LETTER TO THE EDITOR
Heredity (2011) 106, 202. (doi:10.1038/hdy.2010.15 (This differs from the final definitive published version; see the publisher's website)
The B in “BDM”
William Bateson did not advocate a genic speciation theory
In his commentary “One Hundred Years after Bateson,” Johnson (2009) refers to demonstrations of incompatibilities between the products of putative speciation genes that provide “further proof of principle of the model proposed by Bateson (1909) and extended by Dobzhansky (1937), Muller (1942) and subsequent geneticists.” Such “Bateson-Dobzhansky-Muller (BDM) incompatibilities” are held to “form the basic paradigm for much of the current theory on the evolution of reproductive isolation, and therefore the formation of species.”
However, while citing Lewis (2009), Johnson does not mention that Lewis urges caution “in labeling gene incompatibilities as speciation genes,” and “in interpreting them as being causal in the speciation process rather than a result of divergence post-speciation.” Furthermore, while citing the yeast studies of Greig (2009), Johnson does not mention Greig’s suggestion that speciation is due simply to “sequence divergence,” which generates meiotic “antirecombination,” namely “the inability of diverged chromosomes to form crossovers” because of non-genic chromosomal incompatibilities. Likewise, from introgression studies in fruit fly it was suggested that chromosomal incompatibilities were due to “foreign DNA amount” not to its coding potential (Naviera and Maside, 1998). A classic speciation gene causing tumors in interspecies fish hybrids has been brought into question (Schartl, 2008).
Since these studies support the non-genic view that William Bateson expounded in the early decades of the twentieth century (Forsdyke 1999, 2001, 2006), your readers may find it strange that Bateson’s name is linked to the genic viewpoint of Dobzhansky and Muller. It is true theirs is a model of interaction between genes, and that Bateson introduced the term “epistasis” to describe such interactions. But careful contextual reading of Bateson shows that he attributed speciation to a non-genic “residue” that can now be equated with divergence in DNA base compositions (Cock and Forsdyke, 2008; Forsdyke, 2009, 2010).
D R Forsdyke
T (1937). Genetics
and the Origin of Species.
Greig D (2009). Reproductive isolation in Saccharomyces. Heredity 102: 39-44.
Johnson NA (2009). One hundred years after Bateson: a pair of incompatible genes underlying hybrid sterility between yeast species. Heredity 103: 360-361.
Lewis EJ (2009) Origins of reproductive isolation. Nature 457: 549-550.
Muller HJ (1942). Isolating mechanisms, evolution and temperature. Biological Symposium 6: 71-125.
HF, Maside XR (1998). The genetics of hybrid male sterility in Drosophila.
In: Howard DJ, Berlocher SH (eds) Endless
Forms. Species and Speciation.
Schartl M (2008). Evolution of Xmrk: an oncogene, but also a speciation gene? BioEssays 30: 822-832.
End Note (Oct 2011)
Muller, like many others at Columbia University, devoured Robert Lock's textbook Recent Progress in the Study of Variation, Heredity and Evolution that was first published in 1906. Lock was one of William Bateson's most brilliant students and throughout the book he refers to his mentor. Given Bateson's preeminence, it is likely that Muller was thoroughly familiar with his writings, so that when presenting his model for gene-based hybrid reproductive incompatibility, Muller saw no reason to cite Bateson. Likewise, Dobzhansky's famous 1937 textbook (see above) displays knowledge of Bateson, and it is likely that he too saw no reason to cite Bateson when presenting his model for gene-based reproductive incompatibility. Unfortunately, some modern geneticists have fallen into what historians call the "presentist" trap in reading Bateson's 1909 article in Darwin and Modern Science. Fortunately, a 2010 textbook, Elements of Evolutionary Genetics, refers to DM incompatibilities, rather than BDM incompatibilities, but the authors still refer to Bateson as pioneering this viewpoint.
