Evolution SELECTED PAPERS AND COMMENTARY

To really understand evolution we must first understand the historical development of ideas on evolution. But to really understand its history, we must first understand evolution.

OVERVIEW minoan wall decoration showing bird and flowers

Introduction: Species Barriers

Origin of Species (Darwin 1859), Revisited (Romanes and Gulick)

Two Levels of Information in DNA (Romanes and Bateson)

Haldane's Rule

Non-Genic ("Chromosomal") Speciation (Bateson and Goldschmidt)

Grant Allen, George Romanes and Stephen Jay Gould

Heredity as Information Transfer (Butler)

Darwin's 'Weak Point'

SELECTED PAPERS on the Four Black Boxes:

1. Variation

2. Heredity

3. Phenotypic ("Natural") Selection/Isolation

Hybrid Sterility (Darwin 1862)

Variation (Hooker 1862)

Pangenesis (Darwin 1868)

Inutility of Characters (Gulick 1872)

Natural and Artificial Selection (Belt 1874)

Inutility of Characters. Paradox of Sex. Random Drift (Delboeuf 1877)

4. Reproductive ("Physiological") Selection/Isolation

An Unnoticed Factor in Evolution (Catchpool 1884)

Physiological Selection (Romanes 1886)

Physiological Selection (Romanes 1887)
Embryo Transfer (Heape 1890)

"Physiological" Selection/Isolation, the "Chromosomal" basis

Hybridism and the Germ-Cell (Guyer 1900, 1902)

Cytological Basis for the Mendelian Laws (Cannon 1902)

Chromosomes of the Germ Cells (Montgomery 1901)

Chromosomes in Heredity (Sutton 1903)

Two Levels of Genetic Information (Bateson & Saunders 1902)

Heredity and Variation in Modern Lights (Bateson 1909)

A Phenomenon of Arrangement (Bateson 1914)

Chromosomes, Polyploidy and Why Sex Evolved (Winge 1917)

The Blind Watchmaker. Review (1987)

Speciation in Retroviruses (1995)

Origin of Species (1996)

Thinking about Stem-Loops (1998)

Two Levels of Information in DNA (1999)

Haldane's Rule (2000)

Non-Genic (Chromosomal) Speciation (2003)

Allen, Romanes and Gould (2004)

Chromosomal Speciation: A Reply (2004)

Heredity as Information Transfer (2006)

Positive Selection of Synonymous Mutations Initiates Species Divergence (2007)

Darwin's 'Weak Point' (2010)

Acknowledgements

Other Web Sites

Introduction: Species Barriers

The idea of barriers against members of other species was evident in the nineteenth century in the context of infectious disease (Click here). These barriers are both external (e.g. hygiene), and internal (e.g. the immune response). Internally, our bodies ("self") can detect and destroy members of other species ("not-self"; i.e. viruses, bacteria, protozoa).

Another, no less subtle form of self/not-self discrimination, involves our detection of a mate ("near-self") who will be our "physiological complement" such that the union will produce healthy offspring ("hybrids"). An incestuous relationship with a close relative ("too near-self") will probably result in less healthy offspring. On the other hand, extreme out-breeding, such as with an ape (not-self), is prohibited by species barriers.

There is more to this than just the inability to copulate (the gamete transfer barrier). There are both external components (e.g. mate choice), and internal components. Even if the male sperm could meet and fuse with the female ovum, the resulting cell ("zygote") might be unable to grow from embryo to an adult organism (developmental barrier resulting in "hybrid inviability"). Even if these transfer and developmental barriers were overcome, in the gonad (testes, ovary) the two sets of parental chromosomes might be unable to pair for gamete-production (gonadal barrier resulting in "hybrid sterility"). Our modern understanding of these barriers began with Charles Darwin's The Origin of Species (1859).

The debate on the primary mechanism of "speciation" continues to this day. The issues involved are complex.

What are the relative importances of the three barriers (transfer, developmental, gonadal) in keeping species separate ("reproductively isolated")?
Do the barriers appear sequentially, and if so, which appears first?
Are there fewer barriers between allied species, than between distantly related species, or does one barrier just replace another barrier?
Are the barriers we find between closely related (allied) species indicative of the first barriers to appear?
Does a barrier arise suddenly in an all-or-none fashion, or does it arise slowly, so that reproductive isolation is initially only partial?
If one barrier is replaced, does it disappear completely?
Is there a group of species, members of which, for some reason related to their biology, have not progressed beyond the first barrier?
What is the molecular basis of each barrier?
While we recognize that natural selection "succeeds" when more fertile offspring are produced, is there a reproductive barrier that can achieve this as part of a process that, in extreme form, is independent of natural selection?

Four years after the death of Darwin in 1882 a major advance was made by Darwin's close research associate, George John Romanes. Whereas the work of Gregor Mendel (1865) may have been unrecognized until 1900 because of the relative obscurity of its originator and his location, George Romanes was at centre stage.

George Romanes. Painting commissioned by his mother as a wedding present for his wife. 1879.

Ethel Romanes

George Romanes and, his wife and biographer, Ethel Romanes

Photographs of these portraits were kindly provided by their grandson Giles Romanes (also the grandson of Almroth Wright). The portrait on the left is signed by T.H. Huxley's son-in-law, John Collier (1850-1934), who, at Romanes' suggestion, was commissioned by the Linnean Society to provide the famous 1881 portrait of Darwin.

Yet Romanes' contributions to evolutionary theory are only just gaining recognition. Perhaps for the reason given at the top of this page, Biohistorians have not found it easy to tell the story. John Lesch observed in 1975 that:

"The development of evolutionary theory in the two decades from Darwin's death to the turn of the century remains very largely terra incognita for the historian."

William Provine concluded in 1986 that:

"Evolutionary biology in the period 1859-1925 is extraordinary complex".

These web pages makes available some of the primary documentation in the area, so that you can try to sort out the issues for yourself. It is obviously biased towards my own particular evolutionary views, but sites giving alternative perspectives are easily "googled."

D. R. Forsdyke 1998

The Origin of Species, Revisited:

A Victorian who Anticipated Modern Developments in Darwin's Theory

By Donald R. Forsdyke

Queen's Quarterly (1999) 106, 112-133 (With copyright permission from the Editor, Boris Castel.) 106, 112-133 (With copyright permission from the Editor, Boris Castel.)

In his later years Charles Darwin's closest professional relationship was with George John Romanes, to whom he entrusted the burden of his life's work. Four years after Darwin's death, Romanes published a theory of the origin of species by means of "physiological selection". This resolved the major problems in Darwin's theory, but replaced them with a "peculiarity" of the reproductive system which would allow selective fertility between "physiological complements". To most of his contemporaries, and those who came afterwards, this did not convey much. However, bioinformatic analysis of DNA sequence data emerging from genome projects now allows an interpretation. Surprisingly, the words of a "pore flahr gel" can help us understand work which Alfred Wallace, with the unknowing aid of a Kingston lady, had condemned to a century of obscurity.

1848 was a good year for the Reverend George Romanes, professor of classics at Queen's College, Kingston, Ontario. He inherited a "considerable fortune" and his third, and most illustrious son, George John Romanes, was born. The Presbyterian minister had been in Canada for 14 years, and "relieved of any necessity to continue the duties of his chair", he returned to Europe (1850), eventually settling in London.

The children, two surviving boys and two girls, grew up as free spirits. The publication of Charles Darwin's The Origin of Species by Means of Natural Selection when George John was eleven, went unnoticed. Some last-minute private tutoring facilitated George John's entrance to Cambridge University, where he bloomed. His initial interest in theology, gave way to a life-long interest in biology while maintaining his spiritual concerns. The biography relates that he "finally abandoned the idea of a profession" (medicine or the church), and "resolved to devote himself to scientific research."^1,2

In 1874 Romanes published some of his views on evolution in the scientific journal, Nature³. Darwin sent him "a friendly little note" and invited him to visit.

