Why was Darwin’s view of species rejected by twentieth century biologists?

Abstract

Historians and philosophers of science agree that Darwin had an understanding of species which led to a workable theory of their origins. To Darwin species did not differ essentially from ‘varieties’ within species, but were distinguishable in that they had developed gaps in formerly continuous morphological variation. Similar ideas can be defended today after updating them with modern population genetics. Why then, in the 1930s and 1940s, did Dobzhansky, Mayr and others argue that Darwin failed to understand species and speciation? Mayr and Dobzhansky argued that reproductively isolated species were more distinct and ‘real’ than Darwin had proposed. Believing species to be inherently cohesive, Mayr inferred that speciation normally required geographic isolation, an argument that he believed, incorrectly, Darwin had failed to appreciate. Also, before the sociobiology revolution of the 1960s and 1970s, biologists often argued that traits beneficial to whole populations would spread. Reproductive isolation was thus seen as an adaptive trait to prevent disintegration of species. Finally, molecular genetic markers did not exist, and so a presumed biological function of species, reproductive isolation, seemed to delimit cryptic species better than character-based criteria like Darwin’s. Today, abundant genetic markers are available and widely used to delimit species, for example using assignment tests: genetics has replaced a Darwinian reliance on morphology for detecting gaps between species. In the 150th anniversary of The Origin of Species, we appear to be returning to more Darwinian views on species, and to a fuller appreciation of what Darwin meant.

Appendix: How was Darwin’s text misread?

The scientific, and possibly political and metaphysical climate of the times forms the background against which a new understanding of species arose in the 1930s and 1940s. However, this does not excuse misreading Darwin, and I here argue the most influential proponent of the new, non-Darwinian view of species did just this. The claim was made that a revolution against Darwin’s species concept, rather than a modification or improvement of it, was required. Here I show that extremely abbreviated extracts from The Origin exacerbated still further a view of Darwin’s understanding of species promulgated by Mayr in particular. There is a danger, of course, in turning the reading of Darwin into a kind of hermeneutics. However, I believe the case against Darwin’s failure to define species is so clear, once one understands his actual views, that it seems a pity not to highlight how easily Mayr’s extracts can be misleading, especially as this evidence is apparently unknown to many historians of science, even by those generally critical of Mayr’s analysis of Darwin.

Evolutionary biologists probably rarely read Darwin today, with some enlightened exceptions (Berry and Hoekstra 2009). When they do, they tend to skim the “turgid Victorian prose that is uncongenial to modern readers” (Coyne 2008). Even after re-reading The Origin, presumably repeatedly, biologists continue to argue that “speciation … was terra incognita for Darwin” (Berry and Hoekstra 2009), or that “his views on species and speciation are pretty wonky” (Coyne 2009). In the 1900s–1950s, the climate for understanding Darwin was far worse than today. Darwinism had been in decline (Bowler 1992), and though Darwin was revered as the initiator of evolutionary thought, a ‘modern’ book on evolution or systematics probably didn’t require careful reading of Darwin. References by Dobzhansky (1937b) and Mayr (1942) to Darwin or history are generally cursory at this stage (Winsor 2006).

With the centenary of The Origin, it is clear that Mayr in particular did begin to read Darwin’s text carefully (Mayr 1959, 1963); indeed he edited the facsimile reprint of the first edition of The Origin I have used here (Mayr 1964). Mayr’s later work includes abundant quotations from Darwin. Yet his assessment of Darwin’s view of species remained entirely negative, largely perhaps because everything Darwin said on species seemed so strongly opposed to Mayr’s own ‘correct’ and ‘modern,’ reproductive isolation definition of species. Mayr, of course, was not the only influence on evolutionary thought at the time. Yet it is curious that many philosophers and historians of science and biologists use the same quotations about species from The Origin, exactly as cited by Mayr (these co-citations are highlighted below). This is probably because, even when critical of Mayr’s analysis of Darwin, these authors often side with Mayr’s instead of Darwin’s view of species.

My evidence here consists of seven quotations used by Mayr to support his argument on ‘Darwin’s failure’ in The Growth of Biological Thought (Mayr 1982: 267). These make up perhaps the most complete statement anywhere of the modern case against Darwin’s view of species. According to Mayr, these quotations show how Darwin had changed his mind about the definition of species from an emphasis on reproductive isolation in his notebooks to a kind of nihilism in The Origin. Darwin was apparently at this time “… increasingly influenced by the botanical literature and by correspondence with his botanical friends” (Mayr 1982: 267; Sulloway 1979), although why Mayr felt that plant species should be any less well-formed than animal species is not clear (Knapp 2008).

