This is the fourth in a series of posts about Charles Darwin’s view of evolution. Previous posts were:
The present part deals with the subject of speciation, that is, the formation of new species. Modern commentators often regard this as one of the weaker parts of Darwin’s theory. They complain either that Darwin didn’t understand the problem of speciation, or that he did, but gave the wrong solution. On the other hand, some biologists reject the current orthodoxy, and suggest that Darwin’s approach was closer to the truth.
Speciation. By speciation I mean the formation of a new species. This may either occur by change of an existing species to the point where it is classified as a new species, or by the splitting of an existing species into two or more different species. Some authors prefer to confine the term speciation to the latter process (splitting, or ‘cladogenesis’), but I will use it in the broader sense.
The term ‘speciation’ was not coined until early in the 20th century, and therefore was not used by Darwin himself. In letters he occasionally used the term ‘specification’ with much the same sense: Life and Letters, vol.3, p.160, letter of 26 November 1878 to Karl Semper, and More Letters, vol.1, p.380, letter of 25 November 1869 to George Bentham.
Species. The most widely used modern definition of ‘species’ is Ernst Mayr’s Biological Species Definition (BSD), according to which species are ‘groups of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups’ [Mayr, 19]. If two sets of organisms are living in the same place at the same time, and are successfully interbreeding, then they belong to the same species. If they are living in the same place at the same time, but are not successfully interbreeding to any significant extent, then they belong to different species. If two populations live at different places and/or times, they cannot be ‘actually’ interbreeding, and the question is then whether they are ‘potentially’ interbreeding. As Mayr recognises, this cannot usually be directly tested [Mayr, 22]. The crucial question is whether there are ‘isolating mechanisms’ that would be sufficient to prevent successful interbreeding if the two populations were combined under natural conditions [Mayr, chapter 5]. Geographical barriers or distance by themselves do not count as isolating mechanisms, since two separated populations may be reunited and then interbreed. Some intrinsic difference of genetics or behaviour, sufficient to prevent successful interbreeding, is necessary for reproductive isolation .
The BSD is not universally accepted. Some taxonomists find little use for it, as the status of ‘potential interbreeding’ is often uncertain. Mayr himself admitted that the BSD is not always applicable (for example, to wholly asexual species). The BSD does however have one great merit for theoretical purposes. If the pattern of evolution is ‘tree-like’, as generally accepted by modern biologists, then a crucial part in any system of classification is played by the points at which branching takes place. A species, under the BSD, marks the lowest level of classification at which two populations have passed such a point. It is desirable to have a term to mark this distinction, and the BSD meets this requirement. The problem remains that in many cases there is no way of verifying whether two populations have passed the point of separation.
Modes of speciation A large number of different terms have been used to describe processes, observed or hypothetical, by which speciation (in accordance with the BSD) may occur. Usage by different authors is not always consistent. I will use the following terms.
Allopatric speciation occurs when two or more populations of the same species, living in different places (the literal meaning of ‘allopatric’) are separated by a geographical barrier or unoccupied space, and become reproductively isolated from each other. (This is equivalent to what Mayr calls ‘geographic’ speciation.) Reproductive isolation may be acquired by evolutionary changes in the populations following their geographic separation, or by the extinction of intermediate forms in part of a continuous range, leaving the remaining forms reproductively as well as geographically isolated from each other.
Sympatric speciation occurs when two or more species are formed out of a single species living in the same place (the literal meaning of ‘sympatric’). On this interpretation of ‘sympatric’, the terms ‘allopatric’ and ‘sympatric’ do not exhaust the possibilities, because there could be a third case where new species arise in adjacent parts of a continuous range. Mayr, on the other hand, uses ‘sympatric’ to cover every case other than ‘allopatric’.
Parapatric speciation is the third case just mentioned, where new species arise in adjacent areas without geographical separation between them. Mayr calls this hypothetical proceess ‘semigeographic’ speciation [Mayr 525] .
Peripatric speciation is a form of allopatric speciation where new species arise from relatively small geographically isolated populations on the periphery of a species range.
Stasipatric speciation occurs when a new species is formed in a relatively small locality within an existing species range, displacing or coexisting with the parent species, but not interbreeding with it. It is generally assumed that in this case reproductive isolation occurs as a result of polyploidy or some other major change in the chromosomes, and some authors make this part of the definition of ‘stasipatric’. I prefer to avoid assuming a particular mechanism of reproductive isolation, and will use ‘stasipatric’ to refer to any form of speciation in a small area within a species range.
