Thomas Huxley identified as Darwin's ‘weak point’ the failure of breeders when crossing varieties within a species to simulate the sterility of hybrids derived from crosses between allied species. As a result of the sterility, the parents of a hybrid were, in an evolutionary sense, reproductively isolated from each other, so they would be members of distinct species. In his theory of ‘physiological selection’, Romanes postulated germline ‘collective variations’ that accumulate in certain members of a species; these members are thus ‘physiological complements’ producing fertile offspring when mutually crossed, but sterile offspring when crossed with others. Unlike Darwin's natural selection, which secured reproductive isolation of the fit by elimination of the unfit, physiological selection postulated variations in the reproductive system that were not targets of natural selection; these sympatrically isolated the fit from the fit, leaving two species where initially there had been one. Bateson approved of physiological selection. He noted that Mendel's ‘unit characters’ were ‘sensible manifestations’ of what we now refer to as ‘genes’, but postulated a ‘residue’, distinct from genes, that might affect gene flow between organisms and so originate species. The reproductive isolation of the parents of a sterile hybrid was due to two complementing non-genic factors (the ‘residue’) separately introduced into the hybrid by each parent. Modern studies, especially of yeast hybrids, support the Romanes–Bateson viewpoint.
Many organisms repeat the cycle adult–gametes–zygote–adult through the generations. When lineages diverge, this cycle is interrupted and two separate cycles result. The interruption—a potential origin of species—can occur at any stage of the cycle, either prezygotically when gametes meet to form a zygote, or postzygotically when the zygote develops into an adult that can then form gametes. Because each stage requires the action of specific gene products, it follows that changes in certain genes might lead to cycle interruption and divergence into two reproductively isolated lines.1 However, ‘speciation genes’ have been hard to identify,2 and a classical example has recently been questioned.3
The purpose of this paper is not to question the genic view but to remind readers of a non-genic view suggested in 1886 by George Romanes, who was Charles Darwin's research associate for eight years before the latter's death in 1882. This view was further developed by William Bateson, who in 1900 brought Mendel's now famous 1865 paper to the attention of the English-speaking world. In particular, Romanes and Bateson noted what Thomas Huxley had referred to as ‘the weak point’ in Darwin's theory.4 If offspring could be obtained from an inter-species cross they were usually sterile (hybrid sterility), but no breeder had ever produced new forms from intra-species crosses that could be so characterized. Furthermore, in proposing that evolution proceeded smoothly without jumps, punctuations or discontinuities, Darwin seemed to have imposed on himself ‘an unnecessary difficulty’.5
Whereas the work of Mendel went unnoticed for a mere 35 years, the views of Romanes and Bateson were disparaged or went unnoticed for more than a century. This was due partly to the twentieth century's obsession with genes but also to the fact that they were struggling with novel terminology. With much of this (for example ‘allele’ and ‘homozygote’) we are now familiar. But terms such as ‘collective variation’ and ‘residue’, now seen as highly relevant to speciation studies,6 have largely disappeared from view. Proceeding chronologically from the late Victorian era to modern times, I here reintroduce the latter terms and, through textual analyses of selective quotations,7 let Romanes and Bateson retell their story.8
Bateson approved of ‘an additional suggestion’
In the spring of 1886 William Bateson set off on an 18-month scientific expedition to the Russian steppes with the intention of catching up with the relevant literature on his return. However, in the autumn his sister Anna, who was then working with Francis Darwin, dispatched three consecutive issues of Nature containing a serialized May address to the Linnean Society. Here Romanes had made an ‘additional suggestion on the origin of species’ that he named ‘physiological selection’, or ‘evolution of species by independent variation’.9 This had raised a storm of criticism from the senior Darwinians (Alfred Wallace, Thomas Huxley and Joseph Hooker) and their junior surrogates (Francis Darwin, William Thiselton Dyer, E. Ray Lankester and Raphael Meldola). But the response of the 25-year-old Bateson (Kasalinsk, 4 December 1886) indicated tempered approval:
Thanks for those ‘Natures’. I don't agree with you that Romanes' paper is poor. It seems a fair contribution and at all events does, as he says, put the whole view on a much more logical basis. The scheme thus put will at least work logically while the other, as left by Darwin, would not. Of course, as to the novelty of the suggestion I know nothing, and I don't much care. I did not suppose Romanes would ever write as good a paper. … It is a straight forward, commonsense suggestion.10
Another young English biologist, the 27-year-old Joseph Cunningham, was also likely to have approved (see below).