However, Mayr’s interpretation of Darwin’s views in The Origin is now generally viewed as erroneous (Ghiselin 1969). As Ghiselin has remarked:

Mayr [had the] notion that Darwin was inconsistent about species concepts, which I had corrected … earlier [Ghiselin 1969]. As I explained in a passage that was suppressed by the editor of the journal, Mayr reached his conclusion by writing out what Darwin said on cards, and deciding that the statements on the cards were inconsistent (Ghiselin 2004a).

Many problems Mayr (1982: 267) had in interpreting Darwin indeed stemmed from his use of extremely abbreviated quotations. Here I go through the quotations to show how they could have been misconstrued. The first is:

(1) “No one definition has as yet satisfied all naturalists; yet every naturalist knows vaguely what he means when he speaks of a species.” (Darwin 1859: 44, 1872: 33).

Here Darwin merely highlights an existing controversy about what are ‘real’ species. The quotation does not at all show that Darwin himself denied that species exist. The very next paragraph, overleaf, shows what he means here; “Generally the term includes the unknown element of a distinct act of creation.” In other words, Darwin is saying simply that many naturalists and scientists of his day were special creationists, but even so they can’t agree where to draw the line. This statement can hardly be viewed as controversial today, and it does not provide any evidence that Darwin’s species concept had changed or was inadequate.

The next, very widely cited quotation comes much closer to today’s perceived view of Darwin’s failure to define species scientifically:

(2) “In determining whether a form should be ranked as a species or a variety, the opinion of naturalists having sound judgment and wide experience seems the only guide to follow.” (Darwin 1859: 47, 1872: 37. Also used by Mayr 1942: 115; Ghiselin 1969: 95; Wright 1978: 1; McOuat 1996: 515; Ereshefsky 2009: 5–6!, and many others).

Tellingly, a key word, “Hence,” has been omitted by Mayr from the beginning of Darwin’s own sentence, in 1942 as well as in 1982. The “Hence, in determining …” is necessary in Darwin’s text because this sentence forms the conclusion to an argument that varieties are similar to species in difficult cases.

The header on these pages is “DOUBTFUL SPECIES.” Above the quotation, on the same page, Darwin (1859) argues: “Practically, when a naturalist can unite two forms together by others having intermediate characters, he treats the one as a variety of the other, ranking the most common, but sometimes the one first described, as the species, and the other as the variety.” Here we have Darwin’s clear, if somewhat implicit criterion for species defined by gaps in variation; varieties, on the other hand, lack gaps. But Darwin then cites some problems: “… cases of great difficulty … sometimes occur in deciding whether or not to rank one form as a variety of another, even when they are closely connected by intermediate links…” (Darwin 1859: 47). Doubtful cases exist, “Hence, … the opinion of naturalists … seems the only guide to follow.”

This fuller and more correct reading of Darwin’s is reinforced by the very next sentence, overleaf, also under the heading “DOUBTFUL SPECIES.” It begins: “That varieties of this doubtful nature are far from uncommon cannot be disputed …” (Darwin 1859: 48, my emphasis). Darwin is not at all saying, as might be supposed from the partial quotation used by Mayr, as well as many others, that all species are arbitrary units to be determined only via agreement of specialists. He is saying only that the most difficult cases must be so judged, since these borderline cases are indeed a matter of opinion. This is as true today as it was in Darwin’s time.

Now it becomes easier also to understand the following two quotations also from the same section of The Origin:

(3) “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.” (Darwin 1859: 52, 1872: 42; see also p. 469. Also used in Mayr 1959: 222, 1963: 14; Ghiselin 1969: 93, 95; Kottler 1978: 292, 294; Coyne and Orr 2004: 10; Ereshefsky 2009: 4!).

An earlier statement spanning p. 51 (headed “DOUBTFUL SPECIES,” as before) to p. 52 (headed “VARIETIES GRADUATE INTO SPECIES”) reads: “And I look on varieties which are in any degree more distinct and permanent, as steps leading to more strongly marked and more permanent varieties; and at these latter, as leading to sub-species, and to species.” Again, we have the clear assertion of the importance of species distinctness, and that varieties are not distinct. Species are certainly on the same continuum as varieties, but the “arbitrary” criterion we use is that species are more distinct: they have gaps between them. Then, four pages later we have the fourth quotation used by Mayr:

(4) “Hence the amount of difference is one very important criterion in settling whether two forms should be ranked as species or varieties.” (Darwin 1859: 56–57, 1872: 45; also used in Mayr 1959: 222. Similar statement in The Origin p. 485 cited by Ghiselin 1969: 98).

