Chromosomal speciation: a reply
Journal of Theoretical Biology (2004) 230, 189-196
Copyright held by Else vier Ltd.
Keywords: Base composition; Chromosomal hypothesis; Genic hypothesis; Gene homostabilizing propensity; Non-genic hypothesis; Recombination; Speciation; Stem-loops
Biological evolution proceeds linearly within a species until there is a branch into two species, each of which may then continue to evolve in linear mode [see End Note 2008]. A major source of controversy has been the question whether linear and branching evolution can both be explained by Darwinian natural selection acting upon gene products, or whether branching evolution requires another process that is, in its fundamentals, independent of gene products and natural selection. Is species survival fundamentally different from species arrival?
latter half of the twentieth century the controversy coalesced around
two figures, Richard Dawkins (advocate of natural selection and genes)
and Stephen Jay Gould (advocate of hierarchical levels of selection
involving an agency other than natural selection). This gained wide
public attention as is related in popular texts such as The
2001) and Dawkins vs. Gould (Sterelny
and Turney, 2001). In 2002, after a two decade struggle with cancer,
Gould in his posthumous The Structure of Evolutionary
appeared to withdraw an earlier view that there might be "a new
and general theory of evolution emerging" (Gould,
In some quarters Gould's demise may be seen as marking the
demise of the non-genic viewpoint (Kitcher,
However, apparently unknown to Gould, in various laboratories including
my own, bioinformatic analyses of the vast amounts of sequence
information that emerged in the 1990s had yielded what seemed an
independent affirmation. Some members of the genic community took notice
and a "commentary"
was provoked (Kliman, Rogers and Noor,
The non-genic "chromosomal" viewpoint on speciation has a long history that, to my reading of the literature, can best be considered as beginning with George Romanes (1886). Indeed, the classic dual between Alfred Wallace and Romanes in the 1880s covered much the same ground as that between Dawkins and Gould (Forsdyke, 2004a; Smith, 2004). The non-genic torch was borne through the twentieth century by some of the most able biologists of our times - William Bateson, Nicolai Kholodkovskii, Richard Goldschmidt, Cyril Darlington, Addison Gulick, Gregory Bateson, Michael White, Max King, and Stephan Jay Gould. Romanes and Bateson were both convinced of the importance of what we would now call "non-genic" factors, but were reluctant to specify a chromosomal location (Forsdyke, 2001). The role of the chromosomes was made explicit by Kholodkovskii and the Russian school (Krementsov, 1994), a view adopted by all who followed.
As first formulated, the chromosomal
viewpoint was particularly vulnerable to criticism (Coyne and Orr, 1998)
since it postulated that large, often microscopically visible,
chromosomal differences ("macromutations")
would be evident early in the speciation process. These would inhibit
the meiotic pairing of homologous chromosomes so that recombination
would be inhibited and the hybrid would produce fewer and/or
maldeveloped gametes (hybrid sterility). Thus, the parents of the hybrid
would be reproductively isolated form each other. In contrast,
postulated sub-microscopic changes ("micromutations")
that we can now interpret at the level of individual bases. My
bioinformatic analyses emphasized the role of differences in
Chargaff's species-specific component of the base composition, GC% -
an agency that earlier scholars could only refer to in abstract terms (Forsdyke,
Coyne and Orr (1998) considered "the question of whether postzygotic isolation in animals is based on chromosomal or genic differences" and listed five major criticisms of "chromosomal speciation," which I addressed in my 1999 paper. The paper of Kliman et al. (2001) that acknowledges the "helpful comments" of Coyne, and the review of Charlesworth (2003), seems to constitute the Drosophila community's latest response.
We all agree that members of a species are so defined because they are reproductively isolated from members of other species. (When so inclined, even prokaryotes exchange nucleic acid best with their own kind; Radman and Wagner, 1993; Gratia and Thiry, 2003). We all agree that the question of the origin of species is essentially the question of the origin of reproductive isolation. We all agree that reproductive isolation can be achieved in a variety of ways, both genic and non-genic. However, we disagree on which of these ways is likely to have predominated over evolutionary time. This is an issue that cannot be settled by showing how reproductive isolation has been achieved in an individual, or even in several, case(s). The induction as to which form of reproductive isolation is the best candidate for having been the most usual origin of species must be made by looking at a large body of biological, genetical and biochemical evidence that relates to a variety of taxa.
