(a) A brief history of evolutionary views of species
Charles Darwin's ‘On the Origin of Species by Means of Natural Selection’ (1859
) was universally acclaimed as soon as it was published. Yet, perhaps the most insidious and long-lasting critique of Darwinism was contained within the very writings of its first supporters and promoters. ‘Darwin's bulldog’, Thomas Henry Huxley maintained that Darwin had not fully explained how infertility between species could result from natural selection: ‘Mr Darwin is perfectly aware of this weak point, and brings forward a multitude of ingenious and important arguments to diminish the force of the objection’ (Huxley 1860
). Huxley admitted ‘the value of these arguments to their fullest extent’, but he nevertheless argued that this apparent problem with the Origin of Species ‘is not to be disguised or overlooked’.
The always faithful Alfred Russel Wallace would have liked to rise to the occasion and explain how hybrid inviability and sterility could arise by natural selection to protect the purity of the species, but Darwin apparently persuaded him in private letters that his theory would not wash (Mallet in pressc
): evolution by natural selection did not work for the good of the species. Sterility was bound to be a disadvantageous trait for individuals to have (Wallace 1889
These arguments misunderstood Darwin's intended message. Darwin's ‘multitude of ingenious and important arguments’ were produced not to wriggle out of a major difficulty with his theory, but to demonstrate that sterility simply was not the point of speciation at all, so that the criticism was irrelevant. Hybrid sterility (and hybrid inviability) is often associated with crosses between species, but does not at all provide a good definition of species because there are cases of sterility and inviability in crosses within species, and, conversely, cases of species that are interfertile. For example, Darwin documented inbreeding depression and self-sterility within species, whereas hybrids between species in genera such as Pelargonium
are often completely fertile; the same is true in some animal species, such as in the genera Phasianus
. Furthermore, interspecific sterility is often asymmetric: a cross between a female of one species and a male of another may be fertile, while its reciprocal is sterile (Turelli & Moyle 2007
; Lowry et al. 2008
). In Darwin's (1859
‘Now do these complex and singular rules indicate that species have been endowed with sterility simply to prevent their becoming confounded in nature? I think not. For why should sterility be so extremely different in degree, when various species are crossed, all of which we must suppose it would be equally important to keep from blending together?… To grant to species the special power of producing hybrids, and then to stop their further propagation by different degrees of sterility, not strictly related to the facility of the first union between their parents, seems to be a strange arrangement.’
To convince his readership that species have evolved from non-species (such as morphs, varieties and geographical races), Darwin needed a new and flexible definition of species. They would have to be very different from the species hitherto envisaged by biologists, many of whom agreed with the creationist Buffon that species were defined by inability to cross, or ‘sterility’ (in Darwin's terminology, sterility included hybrid inviability). Species, in Darwin's view, are recognized by consistent gaps in morphology (a), but they form part of a continuum with varieties within species, which do not show such gaps. The evolution of these gaps, ‘speciation’ as we call it today, in Darwin's view, results from divergent selection, leading to the extinction of intermediates. Darwin called this his ‘principle of divergence’. Discussions on the topic of sterility were placed by Darwin in his chapter ‘Hybridism’, and consist of two main arguments alluded to above, i.e. sterility within species and fertility between them.
Figure 1 What do we mean by species? How do the concepts relate to one another? There is little disagreement over what we mean by species in sympatry, even though species concepts appear to conflict (see text for details and appendix A for further discussion). (more ...)
It is hard to throw out one's education and preconceptions and get to grips with what Darwin is asserting. And his readers did not. By Darwin's time, it had become ingrained that the correct definition of species was that they were intersterile. Even his chief supporter, Huxley (1860)
, misunderstood or was unconvinced by Darwin's uniformitarian argument, as we have seen, to the latter's evident frustration.
