This series of posts attempts to identify the key propositions of 'Darwinism', and assess their current standing. Part 1 dealt with 'The Pattern of Evolution'. Part 2 considers the 'Mechanisms of Evolution'. Darwin always regarded natural selection as the most important mechanism, but not to the exclusion of all other factors. The post has turned out longer than I intended, but I have not split it up, as I think it is desirable to consider all of Darwin's 'mechanisms' together.

THE MECHANISMS OF EVOLUTION

The Origin of Species has no single neat section listing the 'mechanisms of evolution', so it is necessary to extract them from various chapters of the Origin, supplemented by reference to Darwin's other main evolutionary works, the Variation of Animals and Plants under Domestication (1868), the Descent of Man (1871), and The Expression of the Emotions in Man and Animals (1872). Unless otherwise stated, all page references are to Charles Darwin: The Origin of Species: a Variorum Text, edited by Morse Peckham, 1959, reprinted 2006.

In the following analysis I will classify Darwin's mechanisms of evolution into three groups: (A) those that depend on selection; (B) those that depend on the inheritance of acquired characteristics; and (C) other factors.

A. SELECTION

1. NATURAL SELECTION

I assume that anyone reading this will have a good general understanding of natural selection, but one point may be worth mentioning. Darwin considered that the 'struggle for existence', and therefore the outcome of natural selection, should be interpreted as including 'success in leaving progeny' (146). In various places he recognised that natural selection can operate through differential fertility and not just differential survival. Unfortunately he did not emphasise this strongly or often enough, and it was common for post-Darwinian writers to interpret natural selection as literally a matter of life or death, with the corollary that if a trait did not affect survival as such, it could not have evolved by natural selection. Darwin himself occasionally slipped into this over-simplification.

2. ARTIFICIAL SELECTION

Darwin believed that the characteristics of domesticated animals and plants, and their differences from their wild ancestors, were mainly due to artificial selection; that is, selective breeding by man. He distinguished two forms of artificial selection: 'methodical', where breeders deliberately attempted to change the traits of their stock, and 'unconscious', where there is no intention to alter the stock, but selective breeding is a by-product of other actions (109). For example, a gardener may weed out and discard poor quality plants, or a dairy farmer may slaughter cows that do not produce enough milk.

The influence of artificial selection on domesticated animals and plants now seems self-evident. There is a tendency to assume that the principle of artificial selection was already widely accepted before Darwin, who was therefore able to take it as an uncontroversial basis for comparison with natural selection. From my own reading of pre-Darwinian biology I doubt this. On a minor point, Darwin seems to be the first author to use the term 'artificial selection' itself (though he only uses it occasionally, preferring 'selection by man'). I have searched the pre-1859 texts on Google Books for the phrase 'artificial selection', and not found it used in the Darwinian sense. More important, the concept of artificial selection was not widely accepted in mainstream biology before Darwin. It can be found among some writers on animal husbandry, such as Sir John Sebright, and occasionally among other writers, such as the anthropologist James Cowles Prichard, but seldom among general biologists. [See Note 1] Most biologists assumed that domesticated varieties were 'unnatural' and not relevant to general biology, so they said little about them . When they did discuss domesticated varieties, they did not put much emphasis on selective breeding, but assumed that the varieties had been distorted from the 'natural' form by unspecified factors of environment and nurture. The general neglect of selective breeding by biologists helps explain why Darwin dealt with the subject at such length, first in the opening chapter of the Origin, and then in his longest single work, Variation of Animals and Plants under Domestication.

3. SEXUAL SELECTION

The concept of sexual selection is introduced by Darwin briefly in the Origin (173-5), and at much greater length in the Descent of Man. He distinguished two forms of sexual selection: one based on combat between males, and one based on female preferences (or more rarely, on male preferences.) Post-Darwinian biologists were generally willing to accept the principle of selection by combat, but unwilling to accept female preference. One weakness of Darwin's account is that he did not explain how females come to have such preferences. He does however say 'The females are most excited by, or prefer pairing with, the more ornamented males, or those which are the best songsters, or play the best antics; but it is obviously probable, as has been actually observed in some cases, that they would at the same time prefer the more vigorous and lively males'. (Descent of Man, 1871, vol.1, p.262) Here Darwin comes close to the modern idea that the secondary sexual characteristics of the male act as 'honest indicators' of general health. Modern biologists generally accept the importance of female choice, but there remain theoretical questions about the possible factors behind it, such as Fisher's 'runaway' process, Zahavi's 'Handicap' principle, and Hamilton's theory of the role of parasites.