End Note (July 2013)
In March 2011 Genome Biology and Evolution accepted a paper by Masatoshi Nei and Masafumi Nozawa, who seemed to have independently arrived at the conclusion that it should be "DM" not "BDM":
"Orr (1996) argued that the first person who proposed the DM model is neither Dobzhansky nor Muller but Bateson (1909) and Bateson's model was identical with that of Dobzhansky and Muller. In our view, this argument is disputable. It is certainly true that Bateson considered the two-locus model of complementary genes in order to explain hybrid sterility, but he never considered how such a system can evolve. By contrast, Dobzhansky and Muller spelled out the evolutionary process of hybrid sterility genes, albeit very crudely. In evolutionary biology, it is important to understand the process of evolution. For this reason, we will refer to the model as the DM model in this paper."
The paper concluded that "the currently popular Dobzhansky-Muller model of evolution of reproductive isolation is only one of many possible mechanisms."
Nei N, Nozawa M (2011) Roles of mutation and selection in speciation: From Hugo de Vries to the modern genomic era. Genome Biology and Evolution 3, 812-829.
End Note (February 2017) "WCB" for Chromosomal Speciation Theories
There are growing calls for “analyzing speciation without prejudice” (Johannesson 2010), and hopes that “impediments resulting from deviant paradigms and terminology can be overcome" (Wolf and Ellegren, 2017). If we are going to employ eponyms then they should, at the very least, be accurate. Sadly, two decades after the Orr paper, in 2017 “BDM” lingers on, but the accurate “DM” usage is now often encountered (Coyne 2016). However, there remains confusion. A highly distinguished mouse genetics laboratory that has provided major support for the non-genic “chromosomal” viewpoint (Bhattacharyya et al., 2013), writes:
“several pieces of indirect evidence are in favor of D–M incompatibilities based on non-genic sequence divergence"
There follows a listing of studies beginning with the conclusion of Naviera and Maside (1998) that chromosomal incompatibilities in fruit fly offspring are due, not to differences in their coding potential, but to “foreign DNA amount.” The more recent back-cross studies of Moehring (2011) are also mentioned. Elsewhere, I have described highly supportive bioinformatic studies from various laboratories that support the chromosomal viewpoint (Forsdyke, 2016a, 2017).
Clear articulations of the chromosomal viewpoint trace back to the Danish “father of yeast genetics” Ojvind Winge, and were unknowingly elaborated by Crowther and Bateson in the 1920s (Forsdyke, 2010, 2016a, 2017). Thus, it would seem appropriate that, while retaining “DM incompatibilities” for appropriate genic speciation theories, we introduce “WCB incompatibilities” for appropriate chromosomal theories. The importance of such clarification may extend beyond science (Forsdyke, 2016b).
Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, et al., (2013). Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Nat Acad Sci USA 110: E468–E477.
Coyne JA (2016) Theodosius Dobzhansky on hybrid sterility and speciation. Genetics 202: 5-7. [ref added Aug 2017]
Forsdyke DR (2011). The B in BDM. William Bateson did not advocate a genic speciation theory. Heredity 106: 202.
Forsdyke DR (2016a). Evolutionary Bioinformatics, 3rd edn. Springer: New York.
Forsdyke DR (2016b). William Bateson, black slavery, eugenics and speciation: The relative roles of politics and science. Social Sciences Research Network: https://ssrn.com/abstract=2783480
Forsdyke DR (2017). Speciation: Goldschmidt's chromosomal heresy, once supported by Gould and Dawkins, is again reinstated. Biol Theor 12: 4-12.
[full details added Aug 2017]
Johannesson K (2010). Are we analyzing speciation without prejudice? Ann N Y Acad Sci 1206: 143–149.
Moehring AJ (2011). Heterozygosity and its unexpected correlations with hybrid sterility. Evolution 65: 2621–2630.
Wolf JBW, Ellegren H (2017). Making sense of genomic islands of differentiation in light of speciation. Nat Rev Genet 18: 87–100.
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Go to: Bateson's "Residue" (Click Here)
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Go to: Paper on Romanes' "Peculiarity" and Bateson's "Residue" (1999) (Click Here)
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This page was established in November 2009, posted on the internet 17 Feb 2010, and last edited 06 Aug 2017 by Donald Forsdyke