On p. 48, Darwin had been arguing that the number of plant species in Britain is disputed among naturalists because the criterion of gaps in the distribution of forms can fail. In contrast, “amongst animals which unite for each birth, and which are highly locomotive, doubtful forms … can rarely be found in the same country, but are common in separated areas.” In sympatry, animal species are normally identifiable via gaps, but the problem of making a decision about geographically separated plant or animal populations constantly besets taxonomists, no less today than in Darwin’s time.

In spite of his criticism of Darwin, Mayr recognized the same problem. He argued for “the importance of a nonarbitrary definition of species” (Mayr 1963: 29), but he also recognized that “one finds many populations in nature that have progressed only part of the way towards species status. They may have acquired some of the attributes of distinct species and lack others. One or other of the three most characteristic properties of species—reproductive isolation, ecological difference, and morphological distinguishability—is in such cases only incompletely developed” (Mayr 1963: 24). “The decision whether or not to call such populations species is by necessity somewhat arbitrary” (Mayr 1982: 282).

As did Darwin, Mayr argued that the ‘problem’ was particularly severe in geographically separated populations: “Even though the number of cases causing real difficulties to the taxonomist is very small, it cannot be denied that an objective delimitation of species in a multidimensional system is an impossibility” (Mayr 1963: 24). By ‘multidimensional system’ Mayr meant one consisting of multiple spatially or temporally separated populations showing various levels of genetic divergence. “To determine whether or not an incipient species has reached the point of irreversibility is often impossible” (Mayr 1963: 26).

So what did Mayr think of such doubtful forms? Should they be classified as subspecies, or as separate species? “…Isolated forms, or ‘insular species,’ are excellent evidence in support of geographic speciation and, as such, welcome to the student of evolution; but, on the other hand, they are also very troublesome to the modern taxonomist” (Mayr 1942: 166). Ideally, one would like to infer whether, if brought back together, these populations would remain distinct. “…It is necessary in the cases of interrupted distribution to leave it to the judgment of the individual systematist, whether or not he considers two particular forms as ‘potentially capable’ of inbreeding—in other words, whether he considers them subspecies or species. … We may have to apply the degree of morphological difference as a yardstick in all those cases in which we cannot determine the presence of reproductive isolation” (Mayr 1942: 120–121).

Mayr, like Darwin, evidently felt that the degree of morphological difference was useful in doubtful cases, based on the taxonomist’s knowledge of the group. Comparing this to the degree of difference normally shown by good species in sympatry in the same group would enable decisions about the taxonomic status of isolated populations. Note that Mayr uses almost the exact same wording as Darwin about degree of morphological differences, the need for taxonomists’ (or naturalists’) judgment, and the ‘somewhat arbitrary’ nature of the decision. The main difference is that Darwin concluded from this that species, at least in difficult cases, were somewhat arbitrary, whereas Mayr, although agreeing with this conclusion in practice for species taxa, was somehow still able to conceive of his own theoretical species concept as non-arbitrary. The view of species implied in Mayr’s writings is, in practical terms, therefore only hair-splittingly different from that in Darwin’s. It seems particularly underhand for Mayr to argue that Darwin had an incomplete understanding of species on the basis of the same arguments and indeed almost the same words that Mayr himself uses about the fuzziness of borderlines between doubtful species.

The next quotation used by Mayr is probably the most egregiously tendentious abridgment of the whole crop:

(5) “Varieties have the same general characters as species, for they cannot be distinguished from species.” (Darwin 1859: 58)

The complete sentence from which this apparently nonsensical statement is extracted reads (NOTE: [] = omissions, bold text = additions, in Darwin 1872: 47):

Finally [, then,] varieties [have the same general characters as species, for they] cannot be distinguished from species, – except, first[ly], by the discovery of intermediate linking forms[, and the occurrence of such links cannot affect the actual characters of the forms which they connect]; and [except,] secondly, by a certain indefinite amount of difference between them [, for two forms, if differing very little, are generally ranked as varieties, notwithstanding that intermediate linking forms have not been discovered]; but the amount of difference considered necessary to give to two forms the rank of species is quite indefinite (Darwin 1859: 58–59, Darwin 1872: 47).

This represents the beginning of a two-page conclusion to Chapter II, on “Variation under Nature.” Darwin has been continuing to document how systematists differ in assigning taxa as species or varieties, thus providing further evidence for transmutation of varieties into good species with gaps between them. Darwin points out some other interesting patterns also relevant to transmutationist ideas, for instance that varieties have more restricted distributions than good species, and that species in larger genera (i.e. with more species) tend to be more similar (i.e. more like varieties) than species in smaller genera, as might be expected if rampant evolution of varieties continued into similar diversification of species (Browne 1980). The four pages 56–59 are headed SPECIES OF LARGE GENERA—RESEMBLE VARIETIES.