Darwin describes sexual selection as an alternative to natural selection, rather than a variant form of it. The distinction is largely a matter of convenience. In population genetics it is usually convenient to lump both forms of selection together, but in general biology it is more useful to distinguish between them. Sexual selection has two important special features: it can explain otherwise puzzling differences between the sexes, and it can explain traits such as the peacock's tail which appear disadvantageous to general fitness.

4. ECONOMY OF GROWTH

Darwin devotes a section of the Origin (295-7) to the principle of 'Economy of growth', by which he means 'that natural selection is continually trying to economise in every part of the organisation'. This can help explain the reduction and eventual loss of body parts that are no longer used: 'if under changed conditions of life a structure before useful becomes less useful, any diminution, however slight, in its development, will be seized on by natural selection, for it will profit the individual not to have its nutriment wasted in building up an useless structure'. As is clear from these passages, economy of growth is seen by Darwin as a special case of natural selection rather than a distinct mechanism.

B. INHERITANCE OF ACQUIRED CHARACTERISTICS

Darwin died in 1882. Like most biologists before 1883, when August Weismann first questioned the inheritance of acquired characteristics (IAC), Darwin believed that characteristics acquired by an organism during its lifetime were sometimes inherited by its offspring. The principle of IAC is now often known as 'Lamarckism', because it plays a major part in the evolutionary theory of Lamarck, but it was not invented by Lamarck, and it was seldom questioned before Weismann. Darwin gave IAC a significant but subordinate part in his theory of evolution in a number of ways, as follows.

5. USE AND DISUSE

It is a matter of everyday observation that muscles tend to increase in size if they are heavily used, while those that are not used tend to atrophy. Use and disuse can even affect hard parts like bones, which adapt to imposed strains. Provided it is accepted that acquired characteristics can be inherited, it is logical to infer that the increased use or disuse of body parts can lead to evolutionary change. Darwin discusses this in various places in the Origin (especially 280-6), and he makes it the main explanatory mechanism for the reduction of disused organs such as the wings of flightless birds. He always however regards it as subordinate to natural selection, and concludes 'On the whole, I think we may conclude that habit, use and disuse, have, in some cases, played a considerable part in the modification of the constitution, and of the structure of various organs; but that the effects of use and disuse have often been largely combined with, and sometimes overmastered by, the natural selection of innate differences' (289).

6. INHERITED HABIT

Just as the use of organs leads to their growth, the habitual repetition of actions increases their ease of performance. If the principle of IAC is accepted, it is plausible that habits may also be inherited. Darwin makes this one of the sources of the actions described as 'instinctive': 'If we suppose any habitual action to become inherited - and I think it can be shown that this does sometimes happen - then the resemblance between what originally was a habit and an instinct becomes so close as not to be distinguished' (382). Darwin however also points out that some of the most remarkable instincts - those of social insects - cannot be explained in this way, because the worker insects do not breed.

7. DIRECT EFFECT OF THE ENVIRONMENT

Environmental circumstances sometimes produce an effect on the individual. For example, human skin darkens in response to sunlight, and animals' fur is said to grow thicker in cold weather. If the principle of IAC applies to such changes, they may be inherited. Darwin discusses the direct effect of the environment at Origin pp. 276-80 and Descent vol. 1, pp.113-6 , but regards it as a relatively minor factor.

Assessment of IAC: It is now generally accepted that, with a few special exceptions such as the protective spines of water-fleas, culture, and syphilis, characteristics acquired by individuals in their lifetime are not transmitted to their offspring. (This is not true of the reproduction of cells within an organism, where genetically identical cells are environmentally differentiated into different cell-types which then usually transmit their acquired state to their 'descendants'.) IAC in genetic reproduction at the level of individuals is not logically impossible, but an analysis by John Maynard Smith suggested that it would only be beneficial to fitness in some rather special circumstances. A general system of IAC is therefore unlikely to evolve. From time to time someone (like Edward Steele in the 1980s) claims that IAC is important after all, but such claims have not yet stood up. Unless there is a major new discovery, it therefore seems that Darwin was wrong in attributing a significant role to IAC in evolution. We may still ask:

- was it reasonable, given the available evidence at the time, for Darwin to believe in IAC? and

- did Darwin change his views on the importance of IAC?

Was it reasonable for Darwin to believe in IAC?

I have pointed out that few biologists before Weismann's challenge of 1883 questioned the existence of IAC. Among the many attacks on Darwin's theories in his lifetime, his acceptance of IAC was seldom criticised. If it is reasonable to accept prevailing beliefs of the time, then it was reasonable for Darwin to accept IAC. Compared to some other evolutionists, such as Herbert Spencer and Ernst Haeckel, Darwin gave IAC a relatively minor role in evolution. But this does not entirely let him off the hook. The evidence for IAC was largely anecdotal, and Darwin could have been more critical of it. In Darwin's own lifetime, in the 1870s, Francis Galton anticipated Weismann in questioning IAC, but Darwin paid little attention to Galton's arguments. In Darwin's favour, however, it may at least be said that he recognised the difficulty of finding a mechanism by which IAC could work, and he attempted to do so in his 'provisional hypothesis of pangenesis', which I will discuss in a later post.