Cryptic variability of the reproductive system
Darwin viewed hybrid sterility as a puzzling negative trait that should have been countered by natural selection.11 In his Linnean address Romanes went beyond this, pointing out that, apart from variations between individuals that we can easily detect (for example differences in eye colour), there are likely to be variations that we cannot easily detect. Some variations in parental gonads might ultimately be detected by their conferral of the sterility phenotype on the otherwise healthy offspring of certain pairs. This would designate the parents as reproductively isolated from each other. The partner-specific reproductive-isolation phenotype of the parents would be manifested as the sterility phenotype of their offspring. In Romanes's view, the establishment of this form of reproductive isolation—isolation of the fit from the fit—would in many cases have been critical for branching into two species, with or without the subsequent intervention of natural selection that would isolate (by elimination) the unfit from the fit (linear, non-branching, evolution).
Romanes's physiological selection was an abstraction for which there was then no cytological or biochemical basis. To give his Victorian audience an example of one form of physiological selection, Romanes pointed to a variation that might lead a plant to flower earlier than most members of its species. Early-flowering forms would be reproductively isolated from late-flowering forms by a temporal barrier. At an early stage pollen kept from an early-flowering form would still be capable of fertilizing flowers of late-flowering forms. Over time, incompatibilities between early pollen and late ovules would arise randomly, and this mutual incompatibility (a further barrier) would eventually define the two forms as distinct species. Today we attribute allochronic and gamete-incompatibility barriers, as we attribute allopatric barriers, to differences in genes. But Romanes did not think that this form of variation would have operated generally to originate species:
In many cases, no doubt, this … variation, has been caused by the season of flowering or of pairing having been either advanced or retarded in a section of a species, or to sundry other influences of an extrinsic kind; but probably in a still greater number of cases it has been due to what I have called intrinsic causes, or to the ‘spontaneous’ variability of the reproductive system itself.12
Romanes felt no obligation to clarify intrinsic causes further: ‘It is enough for the explanation which is furnished by Mr. Darwin's theory of the evolution of adaptive structures by natural selection, that the variations in question take place; and similarly as to the present theory of the evolution of species by physiological selection’.13 However, he was quite prepared to agree that this form of variation could proceed continuously as Darwin had proposed for the evolution of adaptations:
Starting from complete fertility within the limits of a single parent species, the infertility between derivative or divergent species, at whatever stage in their evolution this began to occur, must usually at first have been well-nigh imperceptible, and thenceforth have proceeded to increase stage by stage. … Does it not therefore become … in a high degree probable, that from the moment of its inception this isolating agency must have played the part of a segregating cause, in a degree proportional to that of its completeness as a physiological character?14
Collective variation of a population subset
Anticipating modern developments in population genetics, Romanes thought that the slow increase in his postulated independent variation of the reproductive system might reflect its ‘collective’ nature, in that it would affect a distinct lineage within a population. One of the misconceptions of his opponents was
that I imagine physiological varieties always to arise ‘sporadically’, or as merely individual ‘sports’ [mutations] of the reproductive system. On the contrary, I expressly stated that this is not the way in which I suppose the ‘physiological variation’ to arise, when giving origin to a new species; but that it arises, whenever it is effectual, as a ‘collective variation’ affecting a number of individuals simultaneously, and therefore characterizing ‘a whole race or strain’.15
Free intercrossing would have tended to swamp or blend the sporadically appearing variations on which natural selection might act. But Romanes's collective ‘independent variation’ of the reproductive system—postulated to be a ‘general variability … about a mean’ (for example, as human heights form a normal distribution)—was held to militate against this:
I am guilty of no inconsistency when thus arguing for a ‘collective variation’ on the part of the reproductive system, after having urged the difficulty against natural selection which arises from free intercrossing—i.e. the difficulty of supposing that a sufficient number of variations of the same kind should always be forthcoming simultaneously to enable natural selection to overcome the influence of free intercrossing. For, as previously explained, this objection is only valid in the case of ‘accidental’, ‘sporadic’, or ‘spontaneous’ variations, which, ex hypothesi, are relatively very few in number. The objection does not apply to ‘collective variations’, which, being due either to a common cause or to general variability of size, etc, about a mean, affect a number of individuals simultaneously.16
Remarkably, two of Romanes's sternest critics provided valuable guidance on terminology. Thiselton Dyer17 suggested the term ‘reproductive isolation’. Wallace18 noted that two individuals that had each become reproductively isolated from members of their main species (with which they might cross to produce healthy but sterile offspring) might produce healthy and fertile offspring when mutually crossed. Hence the parents could be considered as ‘physiological complements’.
Another critic, Huxley, failed to recognize that his ‘weak point’ criticism of Darwin had been met.19 Romanes had distinguished two types of variation: overt sporadic variations that might lead to the evolution by natural selection of better-adapted forms (which the breeder might capture and selectively pair), and cryptic collective variations that might lead to the evolution of species by physiological selection (which the breeder would find hard to simulate).
