Sunday, October 18, 2009

What Darwin Said: Part 6 - Gradualism (B)   posted by DavidB @ 10/18/2009 04:40:00 AM

This is the sixth in a series of posts about Charles Darwin's view of evolution. Previous posts were:

1: The Pattern of Evolution.
2: Mechanisms of Evolution.
3: Heredity.
4: Speciation.
5. Gradualism (A) , which dealt with Darwin's views on gradualism in the rate of evolutionary change.

The present part deals with another aspect of gradualism: the size of the variations adopted by natural selection. A gradualist in this respect maintains that successful variations (mutations, in modern terminology) are always or usually relatively small in effect.

[Added on 20 October: there is an article on Panda evolution (discussed below) here.]


Unless otherwise stated, all page references are to Charles Darwin: The Origin of Species: a Variorum Text, edited by Morse Peckham, 1959, reprinted 2006.

To denote small variations, Darwin usually refers to 'individual differences', which he describes as 'many slight differences which may be called individual differences, such as are known frequently to appear in the offspring of the same parents, or which may be presumed to have thus arisen, from being frequently observed in the individuals of the same species inhabiting the same confined locality' [122]. 'Individual differences' are therefore envisaged by Darwin as being both small and relatively common.

To denote larger or rarer variations, Darwin uses several terms, with some differences of meaning. Occasionally he refers to 'single variations', meaning those occurring only in rare and isolated individuals. Single variations may be either 'slight or strongly-marked' [178]. He also sometimes refers to 'sports', a traditional term used to describe unexpected new characters such as buds different from the rest of a plant [81]. Another term is 'monstrosity': 'some considerable deviation of structure in some part, either injurious to or not useful to the species, and not generally propagated' [120].

But Darwin most often uses the phrase 'great and sudden', 'great and abrupt', or related terms, to describe variations larger than individual differences [264, 267, 345, 362, , 713, 735, 751] : 'As natural selection acts solely by accumulating light, successive, favourable variations, it can produce no great or sudden modification; it can act only by very short and slow steps' [735; the word 'very' is omitted in the 5th and 6th editions].

The adequacy of individual differences

Darwin believed that in general individual differences were sufficient for the observed pattern of evolution: 'A large amount of inheritable and diversified variability is favourable [to natural selection], but mere individual differences probably suffice' [192].

Some authors have interpreted Darwin's concept of individual differences as covering only continuous variations (quantitative traits, in the modern jargon). I find no strong evidence to support this interpretation. Darwin himself does not use the terms continuous and discontinuous. In the first edition of the Origin he does twice refer to 'insensibly' small gradations [321, 714], and on one occasion to 'infinitesimally small' inherited modifications [185], expressions which might be taken to imply strict continuity. But the words 'insensibly' and 'infinitesimally' were removed in later editions. Darwin moreover says that 'Every one who believes in slow and gradual evolution, will of course admit that specific changes may have been as abrupt and as great as any single variation which we meet with under nature, or even under domestication' [263]. He also says that 'the general pattern of an organ might become so much obscured as to be finally lost, by the atrophy and ultimately by the complete abortion of certain parts, by the soldering together of other parts, and by the doubling or multiplication of others, - variations which we know to be within the limits of possibility' [679]. It is a general rule that when the same body part is repeated many times in the same individual, like the vertebrae of snakes, the number is variable [297]. These statements clearly imply that 'meristic' (numerical) changes can occur in evolution.

No great and sudden changes

Darwin makes several statements against the likelihood of 'great and sudden' changes. Perhaps the strongest is that: 'If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down' [344] This still leaves open the possibility of 'great and sudden changes' which do not produce a new complex organ, but some other change such as a large increase in size. Darwin was sceptical about the likelihood of any great and sudden changes. Many of his comments on the subject was added in the 3rd or later editions of the Origin, for example: 'It may perhaps be doubted whether monstrosities, or such sudden and great deviations of structure as we occasionally see in our domestic productions, more especially in plants, are ever permanently propagated in a state of nature' [121, 3rd edn. onwards]. Darwin's position is not that such changes are impossible, but that he sees little evidence for them, and several arguments against them. His reasoning is considered further below.