Did Darwin change his views on the importance of IAC?

There is a traditional view, for example in Sir Gavin de Beer's old biography of Darwin, that Darwin greatly increased the emphasis on IAC as time went on. My own assessment is that the changes in his position on IAC were minor. Some of the evidence usually given for a major change is inconclusive or irrelevant. For example, it is pointed out that in his last major evolutionary work, The Expression of the Emotions (1872) Darwin puts more emphasis on 'inherited habit' than on natural selection in explaining the inheritance of expressive behaviour. But this does not prove any change in his position, because he had not written previously on the subject of expression. We cannot know how much emphasis he would have given to 'inherited habit' if he had written a book on expression in, say, 1860. In order to fairly assess his position, we need to compare like with like, which can best be done by comparing successive editions of the same work: the two editions of Variation (1868 and 1875); the two editions of Descent (1871 and 1874); and of course the six editions of the Origin (1859 to 1872). In making these comparisons I find only a few amendments that increase the importance given to IAC. For example, where in the first edition of the Origin he had said 'In both varieties and species, use and disuse seem to have produced some effect', in the 5th edition he changes 'some effect' to 'a considerable effect' (738), and where in the first edition he said 'Habit no doubt sometimes comes into play in modifying instincts', in the 6th edition he changes 'sometimes' to 'often' (740). These are significant changes, but not a radical demotion of natural selection. Possibly as a result of Herbert Spencer's writings, which placed a much stronger emphasis than Darwin himself on IAC, Darwin increasingly recognised that IAC (if it occurs) and natural selection tend to work in the same direction, so that it is difficult to decide on their relative importance. In the 6th edition he includes a passage: 'We should keep in mind, as I have before insisted, that the inherited effects of the increased use of parts, and perhaps of their disuse, will be strengthened by natural selection. For all spontaneous variations in the right direction will thus be preserved; as will those individuals who inherit in the highest degree the effects of the increased and beneficial use of any part. How much to attribute in each particular case to the effects of use, and how much to natural selection, it seems impossible to decide' (253). In the Descent he writes: 'We may feel assured that the inherited effects of the long-continued use or disuse of parts will have done much in the same direction with natural selection' (vol. 2, p.387; see also vol.1, pp.121 and 143). Given the fundamental assumption that IAC is possible, these comments are entirely reasonable, and indeed the puzzle is not why Darwin increased the importance he gave to IAC, but why in 1859 he gave it so little.

C. OTHER FACTORS

8. CORRELATION OF GROWTH

Darwin always attached much importance to 'correlation of growth', saying 'the whole organisation is so tied together during its growth and development, that when slight variations in any one part occur, and are accumulated through natural selection, other parts become modified. This is a most important subject, most imperfectly understood' (290, see also Descent vol.1, p.130-1). For example, changes in the front legs may affect the hind legs, and changes in hard parts may affect the adjoining soft parts. Other examples are more surprising, such as the fact that white cats are often deaf. Darwin does not seem to have changed his views on the subject much, but in later editions of the Origin he does point out that it is difficult to be sure whether correlated variation represents a true functional connection or merely an accidental result of inheritance from a common ancestor.The importance of 'correlation of growth' in Darwin's system is that it can help explain traits that do not appear adaptive in themselves, but are correlated in development with adaptive traits. Darwin refers to correlated variation in combination with natural selection (or artificial selection in the case of domesticated varieties), but presumably in principle they could be correlated with traits produced by sexual selection or IAC as well.

Assessment: The idea that genetic changes can have multiple effects is familiar under the name of 'pleiotropy', and is a standard part of modern evolutionary theory. A trait that is not adaptive in itself, but is an unavoidable by-product of an adaptive change, was termed a 'spandrel' in Lewontin and Gould's well-known critique of 'adaptationism'. There remains controversy over the importance of 'spandrels', but they are clearly not 'anti-Darwinian', if by 'Darwinian' we mean what Darwin himself believed.