"From that time began an unbroken friendship, marked on one side by absolute worship, reverence, and affection, on the other by an almost fatherly kindness and a wonderful interest in the younger man's work and in his career. ... Mr. Darwin met him, as he often used to tell, with outstretched hands, a bright smile, and a 'How glad I am that you are so young!'"

George John Romanes. Born 19th May 1848 in Kingston, Ontario. Died 1894 at Oxford.

Darwin had postulated that organisms with variations conferring some advantage in the "struggle for existence" would more likely survive and produce offspring. This process of "natural selection" also discriminated against organisms with disadvantageous variations. The codiscoverer of evolution by means of natural selection, Alfred Russel Wallace, held rigidly to the theory as originally formulated, while Darwin was more flexible. Wallace was also a leading advocate of the credibility of supernatural phenomena, arguing that natural selection was insufficient to account for the evolution of the human brain (1869)⁴, and publishing The Scientific Aspect of the Supernatural (1866)⁵, and Miracles and Modern Spiritualism (1874)⁶.

In 1876 Romanes and his elder brother James were deceived by a "medium" who claimed to be able to communicate with spirits. Romanes wrote two letters to the sceptical Darwin expressing an inclination (short-lived) to believe in the phenomena he had observed. James, who was 14 when the family left Canada, had a friend in Kingston with an interest in spiritualism and he sent her drafts of the letters. Romanes later (1880) expressed doubt publicly concerning "the ascertained facts of clairvoyance and mesmerism" which had been proclaimed in a letter in Nature⁷. This brought a first contact with Wallace⁸. There were two meetings at which Romanes made no mention of his earlier credulity.

Meanwhile, Romanes had formed a close working relationship with the elderly Darwin. Well aware of inconsistencies in the theory of the origin of species by natural selection, Darwin had made their resolution his life's main focus. At the time of his friendship with Romanes, Darwin was much concerned with "Pangenesis" as a possible explanation for the inconsistencies⁹. Pangenesis suggested that the testes and ovaries (gonads) were merely collecting centers for hereditary (and perhaps acquired) information dispersed about the adult body as independent units which he called "generative elements" or "gemmules". In an 1875 letter he wrote to Romanes:

"I hope with all my heart that you are getting on pretty well with your experiments; I have been led to think a good deal on the subject, and I am convinced of its high importance, though it will take years of hammering before physiologists will admit that the sexual organs only collect the generative elements."^{1, 10}

A later letter (1876) began:

"As you are interested in Pangenesis, and will some day, I hope, convert an 'airy nothing' into a substantial theory..."¹⁰.

Darwin's correspondence suggests a sharing, not only of the experimental, but also the theoretical burden of his life's work. Romanes's experiments to prove the gemmule hypothesis came to nothing, but served to focus his attention on the gonads.

Following Darwin's death (1882), Romanes devoted much time trying to find errors in August Weismann's alternative (but correct) proposal that the germ line (contained in the gonad) was quite distinct from the rest of the body ("soma"). Romanes's book, An Examination of Weismannism eventually appeared in 1893, but by this time Weismann's ideas were becoming widely accepted¹¹. Key features of Weismann's proposal, and the Darwinian alternative, appear in Figure 1. Here we see that the germ line is part of an unending cycle, and so is potentially immortal. The soma (that's you and me) lasts for one generation and is then discarded.


Figure 1. The eternal cycling of the germ line. Following the gonad-specific process known as "meiosis", the male gonad (testis) produces male gametes (spermatozoa), and the female gonad (ovary) produces female gametes (ova). [1 = ovum. 2 = polar body. 3 = zona pellucida]

These unite (fertilization) to produce a unicellular zygote, which then multiplies and differentiates to produce an adult organism.

Tissues of the organism are either the "soma" (e. g. liver, brain, kidney), or the "germ-line" (contained in the gonad). Weismann proposed (correctly) that the soma (mortal) merely provides a supporting role for the germ-line (potentially immortal). Darwin proposed (incorrectly) that throughout life the germ-line would collect "gemmules" of information from the soma. The germ line cycle can be interrupted, so that an organism is "reproductively isolated", either because the gametes cannot meet ("transfer barrier"), or because the zygote does not develop to produce a healthy adult ("viability barrier"), or because meiosis fails in the gonad ("sterility barrier").

Romanes died in 1894 at age 46, and is remembered today mainly as Darwin's protege and for the annual Romanes Lecture series he endowed at Oxford. However, Darwin's mantle had been safely entrusted. Four years after Darwin's death Romanes published an extraordinary paper in the Journal of the Linnean Society, entitled "Physiological Selection: An Additional Suggestion on the Origin of Species"¹². In a formidable display of deductive reasoning, paralleled only by that of Darwin himself, Romanes resolved the three major problems in Darwin's theory -- "inutility of characters", "blending inheritance", and "hybrid sterility". We are concerned here mainly with the latter.

Darwin's theory was based on observations of plant and animal species "under domestication". Darwin thought it appropriate to extrapolate these observations to natural species. Yet he was aware (and the biologist Thomas Huxley constantly reminded him) that, if crosses between members of closely related natural species were possible, the "hybrid" offspring were invariably sterile. If we consider the horse and the ass as members of separate natural species, when a cross is made between them the resulting mule, although otherwise healthy, has maldeveloped testes or ovaries, and cannot reproduce.

Conversely, the offspring of crosses between members of "species" created by man (the breeder and horticulturist), are invariably fertile. If one defines a species as a group of organisms which do not breed (produce fertile offspring) with members of other species (e.g. cats do not breed with dogs), then "species" arising under domestication (e.g. poodle and bulldog) are not true species even though they may differ greatly from each other anatomically; they are "varieties", or "races". Hence Darwin confronted a serious problem.

Returning again to Figure 1, we see that failure to produce offspring may have three fundamental causes. The germ-line cycle may be interrupted because:

(i) The sperm and ovum (gametes) are unable to reach each other or will not fuse to form the zygote.
(ii) the zygote cannot develop into an adult organism, so that the "soma" is not present to support the survival of the germ-line in the gonad.
(iii) The formation of gametes in the gonad is impaired.

These are sometimes referred to as the transfer barrier, the viability barrier, and the sterility barrier, respectively.

Romanes focussed primarily on the sterility barrier, often the only barrier separating members of closely related species (i. e. species likely to have arisen recently from a common originating species). He suggested that, like cells of all other organs and tissues, germ line cells might undergo random variations. Variations, for example, in height or eye colour were familiar to everyone. No one knew what caused variations, but no one doubted their existence.

Romanes emphasized one possible class of variation affecting germ line cells, which would make an organism less fertile with other members of the species but not influence somatic characters. Normally the loss of fertility would be highly disadvantageous because the organism would leave no offspring. However, he further argued that if two organisms underwent the same type of variation, they would still be fertile between themselves. They would be "physiological complements". Hence, at any time-point a species would consist of the parental group (comprising the majority of species members), and numerous small variant groups. Members of each variant group would be less fertile with members of the parental group and of the other variant groups. Members of each group, to varying degrees, would be "reproductively isolated" from members of the other groups, but remain quite fertile with each other. Hybrid sterility would be an extreme manifestation of the phenomenon.

Romanes demonstrated that irrespective of any selective factors in the environment (no "survival of the fittest" required), members of the reproductively variant groups would tend also to be somatically variant, just as members of the parental group would tend to be somatically variant (e.g. changes in height or muscular strength). In the absence of environmental selection, however, somatic variations of members of the large parental group would not be sustained, because these members were crossing freely with each other, a process which tended to blend and neutralize variations. For example, although humans vary in height, tall people cross with small people and the average height tends to remain constant.