Theories of speciation
In the second half of the 20th century the dominant theory of speciation was that of Ernst Mayr. Mayr maintained that, except for speciation by polyploidy and other major chromosomal changes, the only major form of speciation was allopatric (or geographic in Mayr’s terminology). He particularly stressed the importance of peripatric speciation in small isolated areas. He argued vigorously against sympatric and parapatric speciation. His main theoretical argument was that major divergence between populations, to the point of reproductive isolation, is not possible without geographical obstacles to gene flow. He did however define ‘geographical obstacles’ very widely, so that, for example, different host species of parasites could be regarded as spatially separated [Mayr 349]. There might be geographical obstacles even within a single fresh water lake [Mayr 465]. Mayr accepted that polyploidy was an important mode of speciation among plants and some invertebrates, but disputed the importance of chromosomal changes in speciation among vertebrates.
Mayr’s views dominated post-war thinking on speciation, but were increasingly challenged from about 1970 onwards. Mayr’s rejection of sympatric and parapatric speciation was based mainly on verbal arguments, whereas quantitative models showed that sympatric and parapatric speciation were theoretically possible. There also seemed to be cases, like species swarms of fishes in lakes, which were difficult to explain by allopatric speciation. However, recent reviews of the evidence suggest that there are few clear examples of sympatric speciation [C&O 178], while it is very difficult to distinguish between the effects of allopatric and parapatric speciation [C&O 118] in those situations where the question arises.
Darwin on Speciation
There is no single section in the Origin devoted to what we now call speciation, so the first step is to identify which parts of Darwin’s work are relevant. Many parts of the Origin could have some bearing on the subject, but the following are the main ones:
‘Variation under Nature’ – important for its discussion on the distinction between species and varieties
‘Natural Selection’ – important for the discussion of circumstances favourable and unfavourable to natural selection, including isolation and interbreeding, and for the ‘principle of divergence’
‘Difficulties of the theory’ – probably the most important chapter for the problem of speciation, because it deals with the question how varieties and species can be formed despite interbreeding
‘Hybridism’ – discusses the evidence on interspecific breeding and the viability and fertility of hybrids
‘Geographical Distribution’ (two chapters) – important for discussion of isolation and means of dispersal.
‘Recapitulation and Conclusion’ – contains brief statements of most of Darwin’s key propositions.
Relevant comments may also be found in other works, and in Darwin’s correspondence.
Darwin’s definition of species
Darwin does not propose a formal definition of ‘species’, and he implies that any such definition would be arbitrary. He argues, especially in the section ‘doubtful species’ [Origin, 126-38], that there is no sharp distinction between varieties and species: ‘Certainly no clear line of demarcation has as yet been drawn between species and sub-species – that is, the forms which in the opinion of some naturalists come very near to, but do not quite arrive at the rank of species; or again between sub-species and well-marked varieties, or again between lesser varieties and individual differences’. Summing up his position, he says: ‘From these remarks it will be seen that I look at the term species as one arbitrarily given for the sake of convenience to a set of individuals closely resembling each other, and that it does not essentially differ from the term variety, which is given to less distinct and more fluctuating forms’. In the chapter on Hybridism Darwin discusses the varying degrees of intersterility and viability of offspring between recognised species, and concludes that ‘neither sterility nor fertility affords any clear distinction between species and varieties’ . Darwin was of course concerned to refute the traditional view that species were created with unbridgeable differences between them, and that intersterility was a special endowment designed by the Creator to keep them separate. This may have led him to play down the importance of reproductive isolation as a criterion of species status. It is unlikely that he would have accepted the BSD, if it had been put to him.
Darwin on Speciation
Regardless of whether or not Darwin would have accepted the BSD, we may still ask whether his theory can account for the division of existing species into new species as defined under the BSD. In other words, does he adequately explain reproductive isolation?
Some critics would claim that Darwin did not even recognise the problem, and that he therefore did not offer a theory of speciation at all. But this is an inaccurate criticism, as a section of the chapter on ‘Difficulties of the theory’ is devoted to the problem. Whether or not one agrees with Darwin’s ‘solution’, he did offer one.