Sporadic and regular sterilities
Romanes died at the age of 46 years in 1894, the year in which Bateson published a major treatise: Materials for the study of variation, treated with especial regard to discontinuity in the origin of species.20 At that time, in keeping with Huxley, Bateson saw the origin of species as a discontinuous process, similar to that manifested as the sudden arising, in one generation, of a new variety of flower with one perfect extra petal. The suddenness of the emergence implied a discontinuous underlying mechanism uninfluenced by natural selection. The book was warmly reviewed by the fish biologist Joseph Cunningham, who noted similarities to Romanes's physiological selection theory but declared Bateson's argument to be ‘defective’ because there was ‘no necessity for discontinuity of variation to explain discontinuity of species’.21
Like various continental botanists (Hugo de Vries, Carl Correns and Erich von Tschermak), in the 1890s Bateson and E. Rebecca Saunders had begun crossing various lines of plants and animals and scoring the inheritance of characters among the progeny. Following the discovery of Mendel's work in 1900, Bateson became its leading advocate in the English-speaking world. Given the intense opposition he faced from the mathematical biologists (‘biometricians’), it is not surprising that his attention was directed more to verifying Mendel's laws than to pronouncing on their cellular basis. However, in October 1902 at the Second International Conference on Plant Breeding and Hybridization, in New York, he noted: ‘We have reason to believe that the chromosomes of the father plant and mother plant, side by side, represent blocks of parental characters.’22
In December 1901 Bateson and Saunders had submitted a detailed 160-page report to the Evolution Committee of the Royal Society, to which they made minor amendments in March 1902.23 The report noted that the classical sterility of the hybrids resulting from a cross between species that were believed to have recently diverged from a common ancestor (allied species) did not follow a Mendelian pattern of character assortment among offspring. Although the offspring might have inherited some conventional character, such as colour or height, in a Mendelian fashion (for example a 3 : 1 ratio), usually the same offspring would all inherit the sterility phenotype (figure 1). At that time they had to admit:
We know of no Mendelian case in which fertility is impaired. We may, perhaps, take this as an indication that the sterility of certain crosses is merely an indication that they cannot divide up the characters among their gametes. If the parental characters, however dissimilar, can be split up, the gametes can be formed. … That the sterility of hybrids is generally connected in some way with inability to form germ-cells correctly … is fairly clear, and there is in some cases actual evidence that this deformity of pollen grains in hybrids is due to irregularity or imperfection in the processes of division from which they result.24
Thus, the hybrid sterility phenotype that resulted from a cross between allied species was something intrinsic to an organism and did not relate to extrinsic environmental elements. That they were thinking of an imperfection in the pairing of homologous parental chromosomes is indicated by their citing Guyer, who ‘in ignorance of Mendel's work’ had independently derived Mendel's laws from the cytology of spermatogenesis in pigeon hybrids.25 Furthermore, early in 1902 Bateson noted:
It is impossible to be presented with the fact that in Mendelian cases the cross-bred produces on an average equal numbers of gametes of each kind, that is to say, a symmetrical result, without suspecting that this fact must correspond with some symmetrical figure of distribution of those gametes in the cell-divisions by which they are produced.26
There was repeated reference to Guyer in Bateson's later works.27
However, Bateson and his colleagues soon came across cases of infertility that followed Mendelian patterns of inheritance (figure 2). Their second report to the Evolution Committee in 190528 drew a clear distinction between this unpredictable sporadic sterility seen among the offspring of crosses between closely related individuals, and the predictable sterility seen among the offspring of crosses between distantly related individuals (that is, members of allied species):
Contabescent [withered] anthers were seen from time to time in many families. … This sporadic sterility has not been particularly studied. It is interesting to compare this example of the definite appearance of sterility … with the familiar occurrence of sterility in cross-breds. Such a phenomenon has often been supposed to indicate remoteness of kinship, yet here a closely comparable effect occurs in F2 as the result of a cross between two types which must be very nearly related. Mr. Gregory in a careful examination of the pollen-genesis, found that the divisions were normal up to the reduction division, when the chromosomes form shapeless knots and entanglements, failing to divide.29
Today we would interpret the latter sterility as a malfunction due to mutation in a gene determining one of the many cell components required for anther development. In this case the component seemed to be required for the reduction division of meiosis. Whatever the ultimate basis of the sterility, Bateson and his colleagues pointed out that this sporadic event arising from a within-species cross (unpredictable in that it had not been expected when the cross was first made) contrasted with the regular (predictable) F1 sterility appearing when allied species in general were crossed. Only the former displayed a Mendelian (that is, genic) pattern of inheritance. Indeed, in one case the sterility character was found to be coupled (linked) to another character, leaf axil colour, that displayed Mendelian inheritance (table 1).