9. FLUCTUATING VARIABILITY

In the first edition of the Origin Darwin says that 'Variations neither useful nor injurious would not be affected by natural selection, and would be left a fluctuating element, as perhaps we see in the species called polymorphic' (164). In the 5th edition Darwin extends the sentence to say '... left either a fluctuating element, as perhaps we see in certain polymorphic species, or would ultimately become fixed, owing to the nature of the organism and the nature of the conditions'. This is the closest that Darwin comes to the modern idea of 'genetic drift', but it is not quite the same. A closer analogy would be with the idea of 'mutation pressure', where mutations towards a certain state occur more often than those away from it, and ultimately lead to fixation. Darwin assumes that every change has some cause, and that the continued operation of the same causes could eventually change the traits of a species in the absence of selection. I do not think he ever quite saw the possibility that an adaptively neutral trait might be lost (or fixed) in a population purely by chance. The importance of this factor depends on the frequency of traits that are 'neither useful nor injurious'. In the 6th edition of the Origin Darwin discussed objections by Bronn, Broca, and Nageli to his reliance on natural selection, and conceded that they had some force. He concludes 'In the earlier editions of this work I underrated, as it now seems probable, the frequency and importance of variations due to spontaneous variability' (232). In the Descent he says similarly 'in the earlier editions of my 'Origin of Species' I probably attributed too much to the action of natural selection or the survival of the fittest. I have altered the fifth edition of the Origin so as to confine my remarks to adaptive changes of structure. I had not formerly sufficiently considered the existence of many structures which appear to be, as far as we can judge, neither beneficial nor injurious, and this I believe to be one of the greatest oversights yet detected in my work' (vol. 1, p.152). He goes on to discuss his two aims in the Origin, of showing that 'species had not been separately created', and that natural selection had been the 'chief agent of change... Nevertheless I was not able to annul the influence of my former belief, then widely prevalent, that each species had been purposely created; and this led to my tacitly assuming that every detail of structure, except rudiments, was of some special, though unrecognised, service. Any one with this assumption in his mind would naturally extend the action of natural selection, either during past or present times, too far'. But even this was not Darwin's last word. In the second edition of Descent (1874), he amended the statement 'I probably attributed too much to the action of natural selection' by substituting 'perhaps' for 'probably', and inserted a statement that 'I am convinced, from the light gained even during the last few years, that many structures which now appear to us useless, will hereafter be proved to be useful, and will therefore come within the range of natural selection'. [Note 2] These changes seem to show some shift of emphasis back to the importance of natural selection.

Overall assessment: there is no doubt that Darwin reduced his emphasis on natural selection in the years between 1859 and his death in 1882. He somewhat increased the emphasis on the inheritance of acquired characteristics, and considerably increased the emphasis on 'non-adaptive' characters resulting from 'fluctuating variability'. But none of the changes are dramatic, and they leave natural selection as the main factor in most cases. Darwin himself fairly indicated the significance of the changes in the final sentence of the Introduction of the Origin. In the first to fourth editions this reads 'I am convinced that Natural Selection has been the main but not exclusive means of modification'. In the fifth and sixth editions this is modified to 'I am convinced that Natural Selection has been the most important, but not the exclusive, means of modification' (73). The shift is therefore from 'main' to 'most important'. From a modern point of view it is usually regretted that he shifted his ground at all, and especially that he gave any role to IAC, which is now generally rejected. On the other hand, there remains considerable doubt about the extent to which all traits are adaptive, or correlated with adaptive traits. Modern biologists would attribute non-adaptive change mainly to genetic drift, which Darwin was unaware of.

There remains a question which I have not considered: are there any important factors in evolution (other than genetic drift) which Darwin was not aware of, or considered but rejected? In Darwin's own day the main objection to his theories was that his proposed mechanisms were inadequate, and that there must be additional factors such as inherent tendencies to perfection or complexity. Such objections were usually, overtly or covertly, motivated by a belief in what is now called Intelligent Design. I will not discuss such objections here. The whole of the Origin is 'one long argument' against them.


I intend the remaining posts to cover:

Heredity
Speciation
Gradualism
Levels of Selection

Note 1: To check my own impressions of the literature, I have consulted the book Artificial Selection and the Development of Evolutionary Theory, edited by Carl Jay Bajema. Bajema includes a dozen or so pre-Darwinian texts referring to artificial selection, but none of these are by mainstream biologists, and most do not go beyond the vague principle that varieties can be 'improved' by selective breeding. Interestingly, there is a discussion of the effects of domestication by Charles Lyell in his Principles of Geology, which (to me) is notable for not mentioning the effect of selection at all. The only pre-Darwinian authors in Bajema's collection who seem to have clearly recognised selective breeding as the main origin of domesticated varieties are James Cowles Prichard and the 18th century French philosopher Maupertuis.

Note 2: these passages are towards the end of the chapter on 'Manner of Development' which is chapter 2 in the 2nd edition (chapter 4 in the first edition). The extensive changes in the 2nd edition have not yet been much studied by Darwin scholars, and there is no variorum text, so it is difficult to detect changes without a line-by-line comparison, which I have not attempted.