First, it may be noted that Darwin deliberately rejected one tempting option: the proposal that the barriers to interbreeding between species were due to the natural selection of sterility between them. In a lengthy correspondence Alfred Russel Wallace tried to persuade Darwin to accept this solution, but after much agonising Darwin rejected it. He concluded that the observed pattern of sterility and fertility was difficult to reconcile with an explanation by natural selection, for example because species from widely separated areas, where there could be no selective pressure against interbreeding, were nevertheless often intersterile, or produced sterile hybrids, in captivity. He also saw a fundamental theoretical objection to Wallace’s theory. Wallace argued that intersterility would be selected because it was beneficial to the species, or to the variety, but Darwin pointed out that there would be no advantage to individuals, (or indirectly to their ‘nearest relatives’ or other individuals of the same variety) in a reduction of fertility.  He therefore did not see how the sterility could be initiated and gradually increased by natural selection. This is one of Darwin’s most important discussions of ‘levels of selection’, and I will return to it in another post. Since intersterility could not be explained by natural selection, or by a ‘special endowment’, Darwin concluded that it was a by-product, ‘an incidental result of differences in the reproductive systems of the parent species’ . This would be generally accepted by modern biologists.
So how did Darwin explain the divergence of varieties to the extent of what we now call speciation?
An important part of the answer was always geographical isolation. Long before the Origin, in a letter of 1844 to Joseph Hooker, Darwin wrote that ‘the most general conclusion, which the geographical distribution of all organic beings, appears to me to indicate, is that isolation is the chief concomitant or cause of the appearance of new forms’ [L&L, ii, 28]. In the Origin the emphasis on isolation is somewhat reduced, but it is still one of the most important factors, for example in the chapters on geographical distribution.
For highly mobile animals, Darwin comes close to regarding isolation as essential for speciation: ‘intercrossing will affect those animals most which unite for each birth, which wander much, and which do not breed at a very fast rate. Hence in animals of this nature, for instance in birds, varieties will generally be confined to separate countries, and this I believe to be the case’ .
In contrast, for ‘hermaphrodite organisms which cross only occasionally, and likewise in animals which unite for each birth, but which wander little and which can increase at a very rapid rate, a new and improved variety might be quickly formed on any one spot, and might there maintain itself in a body, so that whatever intercrossing took place would be chiefly between the individuals of the same new variety. A local variety when thus formed might subsequently slowly spread to other districts’ . This might be regarded as a form of stasipatric speciation.
For the generality of organisms, which are neither highly mobile nor static, the problem remains of explaining how distinct species are formed, rather than a smooth continuous distribution, now called a cline . Darwin considers the possibility that intermittent periods of isolation have always been involved in speciation. But Darwin rejects this option, saying ‘ I will pass over this way of escaping from the difficulty; for I believe that many perfectly defined species have been formed on strictly continuous areas; though I do not doubt that the formerly broken condition of many areas now continuous has played an important part in the formation of new species, more especially with freely crossing and wandering animals’  To account for the formation of distinct species within a continuous area, Darwin describes what would now be called a form of parapatric speciation. He stresses that the organic and inorganic environment seldom change smoothly. Within the range of a species, there are likely to be zones where conditions are relatively unfavourable, and the population will be sparse and liable to periodic ‘extermination’ (325), for example when a predator or prey species fluctuates in numbers. For these reasons the population of a species will be much larger and more continuous (in time) in some areas than others. The areas where the population flourishes will be more favourable to evolution, since there will be more chance for new variations to arise, whereas in sparsely populated intermediate areas there will be less variation, the population will be liable to ‘accidental extermination’, and intermediate forms will be constantly at risk of being overrun by the more successful surrounding varieties, which are more sharply distinct. 
This account of the processes leading to parapatric speciation has much in common with more modern approaches. There is however still one element missing from Darwin’s theory. Modern theories generally incorporate the idea that behavioural mechanisms will evolve to discourage mating between different varieties in ‘border’ zones, where the offspring of such matings would be disadvantaged. There is perhaps a hint of such mechanisms in one remark of Darwin, where he says that ‘I can bring a considerable category of facts, showing that within the same area, varieties of the same animal can long remain distinct, from haunting different stations [ecological niches], from breeding at slightly different seasons, or from different varieties of the same kind preferring to pair together’ . But this passage is a long way from Darwin’s discussion of his ‘parapatric’ model, and it would be straining interpretation to suppose that he intended them to be connected.
We may conclude that Darwin believed in the occurrence of allopatric, parapatric, and possibly stasipatric modes of speciation, even if he did not by modern standards have fully worked-out models of the process.