In 1902 Bateson and Saunders recognized that Mendel's unit characters were ‘the sensible manifestations of physiological units of as yet unknown nature’.30 Although Bateson did not begin to use the word ‘gene’ until the second decade of the twentieth century, it is employed here when referring to the Mendelian ‘physiological units’ that determine characters.
Chromosomes and the residue or irresoluble base
Bateson was among the first to see a link between Mendelian ‘genes’ and chromosomes, and he cited Guyer in this context.31 However, as evidence for a chromosomal location became stronger, Bateson's doubts increased. It was not a question of Bateson's not seeing the wood for the trees. His idea of what constituted the wood differed from that of others. They saw a collection of genes; he saw the genes plus something else that was in some way related to the question of the origin of species. What was the something else and where was it located? Was it on the chromosomes, like the Mendelian factors? Or was it elsewhere, perhaps outside the nucleus in the cytoplasm? No clear evidence on this had emerged by 1926, the year of Bateson's death. Thus his pronouncements on chromosomes were always carefully hedged.32
That the story was somehow incomplete was made explicit early in 1902: ‘Has a given organism a fixed number of unit characters? Can we rightly conceive of the whole organism as composed of such unit characters, or is there some residue—a basis—upon which the unit characters are imposed?’33 This was expressed in slightly different form a few months later:
From the fact of the existence of interchangeable [allelic] characters we must, for purposes of treatment, and to complete the possibilities, necessarily form the conception of an irresoluble base [that is, a base not resolvable by Mendelian analysis], though whether such a conception has any objective reality we have no means as yet of determining.'34
The report of Bateson and Saunders linked the concept to Darwin's great question, the nature of the origin of species—a ‘phenomenon’ that did not ‘attach to’ the elements (genes) that determined allelic characters:
We know, of course, that we cannot isolate this residue from the unit characters. We cannot conceive a pea, for example, that has no height, no colour, and so on; if all these were removed there would be no living organism left. But while we know that all these characters can be interchanged [through breeding experiments], we are bound to ask is there something not thus interchangeable? And if so, what is it? We are thus brought to face the further question of the bearing of Mendelian facts on the nature of Species. The conception of species, however we may formulate it, can hardly be supposed to attach to allelomorphic or analytical varieties [genes]. We may be driven to conceive ‘Species’ as a phenomenon belonging to that ‘residue’ spoken of above, but on the other hand we get a clearer conception of the nature of sterility on crossing.35
Two factors must complement to produce sterility
Bateson was considering the sterile offspring of crosses between allied species that were presumed to have derived from a common ancestral species. Because the offspring of crosses between members of that ancestral species would have been fertile (otherwise there would have been no descendants), the hybrid sterility revealed the emergence of a reproductive barrier between the descendent species (that is, an interruption of the unitary generational cycle). This could have been an originating barrier leading to the state of reproductive isolation that defined them as distinct species. With little indication that he was writing about chromosomes, the residue or an irresoluble base, Bateson developed this theme abstractly in an essay that he contributed to the Darwin centenary celebration in 1909.36 Here he concluded that ‘Failure to divide [to produce gametes] is … the immediate “cause” of the sterility’, so that ‘we are justified in supposing that there are factors which can arrest or prevent cell division.’37 Thus, ‘When two species, both perfectly fertile severally, produce on crossing a sterile progeny, there is a presumption that the sterility is due to the development in the hybrid of some substance which can only be formed by the meeting of two complementary factors … ’ (figure 3a). Applying this line of reasoning to what would seem to be a single species, Bateson continued:
We see that the phenomenon could only be produced among the divergent offspring of one species by the acquisition of at least two new factors; for if the acquisition of a single factor caused sterility the line would then end. Moreover each factor must be separately acquired by distinct individuals, for if both were present together, the possessors would by hypothesis be sterile. And in order to imitate the case of species, each of these factors must be acquired by distinct breeds. The factors need not, and probably would not, produce any other perceptible effects; they might, like the colour-factors present in white flowers, make no difference to the form of other characters. Not until the cross was actually made between the complementary individuals would either factor come into play, and the effects even then might be unobserved until an attempt was made to breed from the cross-bred.38
Thus, the factors (say, Z′) that distinguished certain members of a species from their fellows (bearing, say, Z) would be latent. They would become patent, revealing a sterility-of-offspring phenotype, only if by chance there were a cross between certain individuals that had come to differ in the factors (Z′ and Z; not Z′ and Z′, or Z and Z). At least one of the individuals would be rare, because the normal abundant types were generally fertile when intercrossed (that is, no role was ascribed to Z in the presence of Z, or to Z′ in the presence of Z′). How often could this happen?
