Abstract
In 1913, the geneticist William Bateson called for a halt in studies of genetic phenomena until evolutionary fundamentals had been sufficiently addressed at the molecular level. Nevertheless, in the 1960s, the theoretical population geneticists celebrated a “modern synthesis” of the teachings of Mendel and Darwin, with an exclusive role for natural selection in speciation. This was supported, albeit with minor reservations, by historians Mark Adams and William Provine, who taught it to generations of students. In subsequent decades, doubts were raised by molecular biologists and, despite the deep influence of various mentors, Adams and Provine noted serious anomalies and began to question traditional “just-so-stories.” They were joined in challenging the genetic orthodoxy by a scientist-historian, Donald Forsdyke, who suggested that a “collective variation” postulated by Darwin’s young research associate, George Romanes, and a mysterious “residue” postulated by Bateson, might relate to differences in short runs of DNA bases (oligonucleotides). The dispute between a small network of historians and a large network of geneticists can be understood in the context of national politics. Contrasts are drawn between democracies, where capturing the narrative makes reversal difficult, and dictatorships, where overthrow of a supportive dictator can result in rapid reversal.
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Change history
06 February 2024
Capitalization of names in the reference list updated.
Notes
I began writing this paper after completing (September 2021) the second edition of our Bateson biography (Cock and Forsdyke 2022), which provides detailed background. After my posting of a preprint on the Social Sciences Research Network in June 2022, the 200th anniversary of Mendel’s birth was celebrated in July with an outpouring of papers in high profile journals. Their contents support the conclusion (see end of this paper) that superceding the traditional narrative (if indeed our case merits it) will take some time. This might first occur in a democracy rather than in a dictatorship, but we cannot be sure.
Konashev (2023) notes: According to Filipchenko, in the simplest case, one elementary species (race) will differ from other elementary species in “only one elementary property.” In this case, the question of the origin of species he wrote, “is replaced with a question of the origin of the lowest classification groups within one species, and if between them all a distinction consists in the presence of one property, then we come, eventually, to the question of there being a new property or group of new properties. Once we discover it, we will thereby also find out the source of evolution”.
Contrasting with most characters that Mendel studied where there were two alternatives (e.g., either tall or short pea plants), most observable characters are contributed by a variety of genes that blend in different associations to generate a kaleidoscopic range of alternatives, whose relative frequencies among individuals can be displayed as bell-curves.
GC% can be viewed as the accent of the DNA language. Given single letter abbreviations, the four main bases in DNA are A, C, G and T. The base composition of a segment of DNA can be expressed as the percentage of each base in that segment (A%, C%, G%, T%). Chargaff first parity "rule" is that for double-stranded (helical duplex) DNA, A% = T% and G% = C%. Certain bases are related. Thus, when comparing samples, as A% increases so does T%, and when G% increases so does C%. Since the total base concentration in a sample is constant (100%), it follows that when (A + T)% increases, (G + C)% decreases. So base composition can be approximated using just one of these—abbreviated to "GC%" (Forsdyke and Mortimer 2000; Forsdyke 2016).
Romanes was aware of the work of Mendel. In an Encyclopaedia Britannica article, he listed Mendel among authors who had contributed to the study of hybridism. These included Focke who "has just published an elaborate and valuable work on hybridism in plants … giving a tabular series of all the known vegetable hybrids, and treating the entire subject in a very comprehensive manner" (Romanes 1882). There followed long correspondence with Focke (Romanes 1897, pp. 175–176; Schwartz 2010, p. 71). He believed Romanes' experiments comparing hybrids between geographically isolated forms that had been artificially brought together (i.e., rendered sympatric, Catchpool 1884), with hybrids naturally formed in sympatry, would “solve the whole mystery” (Romanes 1896, pp. 101, 314; Schwartz 2010, p. 601). Romanes was also conducting Mendelian-style breeding experiments (brother-sister matings), which were cut-short by his death in 1894 at age 46 and evidence on their existence long remained unnoticed (Olby 1966; Cock and Forsdyke 2022, p. 169). A letter (May 18th 1894) in the Wellcome Collection (London) provides essential evidence for those who wish to pursue the matter. Romanes was then primarily involved on two fronts. Countering the attacks of the establishment Darwinists on his own physiological selection hypothesis, and experimentally examining Darwin’s postulates on the mobility of the “gemmules” that were part of the latter’s pangenesis hypothesis. Romanes’ negative results on this were not formally published.
The chronologies and extents to which various authors “rediscovered” Mendel’s work has been much discussed (Cock and Forsdyke 2022; Radick 2023) but does not concern us here. The Tschermak brothers supported Bateson over Weldon and were among those who came to acknowledge “special traits” that were distinct from “racial or mendeling traits” (Simunek et al. 2017).
The subsequent era of "molecular biology" led to the classical helical duplex structure of DNA and, beginning in the 1970s, detailed studies of its sequences (Grantham 1980). These led further to the alternative structures that could be adopted by DNA duplexes, so influencing the nucleic interactions required for the genome shuffling and error-correction effects brought about by recombination (Forsdyke 1996).
