Frail Hypotheses in Evolutionary Biology
Jacques Ninio*
Laboratoire de Physique Statistique de l'Ecole Normale Supérieure, UMR 8550 of the CNRS, UPMC Université Paris 06 and Université Paris Diderot, Paris, France
Citation: Ninio J (2010) Frail Hypotheses in Evolutionary Biology. PLoS Genet 6(9): e1001067. doi:10.1371/journal.pgen.1001067
Editor: Ivan Matic, Université Paris Descartes, INSERM U571, France
Published: September 16, 2010
Copyright: © 2010 Jacques Ninio. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The author received no specific funding for this article.
Competing interests: The author has declared that no competing interests exist.
* E-mail: jacques.ninio@lps.ens.fr
In the last decades, under the headings of “mutation strategies,” “evolvability,” or “soft inheritance,” many ideas have been advanced on mechanisms assumed to promote innovative evolution beyond what one may anticipate from the classical model of random mutation and selection. Many population geneticists find these ideas superficially seducing but mathematically unfounded. While agreeing with the need to critically evaluate such proposals in the light of population genetics, I will argue that population geneticists are not immune to criticism. For instance, the “infinite site model” introduced by Kimura makes the unrealistic assumption that any neutral mutation arises only once during a neutral fixation episode, which leads, I propose, to an underestimation of the neutral fixation rates in large populations. Critical parameters such as mutation and recombination rates, effective population sizes or beneficial/deleterious mutation ratios are assigned convenient values, which may seem ad hoc to people outside the field. The lack of concern for the subtleties of genetic mechanisms is also criticized. Phenomena such as compensatory mutations, recurrent mutations, hot spots, and polymorphism, which population geneticists treat in the mathematical context of neutral versus selective fixations, can instead be interpreted in terms of genetic mechanisms for producing complex mutational events. Finally, single nucleotide substitutions are often treated as the quasi-exclusive source of variations, yet they cannot help much once the genes are optimized with respect to these substitutions. I suggest that population geneticists should invest more effort in refining the numerical values of the critical parameters used in their models. They should take into account the recent proposals on how mutations arise. They should also pay more attention to phenotypic variations, and develop criteria to discriminate between proposed evolutionary mechanisms that can actually work, and others that cannot.
Smart Evolutionary Devices?
For over a century, inventing an adaptive story for each particular trait in a species has been a major pastime of evolutionary biologists [1], [2]. This activity lost some of its appeal under the strokes of neutralist theories, according to which most of the nucleotide variations in DNA sequences of higher organisms are either selectively neutral [3] or even slightly deleterious [4]. The new trend is to propose smart evolutionary strategies based on each newly discovered form of genetic or phenotypic plasticity.
There are subtle ways of producing point mutations [5], and many forms of “natural genetic engineering” including transposition, reverse transcription, exon shuffling, combinatorial recombination, RNA editing, horizontal gene transfer [6]–[8]—the list is still expanding [9]. There are also “soft” inheritable variations, more easily reversed than point mutations [10]–[12]. Among these, DNA methylation and chromatin modifications have been proposed as agents in smart evolutionary mechanisms [13]–[14]. A classical theme underlying these proposals is that all forms of genetic and phenotypic variability are under genetic control, so when a beneficial mutation is fixed by natural selection, the gene controlling the production of such mutations is driven to fixation by hitchhiking.
In a remarkable article, Michael Lynch [15] offered a case by case refutation of recent proposals on smart evolution, asking with great clarity, “Have evolutionary biologists developed a giant blind spot; are scientists from outside the field reinventing a lot of bad wheels; or both?”
I do worry about bad wheels, remembering from thermodynamics that all proposals for perpetual motion machines turned out to be flawed. However, I also know that contrary to the formal proofs of yore, objects heavier than air can in fact fly. I will therefore question some current assumptions in population genetics and then present some subtleties of the mutation processes not yet taken into account in evolutionary biology. Finally, I will discuss the soft variation issue and issues in innovative evolution.
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