Darwin does make a partial exception for two kinds of sudden change. One is where a plant has flowers, etc, of two different kinds. If for some reason the plant ceased to produce one of these, there would be a sudden change, though the different types might originally have been produced gradually. [121] Darwin also acknowledged the case, raised by E. D. Cope, of what is now called heterochrony, where different stages of the life cycle of an organism are speeded up or slowed down. In such circumstances some parts of the life cycle may eventually be omitted entirely, and this could be a relatively sudden change, but 'Whether species have often or ever been modified by this comparatively sudden mode of transition, I can form no opinion; but if this has occurred, it is probable that the differences between the young and mature, and between the mature and the old, were primordially acquired by graduated steps' [349]

Darwin's reasons for gradualism

Curiously, in the first edition of the Origin Darwin gives little argument against 'great and sudden changes'. This was not because he had not thought about the matter. In the draft 'big species book' which he was working on before receiving the celebrated letter from Wallace, he included the following passage:

I cannot believe that in a state of nature new species arise from changes in structure in old species so great & sudden as to deserve to be called monstrosities. Had this been so, we should have had monstrosities closely resembling other species of the same genus or family; as it is comparisons are instituted with distant members of the same great order or even class, appearing as if picked out almost by chance. Nor can I believe that structures could arise from any sudden & great change of structure (excepting possibly in the rarest instances) so beautifully adapted as we know them to be, to the extraordinarily complex conditions of existence against which every species has to struggle. Every part of the machinery seems to have been slowly & cautiously modelled to guard against the innumerable contingencies to which it has to be exposed [p. 319, Charles Darwin's Natural Selection, ed. R. C. Stauffer, 1975]

In abridging his draft for the Origin, Darwin omitted this passage, apparently because he did not expect his position to be controversial. In the event, several commentators, including T H Huxley, thought he had been unwise to rule out great and sudden changes or 'saltations'. Darwin's correspondence shows that he was surprised at this objection, and in subsequent editions of the Origin he gave fuller reasons for his position. These may be broken down into the following main points:

1. It is improbable that large and sudden changes would produce the refinement of adaptation we observe in nature: 'almost every part of every organic being, at least with animals, is so beautifully related to its complex conditions of life that it seems as improbable that any part should have been suddenly produced perfect, as that a complex machine should have been invented by man in a perfect state' [121]

2. It is very rare for wholly new organs to appear 'as if created for some special purpose...nature is prodigal in variety, but niggard in innovation' [361] In his chapters on 'Difficulties of theory' and 'Miscellaneous objections' (in the 6th edition) Darwin discusses at length the evidence for transitional stages in the evolution of organs.

3. Closely related species usually differ only slightly, by a number of small differences, and cannot be sharply distinguished from sub-specific varieties, which in turn are merely well-marked individual differences. There is a continuity of variation which suggests that the differences between species are the accumulated effects of individual differences [135, 265]

4. 'Monsters' are usually sterile [121]

5. Embryology shows gradual rather than sudden transitions [267]

6. Great and sudden changes occur only rarely and in isolated individuals. Even if they have some selective advantage, such changes are likely to be eliminated by chance extinction, or diluted by interbreeding with other individuals, before they can establish themselves. [178]. Darwin based this argument on an anonymous article in the North British review (in fact by Fleeming Jenkin). Jenkin intended it as an argument against natural selection in general, but Darwin welcomed it as supporting his position against the importance of 'single variations'.

7. As in his pre-Origin draft, Darwin pointed out that if evolution often occurred through large and sudden changes in a single trait or organ, we ought to be able to find many cases of closely related species, resembling each other in most respects, but differing sharply in some particular way resembling a monstrosity. Darwin claimed that he had diligently searched for such cases but not found any [121]

Was Darwin right?

Mainstream neo-Darwinian evolutionists generally follow Darwin in minimising the role of 'great and sudden' variations. Gradualism usually goes together with a belief in the importance of adaptation and natural selection. In contrast, critics of natural selection, from Darwin's lifetime onwards, have often favoured some kind of saltationism: Mivart, Bateson, Goldschmidt, and Schindewolf being notable examples. More recently, punctuationists such as Stephen Jay Gould and Stephen Stanley have combined acceptance of macromutations with a lukewarm attitude towards natural selection. On the other hand, there is no logical incompatibility between macromutation and natural selection, if large mutations are favoured by selection. A minority of evolutionists, including Francis Galton, De Vries and J. B. S. Haldane, have combined selectionism with acceptance of macromutation as a possibility.

It is sometimes supposed that R. A. Fisher proved the impossibility of large mutations being selected. I am not sure that Fisher himself made such a bold claim. What he did prove, given a few reasonable assumptions, was that:

a. a small mutation is more likely to be beneficial than a large one

b. the probability that a mutation will be beneficial declines as the number of different traits affected by the mutation increases.