If the factors responsible for sterility were acquired, they would in all probability be peculiar to certain individuals and would not readily be distributed to the whole breed. Any member of the breed into which both the factors were introduced would drop out of the pedigree by virtue of its sterility. Hence the evidence that various domesticated breeds, say of dogs or fowls, can when mated together produce fertile offspring, is beside the mark. The real question is, Do they ever produce sterile offspring? I think the evidence is clearly that sometimes they do, oftener perhaps than is commonly supposed.39
Sterility of offspring being a parental phenotype, the fact that a completely sterile offspring could not be subjected to further breeding analysis would not matter. The parents of the offspring complemented each other sufficiently to produce the phenotype, but the complementary factor of one parent (say, Z′) might be more prone to produce the phenotype than the complementary factor of the other (say, Z). Through segregation (further cross-breeding of each parent with other individuals) these complementary factors might be investigated.
In his 1909 essay, Bateson considered two sterility factors working together (complementing) to impede fertility (figure 3a). However, he later noted that organisms could be reproductively incompatible because the reproductive system of ‘each is lacking in one of two complementary elements’ that promote fertility (figure 3b).40 This view, reminiscent of Romanes's, was later adopted by Richard Goldschmidt, who proposed that normally parents contribute complementary factors (for example Z and Z) making parental chromosomes compatible at meiosis in their hybrids, which are therefore fertile (that is, the parental factors work together to produce a positive effect). When the factors are not sufficiently complementary (for example Z and Z′) the parental chromosomes are incompatible in their hybrids, which are therefore sterile.41
Complementation like sword and scabbard
Bateson persisted with his Huxleyan idea that the sterility of a hybrid resulting from a cross between allied species was ‘a distinction in kind, of a nature other than those we perceive among our varieties’.42 And he was still attached to the Huxleyan idea of discontinuous variation. In December 1921 he gave his famous address ‘Evolutionary faith and modern doubts’ at the Toronto meeting of the American Association for the Advancement of Science:
That particular and essential bit of the theory of evolution which is concerned with the origin and nature of species remains utterly mysterious. We no longer feel … that the process of variation now contemporaneously occurring is the beginning of a work which needs merely the element of time for its completion; for even time cannot complete that which has not yet begun. The conclusion in which we were brought up, that species are a product of a summation of variations, ignored the chief attribute of species that the product of their crosses is frequently sterile in greater or less degree. Huxley, very early in the debate, pointed out this grave defect in the evidence, but before breeding researches had been made on a large scale no one felt the objection to be serious.43
A subsequent interchange with C. R. Crowther is of particular interest.44 Questioning Bateson's attitude to the mechanism of meiotic chromosome pairing (figure 4), Crowther began by noting that, although parental chromosomes had to cooperate for development of the zygote from embryo to adult, a far higher degree of cooperation would be needed when the chromosomes paired (conjugated) in the gonad of that adult:
Homologous chromosomes … have to co-operate to produce the somatic cell of the hybrid, and their co-operation [for this purpose] might be expected to require a certain resemblance, but for the production of sexual cells [gametogenesis] they must do more, they must conjugate; and for conjugation it is surely reasonable to suppose that a much more intimate resemblance would be needed.
We might, therefore, expect, on purely theoretical grounds, that as species and genera gradually diverged, it would be increasingly difficult to breed a hybrid between them; but that, even while a hybrid could still be produced, a fertile hybrid would be difficult or impossible, since the cells of the germ-track would fail to surmount the meiotic reduction stage, when the homologous chromosomes conjugate. This is exactly what happens: the cells go to pieces in the meiotic phase.