On the other hand, variations within a small variant group would not be subjected to this "swamping" effect due to blending with members of the parental group (i.e. there would be less non-variants to dilute the variation). Because of this reproductive isolation, the variation would be sustained. If, by chance, the variation happened to confer some advantage to members of the variant group, relative to members of the parental group, that would be a bonus. The selective advantage conferred would allow the commencement of classical Darwinian natural selection.

The major difference between the old Darwinian formulation (natural selection), and the new Romanesian formulation (physiological selection) was that in the first case, natural selection preceded reproductive isolation, where in the second case reproductive isolation preceded natural selection (Figure 2). Reproductive isolation, in any shape or form, would suffice, but the most usual form of isolation would result from physiological selection. Of course in a large population it would be very unlikely that a male and a female whose gonads had undergone the same rare variation would encounter each other. Thus the variation would probably not be perpetuated. Indeed, as Romanes pointed out, successful speciation was rare.

Isolation presedes selection under Romanes' hypothesis

Figure 2. Distinction between the Darwinian and Romanesian Theories of evolution.

Wallace criticized the physiological selection theory publicly (1886)¹³ and Romanes responded publicly (1887)¹⁴. At this time Wallace, famous as much for his books on spiritualism as for his work on evolution, visited North America on a lecture tour. In his 1905 biography he relates that he visited Queen's University, where:

"After the lecture [on "Darwinism"] some friends of Principal Grant came in, and ... a lady who was interested in spiritualism ... asked me if I knew that Romanes was a spiritualist, and had tried to convert Darwin. I told her that I knew he was interested in ... spiritualism, but that I thought it most improbable that he had said anything to Darwin. "But," she said, "Professor Romanes's brother is a great friend of mine, and he gave me the drafts of the letters they jointly wrote to Darwin. Would you like to see them?" I said I certainly should, and she promised to bring them the next morning. ... She said I might take notes on the contents as they were given to her without any restriction."⁸

The name of the lady is not disclosed, but we know that Wallace had made the acquaintance in Washington of the family of the Reverend J. A. Allen, whom he later visited at his home in Kingston. Wallace also took tea at Sir Richard Cartwright's "fine country house in a spacious park a few miles in the country".

Wallace was everything that Romanes was not. Wallace was relatively poor, a socialist (he Alfred Russel Wallace (1823-1913) published Land Nationalization in 1882¹⁵), an anti-vaccinationist (he published Vaccination a Delusion in 1898¹⁶), an advocate of spiritualism, and, with the death of Darwin, the preeminent authority on evolution. At the close of the nineteenth century there was a sense of complacency both in the biological and the physical sciences. It seemed that the major issues had been resolved, and now it was just a question of sorting out the details^17,18. In this environment authorities carried much weight.

In a book entitled Darwinism (1889), Wallace modified views previously expressed in correspondence with Darwin (1868)^{10, 19}. The correspondence contained a nineteen-point "proof" concerning the role of natural selection in hybrid sterility, which began:

"Let there be a species which has varied [note: past tense] into two forms each adapted to certain existing conditions better than the parent form, which they soon supplant [Wallace's italics]"¹⁰.

Darwin replied:

"I demur to probability and almost to possibility of ... [point 1] as you start with two forms which are not mutually sterile, and which yet have supplanted the parent-form".

Two decades later in his 1889 book Wallace admitted:

"The preceding argument ... [now decreased to eleven points] depends entirely upon the assumption that some amount of infertility characterizes the distinct varieties which are in process of differentiation into species; and it may be objected that of such infertility there is no proof"¹⁹.

Under Wallace's scheme, the event which concerned Romanes -- the initiation of the speciation process -- already had happened. Wallace dealt with events subsequent to the process of reproductive isolation (i.e. maintenance rather than initiation; Figure 3). The idea that the infertility he noted might relate to what Romanes proposed did not occur to Wallace. In a separate section of his book he described physiological selection as "another form of infertility," which he then proceeded to attack¹⁹.

Romanes responded publicly once more in 1890, this time not only with scientific arguments, but also noting that one should not rely on the judgement of a person of "incapacity and absurdity" whose past views were highly questionable, namely, on spiritualism, socialism and vaccination²⁰. Wallace wrote Romanes some sour private letters, which were later published⁸. These letters protested the "appeal to popular scientific prejudice," revealed Wallace's knowledge of Romanes's earlier flirtation with spiritualism as gleaned from the Kingston letters, and threatened to make "known the fact of the existence of these letters and their general tenor." This would show that Romanes's private judgements did not accord with his public posture of scepticism with respect to spiritualism. In short, Romanes was a hypocrite. A century later, of course, there are many reasons to conclude that Romanes's mature judgements with respect to spiritualism, socialism and vaccination were correct. Perhaps his judgement on physiological selection was also correct.

With Romanes's untimely death in 1894, the physiological selection theory lost its most powerful advocate. The most able of his English contemporaries, William Bateson (1861-1926), was deeply involved in detailed study of variations, work given great impetus by the discovery in 1900 of a 35-year-old paper by Gregor Mendel²¹. This forgotten paper provided a foundation for the new science of genetics. In a 1904 address Bateson extolled the virtues of the "practical man" who will "stoop to examine Nature" in "the seed bed and the poultry yard". Bateson seemed not to think highly of those (unnamed) with a philosophical bent of mind, who were interested in hybrid sterility achieved by some imaginary form of selection:

"For the concrete in evolution we are offered the abstract. Our philosophers debate with great fluency whether between imaginary races sterility grew up by an imaginary Selection ... and for many whose minds are attracted by the abstract problem of inter-racial sterility there are few who can name for certain ten cases in which it has already been observed"²².

Bateson sent a copy of his data-laden book, Materials for the Study of Variation²³, to Huxley, who replied (1894):,

"How glad I am to see ... that we are getting back from the region of speculation into that of fact again. There have been threatenings of late that the field of battle of Evolution was being transferred to Nephelococcygia [meaning nonsense].²⁴"

In private correspondence in 1888, Huxley had expressed the view that "even people like Romanes" did not really understand Darwin's theory, which was why Romanes had got it "so hopelessly wrong"²⁴. Thus, Romanes did not have the support of some of the most influential people of the time, -- Wallace, Huxley, and Bateson.

While Romanes pursued his evolutionary studies, Conan Doyle was creating the great detective Sherlock Holmes, who advised:

"When you have eliminated the impossible, then whatever remains, however improbable, must be the truth".²⁵

In Holmesian style Romanes had eliminated the "impossible", but "what remained" seemed so "improbable" that few could be convinced that physiological selection "must be the truth". Romanes could not go into specifics as to the cause of the reproductive selection he was postulating, beyond what he termed a "physiological peculiarity" of the reproductive system, the most obvious manifestation of which was the phenomenon of hybrid sterility. Nor could he elaborate upon occasional remarks that speciation (selective fertility) required the "suitable mating of 'physiological complements'." To some, there may not have appeared much difference between this view and the notion of divine creation.

Indeed, the outspoken purpose of people such as the botanist Alexis Jordan, whose observations Romanes used to buttress his case, was to disprove Darwin in favour of divine creation²⁶. It may not have added to his scientific credibility that Romanes was the son of a Presbyterian minister, that his major ally was the Reverend John Gulick,²⁷ and that Romanes, known among his friends as "the philosopher," had written books with such titles as A Candid Examination of Theism (1878)²⁸, Mind and Motion (1886)²⁹, and Thoughts on Religion (1895)³⁰. In 1879 he had declined an invitation from Huxley, well known for his agnostic views, to join the Association of Liberal Thinkers²⁴.