Equivalent percentages of certain pairs of bases (Chargaff's first parity rule) assisted Watson and Crick when devising their helical model for duplex DNA, where two strands were wound round each other. Thus, an A on one strand would pair with a T on the opposite strand, and a G on one strand would pair with a C on the opposite strand. This pairing of complementary bases played a structural role. The order of the bases in each strand was such that at every position the duplex pairing was precise. Chargaff later found that single strands alone also possessed approximately equivalent percentages of the same pairs of bases (Chargaff's second parity rule). Thus, provided potentially pairing bases were appropriately positioned, single strands should be able to locally foldback on themselves, so adopting stem-loop configurations. It was evident that a simple property, base order (rather than base composition), should be particularly informative. Programs Forsdyke developed for single-strand structure analysis in the early 1990s demonstrated the statistical significance of base order-dependent structure forming potential. Combined with strand "kissing" ideas for recombination (Kleckner and Wiener 1993), there emerged a model for structure-dependent meiotic strand pairing, initiated by stem-loops extruded from duplex DNA helices. Stem-loop patterns were sensitive to small single base differences (DNA "accent" differences), which would impede pairing. This would impede recombination, so would have the potential to promote speciation (Forsdyke 1996). Thus, the DNAs of different biological species would have come to differ in their GC% values (Chargaff's GC rule).
A low GC% segment of DNA will have more sets of consecutive bases (oligonucleotides) rich in A and T (e.g., ATC, CAT, AAA, ATA, AGT). A high GC% segment will have more oligonucleotides rich in G and C (e.g., GCT, TGC, GGG, GCG, GAC). Assuming a selective advantage of differences in GC%, this raised the question as to whether a primary selection pressure acted at the GC% level, with oligonucleotide frequencies being a secondary consequence, or vice versa (Forsdyke 1995). It now seems likely that oligonucleotide levels are primary (Forsdyke 2021b).
Adams, Mark B. 1990. "LITTLE EVOLUTION, BIG EVOLUTION. Rethinking the History of Population Genetics." This 34-page typescript, received by the author in 2003, began with an unlabeled introduction, which in the 2021 version is labelled "Did Population Genetics Save Darwinism?" Section headings follow as in the 2021 version, except that the latter has an added section on "Julian Huxley's 'Modern Synthesis'." Furthermore, a section labelled "Simpson and Macroevolution" is retitled "Paleontology and 'Macroevolution'" in the 2021 version. The paper concludes with notes (numbered 1–41) containing comments and pre-1991 references.
Adams recalls (personal communication; 2021) that William Provine had told him that his 1968 and 1970 papers on Chetverikov caused him to change the title of his dissertation (and book) from The Origins of Population Genetics to The Origins of Theoretical Population Genetics.
My webpages were initiated in 1998 when journals were just beginning to make their papers available online. Nineteenth-century journals were then not a priority, so I scanned key papers of Romanes and Gulick, and added them to my pages together with significant twentieth century ones, including those of Winge, Chargaff and Sueoka. These may be accessed by way of the Internet Archives Wayback Machine.
In 2000 I presented a paper on "Chargaff's legacy" at a workshop entitled "Neutralism and Selectionism. The End of a Debate" (Forsdyke and Mortimer 2000). Here I met Sueoka and Grantham (I had been corresponding with both). In the late 1990s, I had pleasant telephone conversations with the elderly Chargaff, who lived in New York. He was delighted to see our paper and sent a photograph for display on my webpages.
Gautier and Lobry (1997) did not appreciate that there are two classes of single-stranded RNA, the ability to correctly fold being critical for the function of only one of the classes. Thus, there is a structure-dependent class, members of which do not encode the information for making a protein (e.g., ribosomal RNA), and a much less-structure dependent class, members of which encode information for making a protein (messenger RNA; mRNA). The structure-dependent class are protected by high GC% from heat-inactivation in organisms that can survive at high temperatures (thermophiles). As an invited peer reviewer of the Gautier-Lobry paper, I advised a correction, which was not implemented. The term "less structure dependent" needs qualification. Like GC% values, the potential of duplex DNA to extrude stem-loops is a dispersed, genome-wide, feature of DNA, which affects both regions encoding genes and those not encoding genes. Thus, mRNAs, while encoding a protein, also have some encoded structure that mainly reflects the structure-potential of the DNA of the genes from which they were transcribed. A loss of structure (at high temperatures) does not impede the mRNA protein-encoding function. Thermophiles have specific adaptations, other than high GC%, for maintaining function at the DNA level.
