly through every widespread species will produce a sudden change of the genetic environment of most loci. This change, in fact, is the most drastic genetic change (except for polyploidy and hybridization) which may occur in a natural population, since it may affect all loci at once. Indeed, it may have the character of a veritable “genetic revolution.” Furthermore, this “genetic revolution,” released by the isolation of the founder population, may well have the character of a chain reaction. Changes in any locus will in turn affect the selective values at many other loci, until finally the system has reached a new state of equilibrium (MAYR 1954, pp. 169–170).

Mayr emphasized that a genetic revolution was not to be expected in every founder population: “A ‘genetic revolution’ in the founder population is only a potentiality but does not need to happen every time a population is isolated, if the genetic constitution of the founders does not favour it” (p. 171). He also emphasized that “during a genetic revolution the population will pass from one well integrated and rather conservative condition through a highly unstable period to another new period of balanced integration. The new balance will be reached after a great loss of genetic variability” (p. 172). Many such populations, after undergoing a genetic revolution, would be severely depleted of genetic variability and subject to extinction should the environment change. Some populations, however, might find a new ecological niche after the genetic revolution and gradually accumulate genetic variability. Mayr illustrated this possibility with his famous diagram (Figure 2), with the point C representing the genetic revolution. [point C is a big dip in genetic variability]

I confess I was not too clear on the difference between Mayr (1942) and Mayr (1954) before I read this, but it still seems to me that the implications of population genetics for evolution in small populations were a crucial bit of the allopatric speciation model.

Apart from this, there is an additional question of whether or not Mayr was right about this being the main mode of speciation – and therefore whether or not Gould was right about Punk Eek. Allopatric speciation clearly occurs, but sympatric speciation seems to be increasing in popularity again, and my vague understanding is that at least for cenozoic mammals the conclusion of paleontologists like Gingerich is that gradual transitions between species are actually fairly common in the fossil record.