In 1886 Romanes had regarded his studies as merely paving the way for future investigations:

Evolutionist and missionary John T. Gulick (1832-1923)

"My suggested explanation of the origin of species opens up another and more ultimate problem, namely, granted that species have originated in the way supposed, what have been the causes of the particular kind of variation in the reproductive system which the theory requires?"¹²

To give his Victorian audience a concrete example of one form of physiological selection, Romanes had mentioned a change in the time of flowering of a plant, which would restrict the plant to fertilization only by other members of the species which had undergone the same change in flowering time:

"Suppose the variation in the reproductive system is such that the season of flowering or of pairing becomes either advanced or retarded. ...some individuals living on the same geographical area as the rest of their species, have varied in their reproductive system, so that they can only propagate with each other. They are thus perfectly fertile inter se, while absolutely sterile with all the other members of their species. This particular variation being communicated by inheritance to their progeny, there would soon arise on the same area, ... two varieties of the same species, each perfectly fertile within its own limits, while absolutely sterile with one another. That is to say, there has arisen between these two varieties a barrier of intercrossing which is quite as effectual as a thousand miles of ocean; the only difference is that the barrier, instead of being geographical, is physiological".¹²

Today we would regard such cases as resulting from primary variations in specific genes which affect the time of flowering. However, Romanes sensed that something more than specific genes was involved in the general case of formation of new species by physiological selection.¹²

The Romanes-Gulick correspondence indicates that although acknowledging its relevance, John Gulick (1832-1923) had not really appreciated the importance of hybrid sterility³¹. Thus, his son and biographer, the biochemist Addison Gulick noted in 1932:

"[John] Gulick's writings of 1887 and thereafter give an elaborate discussion of different aspects of sterility, though never quite placing mutual sterility in relief, the way Romanes did, as likely to be the fuse that ignites the whole powder train".^{27,
31}

Romanes and Gulick had been separately climbing towards the peak of a high mountain, for much of the time their heads being lost in the clouds. Every-so-often the clouds would have cleared and they would have been privileged to views, lonely views, which they could partially communicate to each other, but not to their contemporaries on the slopes below. In 1890 Romanes wrote to Gulick:

"It appears to be desirable that, as you and I are the only two human beings who recognize the full importance of "segregation" [reproductive isolation] in all its forms, we should submit to each other our views before publication, in order that we may speak as far as possible with a common voice".³¹

Meanwhile, Bateson was much occupied with overcoming the opposition to Mendel, and seemed to have forgotten Romanes's work. However, late in Bateson's career the overwhelming importance of the phenomenon of hybrid sterility dawned on him, and he began to consider its possible causes. In 1913 Bateson dismissed sterility associated with certain anther variants in plants as being due to a "simple recessive character," implying that sterility due to defects in one or a few defined characters was unlikely to be of general significance for the evolution of species.³² Microscopical studies of the gonads of sterile hybrids supported this view.

Normally, the set of chromosomes carrying genes contributed by the mother pair, on a one-to-one basis, with the complementary set of chromosomes carrying the genes contributed by the father. Close identity is essential for this pairing, which is required so that subsequent cell division and multiplication can proceed, resulting in the formation of gametes (sperms and ova). In hybrid sterility the pairing is defective and a degenerate gonad results. Thus the question of the origin of species becomes a question of the origin of hybrid sterility, which, in turn, leads to the question of the nature of the chromosomal incompatibilities which prevent pairing, or conversely, the nature of the chromosomal compatibilities which permit pairing. Reminiscent of Romanes's position, Bateson interpreted hybrid sterility as reflecting complementary chromosomal "factors":

"Though we cannot strictly define species, they yet have properties which varieties have not, and ... the distinction is not merely a matter of degree. The first step is to discover the nature of the [chromosomal] factors which by their complementary action inhibit the critical divisions and so cause the sterility of the hybrid".³²

Romanes and Bateson used the word "complementary" in converse contexts. Romanes's "physiological complements" were organisms with reproductive systems which were compatible, so that offspring would be produced. Bateson's "complementary factors" were components of the reproductive systems which were incompatible, thus preventing the production of offspring. As we shall see, these were but two sides of the same coin.

That hybrid sterility was strictly the result of a failure of the pairing of complementary chromosomes was brought home forcefully by experiments showing that hybrid sterility could be "cured" in certain organisms by artificially doubling the number of chromosomes. This was because each chromosome now had a partner with which it could pair (i.e. chromosomes from the mother could pair with each other, and chromosomes from the father could pair with each other). If the sterility had been due to a defect in particular genes, this "cure" would be unlikely³³.

Romanes's ally, John Gulick, remained uninfluential despite a major monograph in 1905³⁴. He generated a complex classification of types of sterility, which, combined with his cumbrous prose, no doubt confused more than it clarified. But Addison Gulick continued the crusade. In his 1932 biography of his father he wrote:

"The problem of physiological isolation has received ... little attention during the last two decades, but the modern picture of the mechanism of reproduction and the physico-chemical processes that it involves would have a very large influence on any consideration of the subject today. The immediate cause of infertility between species would be sought at the present time in either chromosomal incompatibilities or maladjustments of a serological nature .... From several viewpoints the old proposition of Romanes seems today exceedingly plausible, that a rather trivial mutation or group of mutations might set up a barrier of sterility within a species, and cause the two portions to diverge thereafter into well-marked new species".³¹

Unfortunately, Addison Gulick's campaign came too late. By 1932 the high ground of evolution research had been seized by individuals who approached evolutionary questions from a different perspective. Nevertheless, he attempted to open the argument again in 1938:

"With the progress of years we find a striking reinforcement of the scientific cogency of the theory which Romanes and J. T. Gulick championed; namely that a physiological barrier between two otherwise hardly distinguishable stocks may occur frequently, and must have the effect of initiating a train of divergent evolution".³⁵

Addison Gulick's efforts were to no avail. Those responsible for what subsequently became known as "the modern evolutionary synthesis" seem to have been unaware of the physiological selection theory. They spent much time juggling "selection coefficients" and the extent and timing of geographical migrations in order to provide a mathematical underpinning for evolution by natural selection. Their attempts to reconcile Darwin's ideas with Mendelian genetics were described in The Origins of Theoretical Population Genetics by historian William Provine (1971), who concluded:

"Thus, with the gap between theoretical models and available observational data so large, population genetics began and continues with a theoretical structure containing obvious internal inconsistencies".³⁶

Romanes himself had doubts concerning "numerical computation involving the doctrine of chances", remarking:

"In reference to biological problems of the kind now before us, I do not myself attach much importance to a merely mathematical analysis. The conditions which such problems involve are so varied and complex, that it is impossible to be sure about the validity of the data upon which a mathematical analysis is founded".³⁷

This foreshadowed later attacks on the "arid calculations of the mathematical population geneticists", which Provine relates.³⁶ The arch-population geneticist John Maynard Smith in his book Evolutionary Genetics warned in 1989 that: "To paraphrase Mr. Truman, if you can't stand algebra, keep out of evolutionary biology"!³⁸ In a letter to Darwin a century earlier, Romanes noted:

"The mathematicians must be a singularly happy race, seeing that they alone of men are competent to think about the facts of the cosmos. ... Mathematics are ... the sciences of number and measurement, and as such, one is at a loss to perceive why they should be so essentially necessary to enable a man to think fairly and well upon other subjects. But it is, as you once said, that when a man is to be killed by the sword mathematical, he must not have the satisfaction of even knowing how he is killed".¹

In human societies priestly groups always have tended to seize the high ground. Those who occupy such ground in modern times not only find it easier to continue their dominance, but come to act as "gate-keepers", the peer-reviewers who decide what the rest will be allowed to read and whose research will be funded. This has its dangers.