Bateson's disparagement of the idea that species might be ‘a product of a summation of variations’ left Crowther ‘frankly puzzled’, for ‘the proposition is certainly not self-evident.’ Surely, if the sterility of an offspring were due to a failure within that offspring of homologous chromosomes to conjugate, it mattered little whether the lack of complementarity responsible for that failure was produced by one large variation or by the summation of many smaller variations. That Crowther was thinking of primary variations occurring at the chromosomal level, rather than anatomical variations of the sterile individual, was explicit:
If a sword and its scabbard are bent in different directions, it will happen sooner or later that the sword cannot be inserted, and the result will be the same whether the bending be effected by a single blow, or whether it be, in Dr. Bateson's words, ‘a product of a summation of variations.’ Is this illustration inapt? The sword and its scabbard are the homologous chromosomes. … it seems easier to imagine sterility arising from a gradual modification, spread over a length of time, and involving many chromosomes, …
Bateson conceded that discontinuity of variation was not critical:
It is … not difficult to ‘imagine’ interspecific sterility produced by a gradual (or sudden) modification. That sterility might quite reasonably be supposed to be due to the inability of certain chromosomes to conjugate, and Mr. Crowther's simile of the sword and the scabbard may serve to depict the sort of thing we might expect to happen. But the difficulty is that we have never seen it happen to swords and scabbards which we know to have belonged originally to each other. On the contrary, they seem always to fit each other, whatever diversities they may have acquired.45
Modern chromosomal views
In his 1909 essay Bateson did not spell out the relation between his postulated complementary sterility factors and the above ‘residue’ or ‘irresoluble base’. In Bateson's mind not only was the ‘residue’ distinct from genes—the agencies determining the ‘transferable characters’ that were the subject of Mendelian analysis—but it could also limit the extent to which organisms could exchange genes. This limitation (that is, the absence of gene flow) would be complete when the organisms belonged to independent species:
These transferable characters are attached to or implanted upon some basal organization, and the attributes of powers which collectively form that residue may perhaps be distinguished from the transferable qualities. The detection of the limits thus set upon the interchangeability of characters would be a discovery of high importance and would have a most direct bearing on the problem of the ultimate nature of Species.46
Bateson agreed with Crowther that a fundamental form of reproductive isolation, manifested as the hybrid sterility seen when allied species were crossed, was due to an incompatibility that could be characterized cytologically as impaired pairing of paternal and maternal chromosomes at meiosis. It was inferred that if we can understand what makes chromosomes incompatible, then we can understand hybrid sterility. And if we can understand hybrid sterility, we can understand an origin of species. But how do chromosomes that are homologous (that is, are alike) pair with each other? Do they pair by virtue of this likeness (like with like), of by virtue of some key-in-lock (sword-in-scabbard) complementarity, which implies that they are not really alike? One must be the sword and the other the scabbard.
This paradox was resolved when it was appreciated that hereditary information was stored and transmitted as duplex DNA with two strands—a ‘Watson’ strand and a ‘Crick’ strand—that paired with each other by virtue of base complementarity.47 So, in Crowther's terminology, potentially the sword strand of one chromosome can pair with the scabbard strand of the homologous chromosome (and vice versa). For this purpose, swords have to be unsheathed from their own scabbards and then each inserted into the scabbards of the other. Thus, the Watson strand of one chromosome can pair with the Crick strand of the other, and vice versa. This requires that the Watson strand be displaced from pairing with the Crick strand of its own chromosome. Similarly, the Crick strand of the homologous chromosome must be displaced from pairing with the Watson strand of its own chromosome. Then cross-pairing (homology search without strand breakage) can occur, as Crick himself proposed.48
The pairing requires complementarity of DNA base sequences. A sporadically appearing change in a certain base could, if dominant, introduce a new phenotype (such as an extra petal) but would not greatly affect the overall complementarity between parental chromosomes. However, over time, base changes, including some affecting the classical phenotype, could accumulate. Romanes's ‘collective variation’ that would build up ‘in a whole race or strain’ can now be interpreted as the variation of the base composition of DNA about some characteristic value for the species (that is, a normal distribution). When differences between chromosomal homologues reached a critical value, meiotic pairing would be impaired. A possible mechanism for this is described elsewhere49 and is summarized in figure 5. Indeed, assuming experiments with laboratory strains to be relevant to natural yeast populations, such ‘simple sequence divergence’ seems to be the predominant form of species initiation in yeast.50 The initiation might later be reinforced by segmental chromosomal changes that, in some circumstances, could themselves be capable of initiation, as described elsewhere.51
In the twentieth century the writings of Romanes and Bateson on the origin of species were either disparaged or, more usually, ignored.52 However, we can now see them as latter-day ‘Mendels’ whose recognition of the non-genic nature of the hybrid sterility arising from crosses between allied species anticipated by a century modern developments in genome analysis. Although genic differences differentiate species, the spark that originates species can be non-genic. Bateson's non-genic ‘residue’ is not in the cytoplasm but is ‘attached to or implanted upon’ the chromosomes, where the genes reside. Here mutations corresponding to the ‘collective variations’ of Romanes can accumulate, eventually to exceed a critical value in a population subset (the difference between Z and Z′ in the terminology of figure 3). In this event a major discontinuity—an origin of species—can result. We can now see how this might have come about at the DNA level. Further questions—whether, in the general case, genic changes have sparked species originations more often than non-genic changes, and whether the latter have involved multiple base changes more frequently than gross karyotypic changes—are not argued here. The point is that, until controverted, the Romanes–Bateson hypothesis deserves at least an equal place at the table with other hypotheses.