Related issues include the questions of the existence of
hierarchical levels, and different units, of selection (Gould,
and the question whether the mechanisms postulated for the type of group
selection known as speciation are vulnerable to the same criticisms as
are the mechanisms postulated for some other types of group selection (Wynne-Edwards, 1962;
Maynard Smith, 1989). Not considered here is the question
of the existence of some vital force not explicable by known laws of
physics and chemistry (Driesch,
Also not considered here is the argument that, despite disagreements,
evolutionists should present a united front to the advocates of "creationism"
design." Also not considered here is the argument that evolutionists
should present a united front in order not to confuse other scientists
who need to understand speciation although working in other fields.
Sadly, these issues have been coloured by, sometimes ad hominem,
attacks by members of the genic school on members of the non-genic
school. Early targets were Romanes, Bateson and Goldschmidt (Forsdyke
2001, 2003). The most prominent modern target has been Gould
2001; Sterelny and Turney, 2001; Forsdyke,
For both Kliman et al. (2001) and Charlesworth
(2003) a major
stumbling block is that, between species that appear to have recently
diverged, differences in GC% may seem neither substantial, nor primary.
Is an observed GC% difference a cause (non-genic viewpoint) or
consequence (genic viewpoint) of the initiation of divergence into
distinct species? If a cause, how much difference is needed to initiate
speciation, and what is the mechanism?
diverged bacterial species also show early GC% differences,
predominantly at third codon positions (i.e. at the codon position that,
when changed, is least likely to change the encoded amino acid; Bellgard
and Gojobori, 1999; Bellgard et al., 2001; Gupta and Ghosh, 2003).
The case that such differences are primary has been strengthened
by the demonstration of a plausible mechanism relating GC% differences
to reproductive (i.e. recombinational) isolation. There is no one
definitive model for recombination (Holliday,
But all models regard similarity between sequences as necessary
for legitimate recombination, since a successful similarity search
initiates the pairing of complementary strands of potentially
recombining duplexes. Thus, all models associate sequence non-similarity
with recombinational suppression. Among the various models there is one
that implicates GC%. This model postulates that the similarity search is
between stem-loop structures that must be extruded from classical
Watson-Crick duplexes so that a mutual loop-loop "kissing"
exploration, which precedes extensive strand pairing, can begin. A
slight degree of negative supercoiling of DNA (the usual situation)
would favour such extrusion. Small differences in stem-loop
configurations should suffice to misalign loops and prevent pairing, so
inhibiting recombination (Sobell, 1972; Wagner and Radman, 1975; Doyle,
Thus, the present non-genic case rests on the facts that (i) GC%
differences have been observed early in the speciation process, and (ii)
there is a plausible mechanism by which small GC% differences inhibit
recombination. Furthermore, although contested by Kliman et al. (2001),
a variety of biological phenomena ("empirical data") lend
themselves to interpretation in such terms ("post hoc evaluations of
published data"). These include (i) large differences in the GC% of
viruses that have a common host cell (Forsdyke, 1996,
1999), (ii) the
cure of hybrid sterility by polyploidization (Winge, 1917; Goldschmidt,
1940), and (iii) Haldane's rule
Of course, GC% differences can affect gene function, but this
would be largely by affecting first and second codon positions. The non-genic
hypothesis attaches most importance to changes in genomic regions that
do not necessarily affect gene function (i.e. third codon positions,
introns, extragenic DNA). Thirteen years before the discovery of DNA
structure, this point was elegantly made by Goldschmidt (1940):
Thus, stem-loop potential should be best developed in introns and extragenic DNA as, indeed, the evidence suggests (Forsdyke, 1995; Barrette et al., 2001; Bultrini et al., 2003). To regard "G+C differences in --flanking DNA" as producing "the reproductive isolation effect via Forsdyke's compositional model," is not to be shrugged off as a "special pleading" (Kliman et al., 2001).