Later on, this discussion about hybrid sterility became even more confused. Romanes (1886)
, an ardent Darwin acolyte, followed Wallace in arguing for a kind of ‘physiological selection’ that would explain interspecies sterility via natural selection. Another staunch Darwinian, Poulton (1904)
, while recognizing the force of Darwin's arguments against adaptive sterility, proposed that ‘asyngamy’ was the true reality of species. Asyngamy meant, I think, mainly mate choice, or literally, ‘lack of coming together of gametes’, another form of reproductive isolation. These views were reiterated and consolidated in the period of the ‘Modern Synthesis’ by Dobzhansky (1937)
, Huxley (1942)
and Mayr (1942)
. Among evolutionary biologists, perhaps the prevailing view today is characterized as Mayr's ‘biological species concept’: that species are reproductively isolated groups of populations (Coyne & Orr 2004
; Futuyma 2005
); hybrid sterility and inviability, among other ‘isolating mechanisms’, form key parts of our normal definition of species in evolutionary biology (b
). Today's evolutionists are, of course, fiercely supportive of Darwinism. Yet, they ignore or reject Darwin's key argument that reproductive isolation (a trait that can only exist, by definition, at the level of species) is a bad definition of species. Instead, they argue that species are ‘real’ in the sense that they have an unambiguous definition (reproductive isolation), unlike lower or higher taxonomic ranks. Furthermore, they claim that Darwin wrote an interesting book about evolution by natural selection, but failed to explain how species arose:
‘… Darwin's book was misnamed, because it is a book on evolutionary changes in general and the factors that control them (selection, and so forth), but not a treatise on the origin of species’.
‘…despite the title of his greatest book, Darwin did not solve, and scarcely addressed, the problem of how two different species evolve from a common ancestor’.
‘Darwin's magnum opus remains largely silent on the ‘mystery of mysteries,’ and the little that it does say about this mystery is seen by most modern evolutionists as muddled or wrong’.
Darwin has even been accused of attempting to make the evolutionary origin of species more likely than it in fact is by blurring the boundary between species and varieties. According to Mayr (1982
, p. 269), Darwin treated species
‘purely typologically as characterized by degree of difference’, and also that ‘there was a strong, even though perhaps unconscious, motivation for Darwin to demonstrate that species lack the constancy and distinctiveness claimed for them by the creationists. For how could they be the result of gradual change through natural selection if it were true, as Darwin's opponents continued to claim for the next hundred years, that species are sharply delimited and separated by ‘bridgeless gaps’?’
The notion that Darwin was wrong about species and speciation goes hand in hand with the reproductive isolation view of species. Elsewhere, I have discussed whether the idea that Darwin was wrong can be sustained (Mallet in pressa
). But a far more important point to get ironed out is what happens in nature. If we could affirm, as did Darwin, that species are not real at all, but man-made groupings are merely useful in communication among biologists, and if we could show that what we call species and what we call populations actually blend imperceptibly into one another, with no clear natural dividing line, it seems to me that our understanding of how species form would be enhanced, because we would be able to study the entire continuum of varieties diverging into species. We would still be interested in the evolution of reproductive isolation, since the effect of reproductive isolation is to cause divergence along this continuum, but the need to invoke special mechanisms that apply only to speciation would be reduced. In addition, as Mayr implies in the quotation of the previous paragraph, if Darwin was right and species and varieties actually did
form a continuum, we would have much more convincing arguments against creationists. Divergent evolution by natural selection and other forces commonly seen within species, which are simple to demonstrate, could then provide unproblematic modes of speciation.