The invitations of the Organizing Committee of the John Innes Centenary Symposium (K. Roberts, C. Lamb, D. Hopwood, E. Coen, S. Wilmot, P. Nurse and W. Bodmer) and of the organizers of the Galton Institute Conference on William Bateson (T. M. Cox and M. Keynes) are greatly appreciated. The recent decease of Milo Keynes is sadly noted. Queen's University hosts my Web pages, where full-text versions of some of the cited papers, including the relatively inaccessible texts of Guyer, may be found (http://post.queensu.ca/~forsdyke/guyer.htm).
This article is based on an address entitled ‘Bateson's contributions to evolutionary theory’ delivered at the John Innes Centenary Symposium on 9 September 2009, and at the Galton Institute Conference ‘William Bateson: his Exceptions and the Origin of Species Revisited’ at the Royal Society on 1 October 2009. Online versions of the addresses are available at the Web sites of the John Innes Centre (http://www.jic.ac.uk/centenary/events/historyofgenetics/index.htm) and the Galton Institute (http://www.galtoninstitute.org.uk/).
↵1 T. Dobzhansky, Genetics and the origin of species (Columbia University Press, 1937), pp. 228–258; H. J. Muller, ‘Isolating mechanisms, evolution and temperature’, Biol. Symp. 6, 71–125 (1942).
↵2 E. J. Louis, ‘Origins of reproductive isolation’, Nature 457, 549–560 (2009); D. Greig, ‘Reproductive isolation in Saccharomyces’, Heredity 102, 39–44 (2009).
↵3 M. Schartl, ‘Evolution of Xmrk: an oncogene, but also a speciation gene?’, BioEssays 30, 822–832 (2008).
↵4 T. H. Huxley, Letter to Kingsley, 30 April 1863, in Life and letters of Thomas Henry Huxley (ed. L. Huxley) (Appleton, New York, 1901), vol. 1, p. 257; W. Bateson, ‘Huxley and evolution’, Nature 115, 715–717 (1925).
↵5 T. H. Huxley, Letter to Darwin, 23 November 1859, in Life and letters of Thomas Henry Huxley (ed. L. Huxley) (Appleton, New York, 1901), vol. 1, pp. 188–189.
↵6 D. R. Forsdyke, Evolutionary bioinformatics (Springer, New York, 2006), pp. 123–180; Louis, op. cit. (note 2); Greig, op. cit. (note 2).
↵7 Today's readers cannot easily turn to nineteenth-century texts without guidance. For example, the words ‘genetics’ and ‘virus’ were used in various contexts several decades before attaining their modern meanings. Yet failure to read early texts (as did many biologists in the 35 years before the ‘rediscovery’ of Mendel's work) can lead to the reinvention of many wheels (as did de Vries, Correns and Tschermak in the 1890s).
↵8 D. R. Forsdyke, The origin of species, revisited. A Victorian who anticipated modern developments in Darwin's theory (McGill–Queen's University Press, Montreal, 2001); A. G. Cock and D. R. Forsdyke, ‘Treasure your exceptions.’ The science and life of William Bateson (Springer, New York, 2008).
↵9 G. J. Romanes, ‘Physiological selection. An additional suggestion on the origin of species’, J. Linn. Soc. (Zool.) 19, 337–411 (1886a); G. J. Romanes, ‘Physiological selection. An additional suggestion on the origin of species’, Nature 34, 314–316, 336–340, 362–365 (1886b).
↵10 W. Bateson, Letter to Anna Bateson, 4 December 1886, in The William Bateson Papers, section G1b (item 26 in folder 101–150), Archives of Queen's University, Kingston.
↵11 C. Darwin, The variation of animals and plants under domestication (John Murray, London, 1875), vol. 2, pp. 170–171; Forsdyke, op. cit. (note 8), pp. 27–38. Darwin's error was to emphasize hybrid sterility as a character of a sterile individual, rather than of the parents of that individual.
↵12 Romanes (1886a), op. cit. (note 9), p. 400; emphasis added by the present author.
↵13 Romanes (1886a), op. cit. (note 9), p. 411.
↵14 G. J. Romanes, Darwin, and after Darwin (Longmans, Green & Co., London, 1897), pp. 43–44.
↵15 Romanes, op. cit. (note 14), p. 60.
↵16 G. J. Romanes, ‘Physiological selection’, Nineteenth Century 21, 59–80 (1887).
↵17 W. T. Thiselton Dyer, ‘Mr. Romanes's paradox’, Nature 39, 7–9 (1888).