In 1976 Richard Dawkin's The Selfish Gene, which magnificently synthesized the work of William Hamilton and George Williams, added a fresh perspective to Darwinian ideas.^39-41 However, the new viewpoint was largely biological, and many inconsistencies remained. Then in the 1990s came the genome project and a deluge of DNA sequence data from biochemical laboratories. The first results of the bioinformatic analysis of these data have suddenly given the story fresh impetus. It appears that the chromosomal incompatibility which allows species to originate either arises from "macromutations" which affect chromosome segments^{31, 33}, or is the cumulative result of numerous "micromutations," as proposed by the present author in 1996⁴². In either case, Romanes was right as he did not specify the nature of the "peculiarity of the reproductive system" which would lead to reproductive isolation.

The strength of the micromutation proposal is that it allows fine degrees of compatibility, so that a rare reproductive variant would be more likely to find a partially matching physiological complement. The proposal arose from the perception that DNA, the molecule in chromosomes which transmits hereditary information, has two levels of information. There is nothing strange about this. A radio operator has to decide what message to transmit, and on what wavelength to transmit it. Thus the radio signal contains primary information (the message) and secondary information (the wavelength). The message is basically the same whatever wavelength is employed. The role of the secondary information is to allow discrimination between messages; it allows the receiver to tune out unwanted messages.

Shaw's 1913 play Pygmalion provides another helpful metaphor⁴³. If asked to recite a nursery rhyme, the "toff" Freddy Eynsford Hill, of some social standing, would have said:

"Mary had a little lamb, its fleece was white as snow...".
However, the flower seller, Eliza Doolittle, would have said:
"Miree ader li-awl laimb, sfloyce wors woyt ers snaa ...".

Both sentences convey the primary information that Mary possessed an immature, white, sheep. In class-conscious England at the beginning of the 20th century, however, the sentences would also have communicated the secondary information that Eliza was of "lower class" cockney origin, whereas Freddy was of "middle class" origin.

We may regard Eliza's dropped Hs as micromutations. The secondary information, because of such micromutations, constitutes a "reproductive barrier". Cockneys tend to marry cockneys and perpetuate cockney secondary information. The middle class tend to marry into the middle class and perpetuate middle class secondary information. Thus, Eliza appeared to be reproductively isolated from Freddy largely because of her language. Although, perhaps with some difficulty, both could understand each other's primary information, the secondary information (Eliza's dropped Hs) seemed to constitute a barrier.

Shaw tells us that Professor Higgins performed the appropriate experiment. He demonstrated that if the linguistic barrier were removed, then the reproductive barrier would also be removed. Eliza and Freddy lived happily-ever-after. We can say that they then possessed "linguistic complements", by which we mean that they approached linguistic identity. Alternatively, we can say that until Professor Higgins had performed his magic, their reciprocal differences, or "complementary factors" (Eliza's dropped Hs, and Freddy's included Hs) kept them reproductively isolated.

It is important to note that Eliza's cockney accent was a global characteristic of her speech. Each sentence she spoke was influenced by it. While each sentence provided a discrete piece of "primary" information, which was localized in that sentence, the "secondary" information (her accent) was diffused across all sentences.

We should also note that once the marriage knot had been tied (i.e. the barrier to reproduction formally removed), a good chance existed that, even if her accent subsequently regressed (diverged from Freddy's, so that linguistic complementarity was lost), the marriage (reproduction) would continue. Thus the initial secondary information (a reproductive barrier) needed only to be removed temporarily until a more substantial (legal) way of removing the barrier had been substituted.

This latter point proves of considerable importance when we move back to the problem of gaining evidence for two levels of information in DNA. Whatever the initial isolation process which led to the divergence between ancestral lines leading to, say, the modern elephant and mouse, it is clear that there is now a more substantial barrier to reproduction between the two (a gamete transfer barrier). It would probably be fruitless to examine these species for molecular clues as to the way the initial divergence took place (Figure 3). In virus species, however, signs of the initial isolation process might still exist. This, indeed, seems to be the case with viruses with the potential to coexist in the same host cell⁴².

Hypothetical evolutionary tree. Note that although two species might appear anatomically disparate, they might be quite close genotypically.

shepherd.GIF (19268 bytes)

Figure 3. A hypothetical evolutionary tree to show that the initial evolutionary events required for divergence from prototypic ancestral forms (circled regions), are distinct from evolutionary events required for the maintenance and further development of a species.

The first critical evidence emerged from studies of insect viruses by biochemist Gerard Wyatt in 1952, and there is now supporting data from analyses of retroviruses and herpes viruses^44-46. We also know that DNA has at least two levels of information. The primary information occurs in localized "sentences", which are the genes encoding the various characteristics of an organism. The secondary information is the molecular basis of Romanes' "physiological peculiarity" of the reproductive system, and must match between two individuals ("physiological complements") in order that they may reproduce. A divergence in this secondary information, through accumulation of micromutations, appears likely to initiate the speciation process^42,47. We should note that Bateson's careful use of the general term "factors" (not "genes") allowed him to encompass any form of information (primary or secondary) which was contained in the chromosomes⁴⁸.

At the conclusion of the 1932 biography of his father, Addison Gulick wrote:

"We may anticipate that the evolutionary problems which were outlined by Romanes and Gulick will again be reinstated in more perfect form than is today attainable. Until that time arrives it will remain impossible to estimate the relative importance of the several forces that cause the progressive transformation of species living under the conditions that nature provides".³¹

It has been a long wait. 35 years passed before the work of Gregor Mendel²¹ was recognized in 1900. A century has passed since the posthumous publication in 1897 of Romanes' masterpiece, the third volume of his Darwin, and after Darwin, entitled Isolation and Physiological Selection³⁷. Noting the leisurely pace of nineteenth century, compared with twentieth century, science, it can be seen that Romanes was not merely years ahead of his contemporaries, he was light years ahead.

However, there are signs of change. Harvard evolutionist Stephen Jay Gould in a 1980 paper "Is a new and general theory of evolution emerging?" notes a new readiness to entertain "chromosomal alterations as isolating mechanisms", and points out⁴⁹ that:

"Some of the new models ... regard reproductive isolation as potentially primary and non-adaptive rather than secondary and adaptive ... . In ... chromosomal speciation, reproductive isolation comes first and cannot be considered an adaptation at all. It is a ... [random] event that establishes a species by the technical definition of reproductive isolation. To be sure, the later success of this species in competition may depend on its subsequent acquisition of adaptations; but the origin itself may be non-adaptive. We can, in fact, reverse the conventional view and argue that speciation, by forming new entities ... [randomly], provides raw material for selection".,

Of course, Romanes and Gulick would have warmly agreed with this^{12,13, 50,51}.

Notes [For space reasons the notes had to be abbreviated in the paper published in Queen's Quarterly.]

1 E. Romanes, The Life and Letters of George John Romanes (London: Longmans, Green & Co., 1896).

2 C. Darwin, The Origin of Species by Natural Selection or the Preservation of Favoured Races in the Struggle for Life (London: John Murray, 1859).

3 G. J. Romanes, "Disuse as a reducing cause in species", Nature, 10 (1874) 164.

Romanes became a close friend of Norman Lockyer, the founding editor of Nature, and had him as a summer guest in Scotland in the early 1880s.

DRF Aug 2003

4 A. R. Wallace, Review of Principles of Geology by C. Lyell, Quarterly Review 126 (1869) 187-205.

5 A. R. Wallace, The Scientific Aspect of the Supernatural(London: F. Farrah, 1866).

6 A. R. Wallace, On Miracles and Modern Spiritualism (London: James Burns, 1874).

7 G. J. Romanes, ""A Speculation Regarding the Senses"", Nature 21 (1880) 348.

8 A. R. Wallace, My Life (London: Chapman & Hall, 1905), Chapter 36.

9 C. Darwin, The Variation of Animals and Plants under Domestication. Volume II, 2nd Edition (London: John Murray, 1875), Chapter 27. [How did Darwin come upon the idea of pangenesis? For more on this (Click Here).]