The major misunderstanding perpetrated by Mayr’s abridgment is the omission of Darwin’s first exception; the resultant abbreviated quotation then seems to mean almost the exact opposite of what Darwin intended. Darwin is clearly saying, here, that varieties do differ from species by “the discovery of intermediate linking forms….” The “– except, firstly…” section must be read to avoid making a nonsense out of what Darwin is attempting to say! The second exception is of course again Darwin’s argument for use of “degree of difference” in doubtful cases (as did Mayr). Interestingly, another commentator has used a different extreme abbreviation of the above sentence, “… the amount of difference considered necessary to give to two forms the rank of species is quite indefinite” (Kottler 1978: 291) as similar evidence for Darwin’s apparent nihilism. I think it is quite clear what Darwin intended throughout this chapter, and in this concluding sentence as well. He was discussing the difficulty of actual taxonomic decisions in doubtful intermediate cases. He did not base his whole concept of species on an arbitrary degree of difference. His species were instead varieties that had evolved gaps in morphology.

A different kind of misreading is often done with Darwin’s chapter VIII, Hybridism, as I have previously argued (Mallet 2008b). Here is the next quotation used by Mayr (1982: 267):

(6) “It can thus be shown that neither sterility nor fertility affords any [clear] certain distinction between species and varieties” (Darwin 1859: 248, Darwin 1872: 237. Also used by Hull 1967: 336)

Darwin is actually arguing here against the prevailing view, most notably from Buffon, for special creation of species on the grounds of unbridgeable gap of sterility. However, he starts by seeming to state the converse:

“The fertility of varieties, that is of the forms known or believed to have descended from common parents, when intercrossed, and likewise the fertility of their mongrel offspring, is, on my theory, of equal importance with the sterility of species; for it seems to make a broad and clear distinction between varieties and species” Darwin 1859: 246).

It seems to make a clear distinction, and Darwin agrees there is a good correlation between hybrid sterility or inviability and species status. But, he continues, there are cases of sterility within species, and cases of fertility between species. Because of our knowledge of similar cases of mismatch, evolutionary biologists today agree with Darwin that sterility and inviability does not make an absolutely clear distinction between species (Gourbière and Mallet 2010). Darwin is not at all arguing that that reproductive isolation of species is unimportant, but instead that the lack of a precise correlation with reproductive isolation merely demonstrates the evolutionary continuity of sterility among species and varieties (Kottler 1978).

The final quotation used by Mayr is from Chapter XIV, the Recapitulation and Conclusion of The Origin:

(7) “In short, we shall have to treat species in the same manner as those naturalists treat genera, who admit that genera are merely artificial combinations made for convenience” (Darwin 1859: 485. Also used by Hull 1967: 336; Ghiselin 1969: 91, Dobzhansky 1970: 352; Kottler 1978: 292; Coyne and Orr 2004: 10; McOuat 1996: 474; Ereshefsky 2009: 4!)

Once again we come back, in the summary of the whole book, to problems already dealt with about Chapter II (Mayr’s Darwin quotations 1–5, above). Mayr again ignores Darwin’s statements on species in the earlier chapter. Mayr even ignores what Darwin said clearly about species further up on this same page 485 (already cited in the section on Darwin’s view of species): “… varieties … are known, or believed, to be connected at the present day by intermediate gradations, whereas species were formerly thus connected.” Quoted out of context, Mayr’s abridgement appears to attribute to Darwin an utterly vacuous view of species. But the argument of Chapter II, summarised further up on p. 485, is that species are distinct from varieties by having gaps in variation between them, although intermediates are common, and it is difficult to make the actual distinction at the boundary between species and varieties in such doubtful cases. Hence, species are as difficult to define as genera for exactly the same reasons of evolutionary continuity. Darwin stressed it like this because, as before, he was trying to persuade the reader that species evolved from varieties, and that genera evolved from species in the same way (Ghiselin 1969; Kottler 1978; Beatty 1985; Stamos 2006). The argument makes as much sense today as it did to Darwin.

Taken in context, therefore, these abridged quotations fail to prove Mayr’s thesis. They show neither that Darwin believed all species were continuous with one another, nor that Darwin significantly changed his mind about what species were in the years leading up to The Origin (see also Ghiselin 1969; Sulloway 1979).