These points fall short of the strong claim that macromutations can never be beneficial. Confusion on this point has perhaps arisen from Fisher's informal 'microscope' analogy. If a microscope is already fairly well focused (corresponding to an organism which is fairly well adapted, as it must be to survive at all), a small adjustment of the focus has a 50:50 chance of making an improvement, whereas a large adjustment is bound to make things worse. But the latter conclusion depends on the tacit assumption that there is only a single optimum focus. In the case of a microscope we know that this is true, but if instead of a microscope we have some instrument with more than one locally optimal setting, such as an FM radio receiver with many stations, then a large adjustment has a non-zero probability of improving on the current position. Whether the probability is significant will depend on the number and spacing of local optima within the range of possible adjustment. Turning to the biological case, we can make use of the phenotypic version of the 'adaptive landscape' concept. Assuming that an organism is close to a peak in the landscape, a mutation will take its offspring to some other point of the landscape. Whether this is higher or lower in fitness than the parent will depend on the structure of the landscape. If peaks of fitness are few and far between, relative to the range of possible mutational effects, then the probability of a large mutation being beneficial will be very small. If on the other hand there are many peaks within the range of feasible mutations, then a large mutation may well be advantageous. I do not know of any rigorous argument against this scenario.

Darwin himself [121, 267] objects to the sheer improbability that a single, sudden transformation would produce an organism perfectly adapted to its environment. But the macromutationist does not need to claim this much: he need only claim that the organism would on balance be fitter than its predecessors. The adaptation might then be refined by smaller changes.

Turning to Darwin's other points, the argument from embryology is a weak one. It assumes that the evolutionary sequence of mature organisms is closely followed in the embryonic development of an individual, so that there can be no sudden transitions in the former without sudden transitions in the latter. This requires a strong 'recapitulation' theory of embryology, which would not now be accepted.

Fleeming Jenkin's arguments against the selection of 'single variations' depend on the assumption of 'blending inheritance', according to which an offspring is always intermediate between its offspring. But for single gene mutations, which would include many mutations of large effect, the 'blending' assumption fails.

The argument that 'monsters' are usually sterile carries some weight. Large mutations are sometimes due to chromosomal abnormalities, which reduce fertility, while even in the case of single gene mutations the resulting 'monster' may have difficulty finding a mate.

Darwin's remaining arguments are empirical. He claims that it is rare to find an organ in one species which cannot be traced through transitional forms in other species. New organs or body parts are evolved from old ones: for example the wings of birds and bats are evolved from the standard tetrapod forelimb, and not wholly new parts. Related species differ by a number of small differences, not by single radical mutation of the kind known to occur in 'monstrosities'.

It would be difficult to evaluate these claims without a wide-ranging survey of the animal and plant kingdoms. It seems to be true that closely related species often differ by numerous small changes. Cases like the 'geminate species' on the opposite sides of the Panama Isthmus, where several million years of separate evolution have produced slightly differing pairs of species, support this position. There is however evidence that single mutations of striking phenotypic effect have had a larger role in evolution than Darwin supposed. The classic cases of melanism and mimicry in insects seem to be of this kind: a melanic or mimic form first appears by a relatively large mutation, which is then refined by smaller changes. It is also claimed (by Vorontsov) that the hairlessness of the naked mole rat and of the bat species Cheiromeles is due to a single mutation. Whether we call these 'macromutations' is a matter of taste, but they go beyond what Darwin described as 'individual differences'.

There are some cases where the nature of the variation itself seems to require a sudden change. For example, some snail shells coil in the opposite direction to the standard one, and a single-step reversal of chirality (of a kind known to occur by rare mutations) is more credible than a transition through an uncoiled stage. In starfish, most species have five rays, which is evidently the 'primitive' condition, but some species have more than five. A transition through forms with 'five-and-a-bit' rays seems highly improbable, so there was presumably a sudden increase in some lineages. When significant sudden changes do occur, they may conceivably mark the origin of a new higher taxon, such as a family or order. Macromutationists have often argued for this. However, most such claims are vague and poorly supported. For example, Stephen Jay Gould endorsed the view of Dwight Davis that the distinctive features of the Panda (Ailuropoda) may have resulted from a few large mutations (with some subsequent 'polishing'), but there seems to be no direct genetic or fossil evidence for this. On perusing Davis's original 1964 monograph, he really had no reason for his view other than a gut feeling that the changes, such as the enlargement of the radial sesamoid bone, could not have been gradual. It has also been claimed (e.g. by Oliver Rieppel) that Chelonia (tortoises and turtles) must have evolved their armoured shell by large mutational steps. There were until recently no intermediate stages in the fossil record, but some transitional forms have now been discovered, which casts doubt on the macromutationist argument.

Overall, Darwin's gradualism probably went too far. There is no reason (Fisher notwithstanding) to be opposed in principle to macromutational changes, and there is evidence that they have sometimes occurred (perhaps more often in plants than animals). On the other hand, enthusiasm for 'saltationism' has often been linked with hostility towards natural selection, and a subjective inability to see how such-and-such a change can have been gradually selected. 150 years after the Origin, evolutionists should arguably be more open-minded than Darwin to the role of large mutations in evolution, but still cautious in claiming that any given change 'must' have been sudden.