10 F. Darwin and A. C. Seward, More Letters of Charles Darwin (London: John Murray. 1903). [Haeckel had referred to pangenesis as an "airy nothing." In similar vein, Shakespeare in Midsummer Night's Dream wrote:

"And as imagination bodies forth,
The forms of things unknown, the poet's pen
Turns them into shapes, and gives to airy nothing
A local habitation and a name."

11 G. J. Romanes, An Examination of Weismannism (Chicago: Open Court Pub. Co., 1893).

It seems that Weismann eventually came round to adopting something like Romanes' physiological selection in his theory of "germinal selection." Thus he wrote (1896): "The variations presented to personal [natural] selection must have themselves been produced by the principle of survival of the fit! And this is effected ... through such profound processes of selection in the interior of the germ plasm as I have endeavoured to sketch ... under the title of germinal selection."

12 G. J. Romanes, "Physiological Selection: An Additional Suggestion on the Origin of Species", J. Linn. Soc.(Zool.) 19 (1886) 337-411. [Reproductive isolation due to differences in the time of flowering (plants), or pairing (animals) he regarded as "extrinsic". The most important form of reproductive isolation with respect to the origin of species was considered due to a "peculiarity" of the reproductive system, which he regarded as "intrinsic". (For full text - Click Here)]

13 A. R. Wallace, "Romanes versus Darwin", Fortnightly Review 46 (1886) 300-316.

14 G. J. Romanes, "Physiological Selection", Nineteenth Century 21 (1887) 59-80. For full text - Click Here)

15 A. R. Wallace, Land Nationalization its Necessity and its Aims (London: Trubner & Co., 1882).

16 A. R. Wallace, Vaccination a Delusion (London: Swan, Sonnenshein & Co., 1898).

17 L. Badash, "The complacency of nineteenth century science", Isis 63 (1972) 48-58.

18 A. M. Silverstein, A History of Immunology (San Diego: Academic Press, 1989), pp. 142-145.

19 A. R. Wallace, Darwinism (London: Macmillan & Co., 1889), Chapter 7.

20 G. J. Romanes, "Wallace on Physiological Selection", The Monist 1 (1890) 1-20.

21 G. Mendel, "Versuche uber Pflanzen Hybriden", Verh. naturf. Ver. in Brunn 4 (1865) 3-47.

22 W. Bateson, Presidential Address to the Zoological Society; British Association 1904, in William Bateson, F.R.S. Naturalist. His Essays and Addresses, ed. B. Bateson (Cambridge: Cambridge University Press, 1928), pp. 233-259.

23 W. Bateson, Materials for the Study of Variation (London: Macmillan & Co., 1894).

24 T. H. Huxley, Letters, in Life and Letters of Thomas Henry Huxley, ed. L. Huxley (London: Macmillan and Co., 1900).

25 A. Conan Doyle, "The Sign of Four", Lippincott's Monthly Magazine, (Philadelphia) 266 (1890) pp. 172.

26 A. Jordan, "Remarques sur le fait d'existence en societe a l'etat sauvage des especes vegetale affine", Congres de l'Association Francaise pour l'Avancement des Sciences, 1873.

27 J. T. Gulick, "Divergent evolution through cumulative selection", J. Linn. Soc. (Zool.) 20 (1887) 189-274.

28 G. J. Romanes, A Candid Examination of Theism (London: Truebner & Co., 1878)

29 G. J. Romanes, Mind and Motion; and Monism (London: Longmans, Green & Co., 1886).

30 G. J. Romanes, Thoughts on Religion (Chicago: Open Court Pub. Co., 1895).

31 A. Gulick, John Thomas Gulick: Evolutionist and Missionary (Chicago: University of Chicago Press, 1932).

32 W. Bateson, Problems of Genetics (New Haven: Yale University Press, 1913), pp. 238- 242.

33 T. Dobzhansky, Genetics and the Origin of Species (New York: Columbia University Press, 1937), Chapters 7, 9.

34 J. T. Gulick. Evolution: Racial and Habitudinal (Washington: Carnegie Institute publication number 25, 1905).

35 A. Gulick, "What are genes? 1. The Genetic and Evolutionary Picture", Quart. Rev. Biol. 13 (1938) 1-18.

36 W. B. Provine, The Origins of Theoretical Population Genetics (Chicago: University of Chicago Press, 1971).

37 G. J. Romanes, Darwin, and After Darwin. Isolation and Physiological Selection (London: Longmans, Green, & Co., 1897).

38 J. Maynard Smith, Evolutionary Genetics (Oxford: Oxford University Press, 1989).

39 R. Dawkins, The Selfish Gene (New York: Oxford University Press, 1976).

40 W. D. Hamilton, "The Genetic Evolution of Social Behaviour", Journal of Theoretical Biology 17 (1964) 1-54. [For more on WDH (Click Here)]

41 G. C. Williams, Adaptation and Natural Selection (Princeton: Princeton University Press, 1966).

42 D. R. Forsdyke, "Different biological species 'broadcast' their DNAs at different (G+C)% "wavelengths"", Journal of Theoretical Biology 178 (1996) 405-417.(For full text - Click Here)

"Micromutations" were also suggested by Richard Goldschmidt in his Material Basis of Evolution (1940).
DRF Aug 2003

43. G. B. Shaw, Bernard Shaw. Complete Plays with Prefaces. Volume I. (New York: Dodd, Mead & Co., 1963). [A character in another Shaw play "The Doctor's Dilemma" is inspired by Sir Almroth Wright, who shares with George J. Romanes the honour of being grandfather to Giles J. Romanes.]

44 G. R. Wyatt, "The nucleic acids of some insect viruses", Journal of General Physiology 36 (1952) 201- 289.

45 E. C. Bronson and J. N. Anderson, "Nucleotide composition as a driving force in the evolution of retroviruses", Journal of Molecular Evolution 38 (1994) 506-532.

46 G. A. Schachtel, P. Bucher, E. S. Mocarski, B. E. Blaisdell, and S. Karlin, "Evidence for selective evolution in codon usage in conserved amino acid segments of human alphaherpesvirus proteins", Journal of Molecular Evolution 33 (1991) 483-494.

47 More scientific background is provided by references in my 1996 paper (note 42). See also D. R. Forsdyke, "An alternative way of thinking about stem-loops in DNA", Journal of Theoretical Biology 192 (1998) 489-504. (For full text - Click Here) The latter paper provides evidence that pairing of chromosomes should be influenced by small fluctuations in the species-dependent component of the base composition of DNA [(C+G)%].

48 H. A. Orr, "Dobzhansky, Bateson, and the genetics of speciation", Genetics 144 (1996) 1331-1335. I further analyze Bateson's contribution in Journal of Theoretical Biology (1999) 201, 47-61. "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)%". [For full text - Click Here)]

49 S. J. Gould, 1980. "Is a new and general theory of evolution emerging?" Paleobiology 6 (1980) 119-130.

Lest this quotation be deemed prescient, we should note recantation by SJG in 2002 (The Structure of Evolutionary Theory. p. 1003). Here he stated:

"I do not, in fact and retrospect ... regard this 1980 paper as among the ... most cogent ... that I have ever written. ... I then read the literature on speciation as beginning to favor sympatric [same country] alternatives to allopatric [different country] orthodoxies ... and predicted that views on this subject would change substantially, ... . I now believe that I was wrong in this prediction."