The theoretical population geneticists here note that pairing between G and C is stronger than pairing between A and T, so that, on average, GC-rich DNAs (and RNAs copied from them) would be expected to have stronger pairing of complementary strands (hence being more stable at high temperatures). In analyses of single-strand structure potential, this genome-wide base composition dependent stability component can be identified in a segment because it is not affected by sequence shuffling. Once removed, there remains a precise value for the base order dependent stability component. Given the dispersed and relatively uniform nature of the contribution of base composition to the structure (it is the “accent” of DNA), the base order component reveals local sequence adaptations that have been selected over evolutionary time (“Nature’s experiments”). When scored (by convention) as negative, base order supports the stability assigned by base composition (that also scores negatively), thus indicating a locally compact structure. When scored as positive, base order opposes the stability assigned by base composition, thus indicating a locally more open structure (Forsdyke 1996; Forsdyke 2016; Zhang and Forsdyke 2021). This approach has advantages over the modeling of various potential equilibrium structures calculated from sequence ensembles by determining probabilities of individual bases being paired or unpaired (Zhang et al. 2022). Technical disputes in this area are approaching resolution (Andrews et al. 2023).
It is possible that Provine was unhappy with my joking comparison between Ernst Mayr and Beau Geste—the fictional last defender of a besieged desert fortress (Wren 1924). In 2001 (18th September), I sent him a copy of my speciation book (Forsdyke 2001), which acknowledged his help: “Please accept the enclosed book for your library, with many thanks for the great help your work provided. I hope the ‘tiny’ paper you mentioned in your email of 2nd July is progressing OK and look forward to a copy. I am not so pessimistic about ‘the hopeless isolating mechanisms which differ in every case of speciation’ (quoting from your email). In the book I opt for one mechanism as likely to have been usually operative in the general case. While I agree there is no ‘the’ origin in an absolute sense, some origins are more likely to have prevailed than others, and one in particular, should be receiving more attention. With best wishes for your continuing good health.”.
The 13-page, single-spaced, typescript of the ‘tiny’ paper—“Speciation in Historical Perspective” —duly arrived (9th December). Later (24th February 2004) Provine sent his review of Forsdyke (2004): “JTB asked me to review your article. My comments are attached. You asked me earlier to send you my speciation paper. It also is attached, and from it you can see that we differ a lot on species and speciation. That does not detract me from recommending that JTB publish your paper. You are one inventive guy. I have now read your entire book, too, and enjoyed it very much. You and Steve Gould tend to use history to build up to your own views, but that seems appropriate for scientists.” His 5-page review concluded cautiously: “Should the thesis of this paper be borne out by extensive future research, it would be a foundation stone of speciation studies.”.
The dark side of the life of Nobelist Niels K. Jerne (1911–1994) emerged after his death (Soderqvist 2003; Eichmann 2008; Forsdyke 2012) and has received some publicity (Yakura 2011). The Soderqvist-Eichmann-Forsdyke grouping cannot be viewed as a "network" in the sense implied by Adams (2001), since there was no personal communication between its members. There was no concerted push-back. Thus, the powerful Jerne network (Eichmann 2008) had free rein.
A long-held intuition of Mayr was in principle correct. In his first book he had written (Mayr 1942, p. 225): "A single mutation does not make a new species except in the case of polyploidy. New species are due to gradual accumulation and integration of small genetic differences." If we now interpret "small genetic differences" as changes in single nucleic acid bases, Mayr's thinking accords well with the viewpoint espoused here. Often critical to the initiation of species are differences in Bateson's "residue" (Forsdyke 2010), which now appears to relate to the slow accumulation, genome-wide, of base differences that modify GC% values and hence oligonucleotide frequencies (Forsdyke 2021b). Mayr never appreciated this, nor did a member of the late population genetics wave, H. Allen Orr (academic genealogy: Filipchenko, Dobzhansky, Lewontin, Coyne, Orr). His paper (Orr 1996) continued to receive multiple citations, despite its disparagement of Bateson and a narrow focus on Dobzhansky-Muller incompatibilities (Forsdyke 2011; Nei and Nozawa 2011).
While this paper was under review there were three developments. 1. Population geneticists reported that the term “reproductive isolation” in the context of speciation was first employed in 1935; after discussion with the authors, the editor issued a correction (Reuter 2023). 2. Masatoshi Nei died. Having obtained results that “are complex and quite confusing,” he had sought with “a historical perspective” to “clarify the roles of mutation and natural selection in speciation” (Nei and Nozawa 2011). In an obituary, the senior author of Long et al. (2018) noted how Nei’s work had launched many careers in theoretical population genetics and that “Toward the end of his life, he pushed ideas about mutation-driven evolution, but despite my attempts to get a deeper understanding of what he was getting at, I never quite pulled this out of our conversations and was left feeling that I was missing out on something” (Lynch 2023). 3. A fuller translation of Russian works became available (see note 2).
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Acknowledgements
Correspondence with William B. Provine and Mark Boyer Adams greatly assisted this study. John Wilkins (Melbourne) and an anonymous reviewer provided helpful reviews. My biohistory webpages are hosted by Queen's University and the Internet Archives (The Wayback Machine). The Social Sciences Research Network has posted preprints.
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Forsdyke, D.R. Speciation, natural selection, and networks: three historians versus theoretical population geneticists. Theory Biosci. 143, 1–26 (2024). https://doi.org/10.1007/s12064-024-00412-9
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DOI: https://doi.org/10.1007/s12064-024-00412-9