Should we tailor scientific definitions to improve discussions with non-scientists? It seems to me that we should, given the problems we biologists presently have with the religious right. Surely, it is better to define terms if necessary in order to win an argument that we know to be correct than to stick blindly to principles (e.g. based on monophyly) that are not helpful in this effort. A creationist theory of species is a theory, even if not a very useful one, and definitions of terms should at least consider the possibility that any possible alternative theory is correct (i.e. that there is no true phylogeny generated by evolution). Perhaps more importantly, if Darwin's uniformitarian conception rather than Mayr's ‘species reality’ view were generally accepted, it could have critical implications for understanding the biological basis of speciation. The punctuated equilibrium theory to explain gaps in the fossil record was founded on the Mayrian view of species and speciation (Mayr 1963
), that speciation was not possible without some kind of deus ex machina
to help it along, in the form of allopatry, rapid founder effects, leading to genetic revolutions (Eldredge & Gould 1972
; Gould 1980
). By contrast, if all stages of speciation from local populations, geographical or ecological races, to full species were commonly visible in nature, there would be good evidence that continuous processes of divergence leading to speciation can often occur, even while populations are in contact. This was the purpose of Darwin's argument.
For these reasons, I feel the time is right for evolutionists and geneticists to re-examine the Darwinian views on the nature of species. I worry that this proposal may seem too radical to many. For 70 years, we have come to accept that Darwin did not write a book about the origin of species at all; that species are real facts of nature, rather than human-circumscribed entities; that speciation is difficult, or at least more difficult than ordinary within-species evolution; and that the origin of species requires special conditions not normally found in everyday populations. Yet, I hope it can be accepted that it would be worth achieving a more uniformitarian, Darwinian view of species and speciation if that is the way nature really is.
The other problem with attempting to revive a more Darwinian view of species is the reverse: that the argument is not radical enough, and it seems merely like an exercise in splitting hairs. We all in some sense know that varieties blend imperceptibly into species, and that there are many ‘difficult cases’. Furthermore, we have certainly endured too many tedious arguments about species concepts, when we all really know what we mean by species anyway. My defence is that, having studied the problem and its history in some detail, I feel it could be a rather more important definitional problem than usual, and that there is something still missing from most current definitions of species. In particular, crude thought experiments and simplistic caricatures of theoretical phylogeny or reproductive isolation between species have been too widely used in this debate in the past. All too often, the many clear facts in nature have hardly been perceived through a thick idealized smokescreen of species beliefs. The Darwinian view, once seen, allows many facts to fit more simply into place, even though from the outside the change from the Mayrian viewpoint may seem subtle. Having made this small transition against the force of the education we have all received, I can assure the reader from personal experience that it allows a much greater understanding of just how major were Darwin's discoveries about evolution. In particular, it suddenly becomes clear how and why ‘On the Origin of Species…’ was a book about speciation after all.
Here I outline the mounting empirical evidence from nature for a more Darwinian view of species. Some of this evidence has been known for a long time, but, writing in 1942, Mayr was able to argue, in his chapter VIII on non-geographical speciation, that most cases of ecological races, species swarms in isolated lakes, etc., could be explained either by arguing for phenotypic plasticity rather than genetic differences, or by positing that the ‘races’ were in fact sibling species that had undergone former periods of allopatry (geographical isolation) necessary to achieve the level of divergence seen. Similarly, Mayr (1942)
insisted that hybridization between species was an unusual ‘breakdown of isolating mechanisms’, that it was caused mainly by human-induced environmental changes, and had little importance for the understanding of species and speciation, thus adding to the impression that there was no middle ground between species and varieties. By contrast, Huxley (1942)
reviewing the same kinds of evidence, argued for a much more nuanced view of species and of speciation (although still not entirely Darwinian). The title of Huxley's (1942)
book introduced the term ‘Modern Synthesis’, which in Huxley's view represented a fusion of Darwinian evolution and Mendelian genetics. By contrast, Mayr argued that in the Modern Synthesis an important part of the Darwinian hypothesis about the nature of species and speciation needed to be overturned (Mayr 1981
). As it happened, Mayr's arguments have been more persuasive–-until recently, now that new genetic data begin to blur the earlier certainties.