DRF April 2002

There are uncanny similarities between Romanes and Gould. Both were center stage, both were well versed in biohistory, both wrote for popular and scientific audiences, both were attacked by the establishments of their days, and both contracted cancer in their forties. Modern chemotherapies may have given Gould another 20 years, whereas Romanes died at 46.

DRF Aug 2003

50 There is a somewhat surrealistic personal twist to this story:

My bioinformatic work (note 42) led to a relatively simple view of the origin of species, which made me wonder if one of the perspicacious Victorians close to Darwin might have anticipated me.
After following several false trails in my search for a Victorian (e.g. note 36), I came across Romanes in the fall of 1997 and learned of his Canadian origin. Now, it so happens that, with my family, I had moved in 1982 to a grey stone house which forms part of a small block in William Street, Kingston. Shortly after the move we found that in the 1840s the block had housed Queen's College (see Queen's: The First Hundred and Fifty Years (Newburgh: Hedgehog Productions Inc., 1990), pp. 28-29).

My 1997 enquiries led to the discovery that Professor George Romanes and his family occupied part of the block from 1846 to 1850 (see M. Angus, "Queen's College on William Street", Historic Kingston 34 (1986) 86-98 and photo of a painting below dated 1914). Since George John Romanes was born in 1848, it seems likely that he was born, and had passed his first two years, but a few yards from where these words are being typed!

207 William Street, Kingston, Ontario. The probable birth place of George John Romanes. In 1916 the building was a women's residence of Queen's University.

51 I thank Geoffrey S. Smith (Department of History, Queen's University), and Charlotte and Ruth Forsdyke for most helpful editorial comments. The painting of 207 William Street by Jane Redpath Drummond (1916) was exhibited at the Agnes Etherington Arts Centre, and the above photograph (courtesy of Dorothy Farr) is displayed with the permission of Mr. Douglas Petty (owner of the original painting).

Embryo Transfer

On 27th April 1890, Walter Heape (1855-1928) successfully transferred rabbit embryos from one mother to another, thus performing what we believe was the first mammalian embryo transfer. He thus achieved what Romanes had attempted but failed to do; namely, to demonstrate that, at least during the period of embryogenesis, the postulated "gemmules" or "pangens" of genetic information postulated by Darwin, could not be transferred from the mother to the foetus. The new born rabbits had all the characters of the biological parent. However, while Heape asked "What effect, if any, does a uterine foster-mother have upon her foster-children?", he made no claim to be testing Darwin's hypothesis of pangenesis.

Biggers (1991) suggests that "Romanes abandoned his ovarian transplantation and embryo transfer studies when he became convinced, somewhat surprisingly, that, when two breeds of rabbit hybridize, no intermediate between the two parental forms are produced." In theory, at least some of Darwin's "gemmules" should have transferred between the two parental genomes to produce intermediate types. Thus, in his own way, Romanes had rediscovered some of what Naudin and Mendel had discovered in the 1860s.

Romanes did not easily give up on the possibility of "gemmule" transfer, which might explain the acquisition of acquired properties (Lamarkism). Shortly before his premature death in 1894 he wrote to Sharpey-Schafer (May 18th) who had reported some success in transfer experiments:

"I have found, after several years experimenting with rats, rabbits and [ ], that one may breed scores and hundreds of first crosses between different varieties, and never get a single mongrel throwing off intermediate characters - or indeed any resemblance to one side of the house. Yet, if the younger are subsequently crossed inter se (i.e. brothers and sisters, of first crossings) the crossed parentage at once repeats itself. Ergo, even if the pups wh. are born appear to give a negative result, keep them to breed from with one another."

Unknown to Romanes (although he had cited Mendel in a review for the Encyclopedia Britannica), this is what Mendel reported with pea crosses in 1865.

Much like Romanes, Walter Heape was independently wealthy and was educated by a private tutor. He was interested in the application of scientific knowledge to human welfare, but appreciated how inadequate was the knowledge base. He supervised the construction of the Plymouth Laboratory under the auspices of the Marine Biological Association to serve the fishing industry. At Cambridge, he was a student of Foster, and here he probably first encountered William Bateson. At a critical point, he was appointed to the Evolution Committee of the Royal Society of London. Here, the knives were out between Bateson and the "Biometricians" (including Weldon). The Committee ended in backing Bateson. Heape's work was confirmed by Castle & Phillips (1909) with guinea pigs.

A related issue was whether prior fertilization by one male could be evident in the offspring of fertilization by another male ("telogony"). Thus, a woman might have, by a second husband, children who resembled a former husband. The "gemmules" of the ex-husband would have persisted long enough to influence later children (a handy excuse for a randy ex). This was investigated by another member of the Evolution Committee, J. Cossar Ewart (1851-1933), who had collaborated in research with Romanes in Scotland in the 1870s, and had been supported by Romanes in seeking (and obtaining) the Chair of Natural History at the University of Edinburgh. He prompted Lord Rosebery to sponsor a series of lectures by Romanes in 1888 on "The Philosophy of Natural History," which formed the basis of the latter's three volume series Darwin, And After Darwin.

Biggers, J. D. (1991) Walter Heape, FRS: a pioneer in reproductive biology. Centenary of his embryo transfer experiments. J. Reprod. Fert. 93, 173-186.

Castle, W. E. & Phillips, J. C. (1909) A successful ovarian transplantation in the guinea-pig and its bearing on problems in genetics. Science 30, 312-313.

Romanes, G. J. (1894) Sharpey-Shafer correspondence. Welcome History of Medicine Museum, London.

Acknowledgement. Dr. K. J. Betteridge provided helpful information on Heape and Ewart.

Struggle to Define and Show Relationships between the Four Black Boxes:

1. Variation

2. Heredity

3. Phenotypic ("Natural") Selection/Isolation,

4. Reproductive ("Physiological") Selection/Isolation

Hybrid Sterility (Darwin 1862)

Variation (Hooker 1862)

Pangenesis (Darwin 1868)

Inutility of Characters (Gulick 1872)

Natural and Artificial Selection (Belt 1874)

Inutility of Characters. Paradox of Sex. Random Drift (Delboeuf 1877)

Struggle to Establish "Physiological" Selection/Isolation as the most Important Form of Reproductive Selection/Isolation

Minoan wall decorations. Some of the earliest paintings of living forms.

An Unnoticed Factor in Evolution (Catchpool 1884)

Romanes (1886)

Romanes (1887)

Embryo Transfer (Heape 1890)

Struggle to Establish the "Chromosomal" (not "Genic") basis of Physiological Selection/Isolation

Hybridism and the Germ-Cell (Guyer 1900, 1902)

Cytological Basis for the Mendelian Laws (Cannon 1902)

Chromosomes of the Germ Cells (Montgomery 1901)

Chromosomes in Heredity (Sutton 1903)

Two Levels of Genetic Information (Bateson & Saunders 1902)

Heredity and Variation in Modern Lights (Bateson 1909)

A Phenomenon of Arrangement (Bateson 1914)

Chromosomes, Polyploidy and Why Sex Evolved (Winge 1917)

The Blind Watchmaker. Review (1987)

Speciation in Retroviruses (1995)

Origin of Species (1996)

Thinking about Stem-Loops (1998)

Two Levels of Information in DNA (1999)

Haldane's Rule (2000)

Non-Genic (Chromosomal) Speciation (2003)

Allen, Romanes and Gould (2004)

Chromosomal Speciation: A Reply (2004)

Heredity as Information Transfer (2006)

Positive Selection of Synonymous Mutations Initiates Species Divergence (2007)

Molecular Sex (2007)

Darwin's 'Weak Point' (2010)

Some Evolutionary Terms Used in these Pages

Evolutionary event. Evolution results from the accumulation of many evolutionary "events", each involving some or all of four processes: variation, heredity (inheritance), phenotypic selection, reproductive isolation. An evolutionary event begins with variation and is followed by the process of heredity continuing through the generations. Differential selection may follow variation.

