Note – this post has been updated since originally posted.
In its conclusion prof. Gregory suggests that we claim that “Non-coding DNA does
accumulate “so that” it will result in longer-term evolutionary advantage”.
We ABSOLUTELY NEVER stated such a non-sense. It is curious that the same accuse was moved by prof. Gregory in its article “Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma”, that we cite in our paper, to an article by Jain that we also cite in our paper. So, either prof. Gregory has a very poor opinion of our intelligence, or he thinks that we do not read the articles that we cite. Let us state, unambiguously, what we and Jain really say: “IF does exist a mechanism for genome size increase, THEN maybe the resulting long-term advantage can overcome the short-term disadvantage” (Jain was referring to the selfish dna as the genome increasing mechanism while we do not give any preference). Prof. Gregory reverts the implication: “IF there is a long-term advantage THEN the mechanism of genome increase is the product of selection”, and then explains us that it can’t be true. Incidentally, in the case of Jain, I think that what he was really intending can be clearly understood just by the title: “Incidental DNA”.
When someone suggests that one has misinterpreted the claims of an author, the appropriate thing to do is to consult the original article to be sure. So, I looked up the Jain (1980) letter, some quotes from which are given here
Natural selection is concerned not only with the existing variability but even more so with mechanisms which ensure its continued availability. If there is intragenomic selection leading to rapid build-up of some of the DNA sequences (the selfish DNA of Doolittle and Sapienza and Orgel and Crick) we must treat this part of DNA as incidental to the fundamental process of mutability so vital for ensuring continued supply of raw material for the production of new genes. It does not follow that all of the DNA produced in this manner will, in fact, acquire a function. A large part of it (or even all of it) may not do so and may be eliminated only on an evolutionary time scale. Meanwhile, new DNA of the same and similar kind may continue to be produced so that at a given point of time there will always be large amounts of non-specific DNA. This fraction is best described as ‘incidental’ rather than ‘selfish’ DNA. We may call it incidental because it is a byproduct of the inherent property of mutability of the genome, a characteristic to which natural selection attaches great importance even if it leads to the production of repeated sequences and a wasteful deployment of energy. Viewed in this light, non-functional DNA is very much a product of natural selection — a selection operating for mutability per se. Its relative abundance is probably a function of its nonfunctional nature for any other DNA which carries information of one kind or another would create genetic imbalance and would be quickly rejected.
Nature places considerable premium on playing safe so that it will not run short of raw material even if this means indiscriminate production leading to sequences which are destined to remain functionless.
Now, Dr. Musso may interpret this very differently, but I take it to mean that Jain argued that non-coding DNA was preserved by natural selection specifically because it may become useful as a source of new genes. Moreover, this would have to be non-coding DNA that was preserved in this way because adding coding regions for future use would create complications in genic function. I have discussed in various posts (e.g. here, here) why this notion is untenable.
UPDATE: My interpretation of Jain (1980) was that he was arguing that non-coding DNA is preserved by selection because it contributes to mutability. Further discussion with Jonathan Badger, and another re-read of Jain (1980) in the context of alternative interpretation, has bolstered the conclusion that he was in fact suggesting something different from what I said. The much more reasonable interpretation, and what I now think he was actually arguing, is that the genome is inherently unstable for reasons unrelated to non-coding DNA and that this is maintained by selection (though, it must be said, not in the usual sense but interlineage level) and the accumulation of non-coding DNA is a byproduct of this. I will accept that the authors of the paper that began the discussions saw it this way — though their phrasing “IF does exist a mechanism for genome size increase, THEN maybe the resulting long-term advantage can overcome the short-term disadvantage” is easily confused with arguing that non-coding DNA generates some long-term advantage that overcomes its immediate disadvantage (rather than representing a side-effect of some other process with a long-term advantage). And then, there is still the issue of what the original article stated:
From this point of view, we can think of TMs in our simulations as organisms trying to increase their gene pools adding new genes assembled from junk DNA. If the organisms possess more junk DNA it is possible to test more “potential genes” until a good one is found.
Though I doubt he will read this post, I do apologize to Dr. Jain if indeed I misinterpreted his argument. That said, I do think his phrasing of selection is imprecise and that this probably contributed to the confusion. In my original citation written 8 years ago, I cited Jain as an example of a “noncoding DNA is there because it might be useful” line of thinking, and while he may have been an inappropriate example, this notion is still around and needs to be fixed. In any case, I have not changed my opinion that the article that started this discussion drew undue links between a model and biological genome evolution, and that their results have little bearing on the genome size question.