↵18 A. R. Wallace, ‘Physiological selection and the origin of species’, Nature 34, 467–468 (1886).
↵19 Forsdyke, op. cit. (note 8), pp. 222–229.
↵20 W. Bateson, Materials for the study of variation, treated with especial regard to discontinuity in the origin of species (Macmillan, London, 1894).
↵21 J. T. Cunningham, ‘The origin of species among flat-fishes’, Nat. Sci. 6, 169–177, 234–239 (1895).
↵22 W. Bateson, ‘Practical aspects of the new discoveries in heredity’, Mem. Hort. Soc. New York 1, 1–9 (1904). The conference ran from 30 September to 2 October 1902. Bateson spoke on the first day. His comment on chromosomal localization was made in the discussion after a paper presented for W. A. Cannon on 1 October (p. 123).
↵23 W. Bateson and E. R. Saunders, ‘Experimental studies on the physiology of heredity’, Rep. Evol. Cttee R. Soc. 1, 1–160 (1902).
↵24 Bateson and Saunders, op. cit. (note 23), pp. 148–149.
↵25 M. F. Guyer, ‘Spermatogenesis in hybrid pigeons’, Science 21, 248–249, 312 (1900).
↵26 W. Bateson, Mendel's principles of heredity. A defence (Cambridge University Press, 1902), p. 30.
↵27 D. R. Forsdyke, ‘Two levels of information in DNA. Relationship of Romanes’ “intrinsic” variability of the reproductive system and Bateson's “residue” to the species-dependent component of the base composition, (C + G)%', J. Theor. Biol. 201, 47–61 (1999); P. Bungener and M. Buscaglia, ‘Early connection between cytology and Mendelism: Michael F. Guyer's contribution’, Hist. Phil. Life Sci. 25, 27–50 (2003).
↵28 W. Bateson, E. R. Saunders and R. C. Punnett, ‘Experimental studies on the physiology of heredity’, Rep. Evol. Com. R. Soc. 2, 1–131 (1905).
↵29 Bateson et al., op. cit. (note 28), p. 92.
↵30 Bateson and Saunders, op. cit. (note 23), p. 159.
↵31 Bateson and Saunders, op. cit. (note 23), p. 149.
↵32 Cock and Forsdyke, op. cit. (note 8), pp. 339–377.
↵33 Bateson and Saunders, op. cit. (note 23), p. 148.
↵34 Bateson, op. cit. (note 26), p. 28.
↵35 Bateson and Saunders, op. cit. (note 23), p. 148.
↵36 W. Bateson, ‘Heredity and variation in modern lights’, in Darwin and modern science (ed. A. C. Seward), pp. 85–101 (Cambridge University Press, 1909).
↵37 Bateson, op. cit. (note 36), p. 99.
↵38 Bateson, op. cit. (note 36), pp. 97–98.
↵39 Bateson, op. cit. (note 36), p. 98.
↵40 W. Bateson, Problems of genetics (Yale University Press, New Haven, 1913), p. 241.
↵41 D. R. Forsdyke, ‘William Bateson, Richard Goldschmidt, and non-genic modes of speciation’, J. Biol. Syst. 11, 341–350 (2003).
↵42 Bateson, op. cit. (note 40), p. 237.
↵43 W. Bateson, ‘Evolutionary faith and modern doubts’, Nature 109, 553–556 (1922).
↵44 C. R. Crowther, ‘Evolutionary faith and modern doubts’, Nature 109, 777 (1922).
↵45 W. Bateson, ‘Interspecific sterility’, Nature 110, 76 (1922).
↵46 W. Bateson, Mendel's principles of heredity (Cambridge University Press, 1909), p. 73.
↵47 J. D. Watson and F. H. C. Crick, ‘Genetical implications of the structure of deoxyribonucleic acid’, Nature 171, 964–967 (1953).
↵48 F. Crick, ‘General model for the chromosomes of higher organisms’, Nature 234, 25–27 (1971); J. H. Wilson, ‘Nick-free formation of reciprocal heteroduplexes: a simple solution to the topological problem’, Proc. Natl Acad. Sci. USA 76, 3641–3645 (1979).
↵49 Forsdyke, op. cit. (notes 6 and 27); D. R. Forsdyke, ‘Molecular sex. The importance of base composition rather than homology when nucleic acids hybridize’, J. Theor. Biol. 249, 325–330 (2007).
↵50 Louis and Grieg, op. cit. (note 2).
↵51 M. J. D. White, Modes of speciation (Freeman, San Francisco, 1978); M. King, Species evolution. The role of chromosome change (Cambridge University Press, 1993).
↵52 Cock and Forsdyke, op. cit. (note 8).
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