Variation (like does not produce like). There is variation among members of a biological species and the resulting variant members are candidates for differential selection. Variation is a process which produces the variant features of variant organisms. These variant features are themselves often referred to as variations. Thus the word "variation" must be understood in context either as the process, or as the result of that process. Some variant features are latent or cryptic (i.e. not immediately observable).

Heredity (like produces like). There is inheritance of a newly acquired variation by at least some of the offspring of variant members, and inheritance of that variation, in turn, by some of their offspring, and some of the subsequent offspring. If a variation is not inherited (overtly or cryptically) then it may be the result of some environmental influence and is not strictly related to the evolutionary event under consideration. Thus, increased muscular strength acquired through exercise would not be transferred to offspring.

Blending inheritance (like and non-like merge). Recombination being a rare and random event, each gene tends to be inherited intact and a corresponding character may emerge unblended with other characters. Thus, the major factor determining tallness in peas is stem-length, which is controlled by one gene. The tall character is inherited without blending. The individual pea plant is either tall or short. There are no intermediates. However, often dominance is incomplete, so a blended phenotype appears among offspring. Thus, all the offspring of a cross between red and white flowering plants may all be pink in the first generation. Furthermore, numerous characters are multigenic (non-allelic). Thus, tallness in man depends on the lengths of many individual bones. It was recognized by Mendel, Bateson and, later, Fisher, that multigenic characters will blend in offspring (i.e. a range of intermediates will be observed). Thus, the extent of phenotypic variation offered to natural selection will be decreased relative to non-blending inheritance. Blending inheritance will tend to slow the rate of evolutionary change.

Selection. The words "selection" and "isolation" have led to confusion. The words have the same meaning, although one may be preferred in a particular context. Selection is something which can be done when there is more than one of something. If there is only one of something, then it can be considered as already selected (or isolated). In much of the literature, "selection" often means phenotypic selection; "isolation" often means reproductive selection.

Phenotypic selection There is positive selection of members of the species with advantageous variations, and negative selection of members of the species with disadvantageous variations. This isolation on the basis of phenotypic adaptations (positive or negative) is the type of selection with which Darwin was primarily concerned. In this respect he and others spoke of "survival of the fittest" and the "struggle for existence". He used the term "natural selection" to distinguish this form of phenotypic selection from the artificial selection carried out by the horticulturalist or breeder. However, reproductive isolation/selection can also be natural or artificial.

Reproductive isolation. Variation, heredity and phenotypic selection can operate so that advantageous phenotypic characteristics tend to increase in a population, and disadvantageous phenotypic characteristics tend to decrease in a population. They provide for the adaptation of species, and operate primarily at the level of the individual member of the species (individual selection). Ultimately, this linear process (isolation of the fit from the unfit) can lead to new species (i.e. one that would have been reproductively incompatible with the ancestral species if the cross were still possible). Here the fit are reproductively isolated from the unfit, because the latter are eliminated. However, sometimes an origin of species arises from a divergence between two equally fit populations, and reproductive isolation is needed more directly. To originate species in this way (isolation of the fit from the fit) groups have to be selected. Speciation (species selection) is a form of group selection. A group is a set of units. For our purposes, if there is only one unit in a set it is an individual, and does not constitute a group. A group whose members reproduce only asexually is, by definition, already reproductively isolated from other groups.

Species . The most secure definition of a biological species is a group of organisms which is reproductively isolated from other groups of organisms. Members of the group are unable to cross (continue the line) with all other organisms except those organisms which belong to the group. Inability to cross includes the production of offspring that are sterile (infertile). Degrees of infertility are characteristic of organisms at the species interface (i.e. potential incipient species).

Hybrid. The offspring of crosses between members of two anatomically distinct lines (varieties, races) are often referred to as "hybrids". Since the definition of species is based primarily on reproductive performance, rather than anatomical difference, this can lead to confusion. For our purposes any offspring is the hybrid of its parents if the parents are different genomically. There may be hybrid vigour ("positive heterosis"). There may be "negative heterosis" manifest as hybrid inviability (developmental barrier) or hybrid sterility (gonadal barrier). For humans, the only possible offspring not a "hybrid" would be the extremely improbable case of a female who inherited absolutely identical sequences from both parents. In the case of a human male, even if the autosomes were absolutely identical, the sex chromosomes would differ; so, under our definition, all males are hybrids.

More usually, the term is used in the context of a specific character (e.g. height). An organism may be pure (homozygous) for that character (e.g. corresponding paternal and maternal chromosomes both contain a gene conferring tallness), or it may be a hybrid for that character (e.g. the paternal chromosome may contain a gene conferring tallness and the maternal chromosome may contain a gene conferring smallness). If tallness is dominant, then the hybrid (heterozygote) may be as tall as organisms which are homozygously tall.

Genome. This term might be interpreted by the uninitiated as "gene home". We talk of "the human genome" or "the genome of the bacterium Escherichia coli". We usually mean the most obvious form of genetic material, which in these organisms is DNA. It is true that most of the E. coli genome consists of genes, but in "higher" organisms there is much DNA which is not so obviously "genic". Our genomes are not just "gene homes". Note also that a piece of the genome which we recognize as a "gene" may be serving functions other than those conventionally considered "genic". This is considered more in the Bioinformatics/Genomics section of these pages.

Further Acknowledgements. The photographs of Romanes and Gulick are from Romanes' Darwin, and After Darwin (Longmans). Photographs of the portraits of George and Ethel Romanes were made available by Giles J. Romanes. The photographs of Charles Darwin and Thomas Huxley are from the History of Medicine Division of the National Library of Medicine, USA (Click here). The photographs and drawing of Bateson are from the Report of the Royal Horticultural Conference on Genetics, 1906, as reproduced by H. F. Roberts in Plant Hybridization Before Mendel (Princeton University Press, 1929), and Beatrice Bateson's two books Letters from the Steppe (Methuen, London, 1928), and William Bateson F.R.S. (Cambridge University Press, 1928; original in the National Portrait Gallery, London). In the Delboeuf paper, the beautiful photograph of a South American butterfly (Heliconidae) is from Dr. William T. Hark's Butterfly Web Page (Click here), and the orangatan is from the Web Page of the Orangatan Foundation International, Los Angeles. Other acknowledgements are given in individual pages. The pictures of gametes and early divisions of the zygote in the legend to Figure 1 are from the prolife webpage of Simbahayan Sa Maynila, who, in turn, acknowledges Dr. Anna E. Ross of Christian Brothers' University.he portraits of George and Ethel Romanes were made available by Giles J. Romanes. The photographs of Charles Darwin and Thomas Huxley are from the History of Medicine Division of the National Library of Medicine, USA (Click here). The photographs and drawing of Bateson are from the Report of the Royal Horticultural Conference on Genetics, 1906, as reproduced by H. F. Roberts in Plant Hybridization Before Mendel (Princeton University Press, 1929), and Beatrice Bateson's two books Letters from the Steppe (Methuen, London, 1928), and William Bateson F.R.S. (Cambridge University Press, 1928; original in the National Portrait Gallery, London). In the Delboeuf paper, the beautiful photograph of a South American butterfly (Heliconidae) is from Dr. William T. Hark's Butterfly Web Page (Click here), and the orangatan is from the Web Page of the Orangatan Foundation International, Los Angeles. Other acknowledgements are given in individual pages. The pictures of gametes and early divisions of the zygote in the legend to Figure 1 are from the prolife webpage of Simbahayan Sa Maynila, who, in turn, acknowledges Dr. Anna E. Ross of Christian Brothers' University.