Update, part two
I hate to keep updating this post (though I have preserved the original form with strikeouts), but I just knew I was not the only person to have interpreted Jain (1980) as suggesting that noncoding DNA was preserved because of its potential long-term benefits. It seems W.F. Doolittle (an originator of the “selfish DNA” idea, and whose paper Jain was commenting on) got the same impression. I will quote at length from Doolittle (1982), in which he discussed the varying reactions to the notion of selfish DNA shortly after it was proposed (italics in original, most in-line references omitted).
(c) The long-term evolutionary advantage of genomic rearrangements. Transposable elements promote genetic rearrangements, and the kinds of rearrangements (transpositions, deletions and inversions) seem similar in both prokaryotes and eukaryotes. This (and the occasional turning on and off of genes adjacent to the site of insertion) appears to be all that many, perhaps most, transposable elements actually do for the organism which bears them and it does not seem to be a good thing. Selection operating on individuals should eliminate such elements. Thus many have claimed that transposable elements are maintained because they play important “evolutionary roles”. This is not a straw man which Carmen Sapienza and I set up in order to have a hypothesis against which to pit the notion of selfish DNA. I can only document this with quotations not, I hope, taken out of context:
“Whether they (insertion sequences) exert functions at these positions or are simply kept in reserve as prefabricated units for the evolution of new control circuits remains unclear.”
“It is possible that the sole function of these elements is to promote genetic variability…”
“A tenable hypothesis regarding the function of transposition is that it allows adaptation of a particular cell to a new environment.”
“All these alterations could lead to changes in structural gene function and in the control of gene expression and could provide organisms with a means of rapid adaptation to environmental change.”
Evolutionary roles have similarly been invoked for heterochromatic highly repetitive DNAs, whose presence does affect recombination in neighbouring and distant regions and whose characteristics may (although the experimental evidence is not strong) affect chromosome pairing.
Neither we [Doolittle and Sapienza] nor Drs Orgel and Crick denied that transposable elements or heterochromatic highly repetitive DNAs have such evolutionary effects, nor that these effects might not be important, perhaps even as the basis for macroevolutionary change. What we were arguing against was the assumption that these elements arose through and are maintained by natural selection because of these effects.
This assumption is often only implicit in the writings of many who suggest that the only roles of mobile dispersed and tandemly reiterated DNAs are evolutionary ones. Thus we have been accused by some of these of misrepresenting their positions and thus indeed of attacking straw men after all. I apologize to those who feel we have put words in their mouths. But I do not see how statements that the only “functions” of transposable elements or highly repetitive DNAs are to generate or modulate genetic variability can mean anything other than that natural selection maintains, and probably even gave rise to, such elements through selection for such “functions”. Shapiro (1980) has been brave enough to articulate this view outright:
“Why, then, are insertion elements not removed from the genome? I think the answer must be that there is a selective advantage in the ability to generate new chromosome primary structure.”
Those who speculate on the function of excess DNA have formulated this position in a more extreme way. For instance, Jain (1980) states
“at a given point of time there will always be large amounts of non-specific DNA. This fraction is best described as ‘incidental’ rather than ‘selfish’ DNA. We may call it incidental because it is a byproduct of the inherent property of mutability of the genome, a characteristic to which natural selection attaches great importance even if it leads to the production of repeated sequences and a wasteful deployment of energy. Viewed in this light, non-functional DNA is very much a product of natural selection — a selection operating for mutability per se.“
The question of whether natural selection operates in this way, that is of whether the evolutionary process itself evolves under the direct influence of natural selection, lies at the root of the real controversy over whether self-maintaining, structured, genomic components without phenotypic function can properly be called “selfish”. This may seem like a small and metascientific quibble. In fact it is not; it is one of the most troublesome questions in evolutionary biology today. It manifests itself in debates over the origin and maintenance of mechanisms involved in the optimization of mutation rates, recombination, sexual reproduction, altruistic behaviours of all sorts and even speciation. Such mechanisms are not clearly advantageous to, and can be detrimental to, the fitness of the individual. Yet they may increase the long-term survival properties of the group to which the individual belongs, thus seeming to be the product of what has been called “group selection”.
Doolittle, W.F. (1982). Selfish DNA after fourteen months. In: Genome Evolution (G.A. Dover and R.B. Flavell, eds.), Academic Press, New York, pp.3-28.
Jain, H.K. (1980). Incidental DNA. Nature 288: 647-648.