There remains the question whether Darwin also believed in the occurrence of sympatric speciation. Of course, if ‘sympatric’ is defined so as to include ‘parapatric’, then the answer is trivially ‘yes’. But if we define ‘sympatric’ more narrowly, to require divergence of two populations living together in the same or widely overlapping areas, then the answer is not so clear. Some modern commentators are confident that Darwin did accept sympatric speciation in this sense [C&O 125] . Against this, we may set a quite explicit denial by Darwin himself: ‘I do not believe that one species will give birth to two or more new species, as long as they are mingled together within the same district. Nevertheless I cannot doubt that many new species have been simultaneously developed within the same large continental area; and in my ‘Origin of Species’ I endeavoured to explain how two new species might be developed, although they met and intermingled on the borders of their range. [Darwin's emphasis] It would be a strange fact if I had overlooked the importance of isolation, seeing that it was such cases as the Galapagos Archipelago, which chiefly led me to study the origin of species’ [letter of 13 October 1876 to Moritz Wagner, Life and Letters, iii, 159]. One could hardly expect a clearer statement of the distinction between parapatric and sympatric speciation, or a clearer rejection of the latter. How then can it be maintained that Darwin believed in sympatric speciation?
It is, unfortunately, common for an author to be confused or inconsistent in his or her views, so a clear denial by Darwin of sympatric speciation in one passage does not rule out his acceptance of the process elsewhere. The interpretation of Darwin as an advocate of sympatric speciation rests on the section on ‘divergence of character’ in the chapter on Natural Selection. Here Darwin attempts to explain why the descendants of a single species diverge into many different types. The general explanation is that there are advantages in an ecological ‘division of labour’: ‘the more diversified the descendants from any one species become in structure, constitution and habits, by so much will they be better enabled to seize on many and widely diversified places in the polity of nature, and so be enabled to increase in numbers’.  They may, for example, feed on different kinds of prey, or live in different habitats such as trees or water. Even in the same patch of ground, a diverse mixture of species and genera of plants will produce more vegetation than a single species or variety. 
The principle of divergence of character is important and in general plausible, but its application to varieties within a single species and in a single geographical area is problematic. If Darwin had confined the principle to varieties which had already reached the stage of distinct species, there would be no problem, but some of his wording does seem to apply to sub-specific varieties. Darwin opens his discussion by asking, ‘how then does the lesser difference between varieties become augmented into the greater difference between species?’ , and the principle of divergence is his ostensible answer . There would still be no problem if he confined the divergence of varieties to cases where they live in different areas, but he does not explicitly limit the principle in this way, and some of his illustrations of the principle seem to involve such cases; notably, he refers to different varieties of grass in the same patch of ground . Yet the evolution of different varieties within the same small area would conflict not only with Darwin’s clear contrary statement to Wagner, but with those passages of the Origin itself which deal with the ‘blending’ of varieties through interbreeding. Moreover, even in the section dealing with divergence of character, Darwin goes on to say that the animals and plants living on a small patch of ground, and which therefore compete most severely with each other, in general belong to different genera or orders: ‘where they come into the closest competition with each other, the advantages of diversification of structure, with the accompanying differences of habit and constitution, determine that the inhabitants which thus jostle each other most closely, shall, as a general rule, belong to what we call different genera and orders’ .  In this case they cannot be recently descended from different varieties of the same species. It is all rather confusing. The charitable interpretation is that Darwin wished to deal only with one issue at a time, and intended his discussion of divergence to be qualified by the discussion of ‘blending’ in the chapter on ‘Difficulties of the Theory’. I think however it is more likely that Darwin simply overlooked the tension between his comments on divergence and his comments on blending.
Overall, Darwin’s position on the modes of speciation is pluralistic. He recognised what we call allopatric and parapatric speciation, and possibly also stasipatric speciation. His position on sympatric speciation is more doubtful.
This pluralism contrasts with the dominant modern doctrine of Ernst Mayr, which recognises only allopatric speciation (with polyploidy and other major chromosomal changes admitted as a special exception). Mayr and his adherents therefore found Darwin’s position unsatisfactory. Orthodox ‘Mayrism’ has however come under increasing criticism in the last few decades. Not surprisingly, some of those who criticise Mayrism have found support in Darwin’s writings, and applaud his supposed acceptance of sympatric speciation [H&B 90]. The importance and prevalence of different modes of speciation remain open questions in evolutionary biology.
Origin: Charles Darwin: The Origin of Species: a Variorum Text, edited by Morse Peckham, 1959, reprinted 2006.
Mayr: Ernst Mayr, Animal Species and Evolution, 1963
C&O: Jerry Coyne and H. Allen Orr, Speciation, 2004
H&B: Endless Forms: Species and Speciation, ed. D. J. Howard and S. H. Berlocher, 1998.
Life and Letters of Charles Darwin 3 vols, ed. Francis Darwin.
More Letters of Charles Darwin, 2 vols, ed. A. C. Seward and Francis Darwin.