(b) The real advance made by the biological species concept
Before I review the empirical information, I should point out an aspect of the Mayrian view of species that is beyond reproach, and which builds on the ideas of E. B. Poulton, D. S. Jordan, K. Jordan and others from the 1890s and early 1900s. This was to deal with the issue of spatially separated forms. To Darwin (1859)
, species were morphologically differentiated populations separated by gaps, which in his view were caused by competition, leading to the extinction of intermediates (a
, appendix A
). Geographical populations of a lineage with different morphologies were therefore often regarded as separate species in the mid-nineteenth century, rather than as geographical races within the more inclusive ‘polytypic’ species that became popular later. In the late nineteenth and early twentieth century, it became obvious that the evolution of such geographical forms was somewhat different from the evolution of forms that can overlap in sympatry (Mallet 2004
). Clearly, when an isolated population evolves a new morphological or genetic trait, this is probably due to natural selection, but can it be said to be speciation? Mayr, Dobzhansky and Huxley promoted the idea that geographical divergence was not the same thing as speciation. I suspect Darwin and certainly Wallace would have agreed, but they did not express it very clearly (but see Wallace 1865
). Only if the new form could overlap in sympatry () would this kind of evolution contribute to the most interesting kind of multiplication of species, an increase of biodiversity that shows itself within one time and place as well as globally.
Figure 2 (a) (i) Pure sympatric, (ii) mosaic sympatric and (iii) parapatric distributions. Geographical sympatry is not necessarily the same as perfect panmixia (see appendix B for further discussion). Compared with the scale of dispersal (double-headed arrow, (more ...)
In the 1940s, speciation then became, correctly in my view, the evolution of differentiated forms that could coexist in sympatry. Darwin and his immediate circle probably did not fully appreciate this. When geographical forms in different areas were connected by zones of intergradation, nineteenth century Darwinians argued that this was evidence for speciation.
‘This complacent attitude was distinctly associated with the old morphological species concept and it reigned supreme until the new biological species concept began to replace it. Then it was suddenly realized by the more progressive systematists that those species between which they had found intergradation were their own creations, and not biological units. As the new polytypic species concept began to assert itself, a certain pessimism seemed to be associated with it. It seemed as if each of the polytypic species (Rassenkreise) was as clearcut and as separated from other species by bridgeless gaps as if it had come into being by a separate act of creation’.
A practical version of what became the biological species concept (b
), known as the polytypic concept, which involved the concept of sympatry, became important in taxonomy and evolutionary biology at the beginning of the twentieth century, and grew in influence at least until the 1980s. Today, however, consensus is changing towards a more phylogenetic approach to species classification (e.g. Papadopoulou et al. 2008
), typified by Cracraft's (1989)
phylogenetic or diagnostic species concept (c
; for further discussion of the relationships between Darwin's morphological concept, the biological concept and the phylogenetic concept of species, see and appendix A
). These newer ideas have led to rapid taxonomic inflation, especially in some charismatic vertebrate groups. In primates, the number of taxonomic species has actually doubled since 1985 (Isaac et al. 2004
), even though few new taxa have been discovered. Inflation resulted when formerly recognized subspecies were elevated to species level. Evidently, we are returning to a pre-Darwinian view of species as differing in a number of characters, rather than in ability to overlap in sympatry. Changes in taxonomy are a worry for biodiversity studies and conservation (Isaac et al. 2004
), but do not concern us here, because speciation scientists generally employ the sympatry overlap argument in defining species.
Today, it is not generally realized that the original purpose and chief advantage of the biological species concept was to address the taxonomic problem of geographically divergent taxa by naming many of them as subspecies within inclusive, more broadly distributed species, rather than just to promote reproductive isolation as the only true reality or essence of species. This 1900–1940s definition of species implied that speciation consisted of the evolution of morphologically (and genetically) differentiated forms that could coexist in sympatry (Mayr 1942
). Sympatric species that remain distinguishable in sympatry are generally accepted whatever the species concept adopted (Cracraft 1989
; Mallet 1995
; Coyne & Orr 2004
), even though distinct geographical populations may be classified sometimes as species, sometimes as subspecies, depending on the concept employed.