The Darwinian neo-synthesis strikes back

The Charlesworths and Nick Barton remind us that no, epigenetics did not make Darwinism obsolete.

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Despite the title, I do not think the Darwinian Modern synthesis (as defined by Julian Huxley in 1942) is some evil empire (titles only serve the purpose of catching your attention, right?). I do not think, either, that it is threatened by some insurgent group on a remote planet. Actually, I think that it is very healthy and solid.

Yet, every now and then some press release informs us that somebody has made some discovery that challenges Darwin’s ideas (some other people, meanwhile, at about the same rate, confirm Einstein’s relativity theory; the reason why it is so exciting when somebody challenges the one theory, and at the same time it is exciting when someone confirms the other, escapes me entirely).

Hence an article by three heavyweight figures of evolutionary and population genetics (D Charlesworth, NH Barton, B Charlesworth (2017) The sources of adaptive variation. Proc Royal Soc B 284: 20162864). The three Modern synthesis fighters probe the solidity of proof in favour of mechanisms that would fundamentally question the Modern synthesis. Are they relevant? common? do they work differently – evoluton-wise – than classical sequence variation? The paper is a review of the evidence supporting the generality and impact of several non-Mendelian inheritance mechanisms, and the Authors generally conclude that they are limited to a small number of particular cases or they have little impact on trait variation. Nothing is left standing after the paper’s judgement: not the role of epigenetic* alleles in the determination of traits, not the transmissibility of epigenetic marks; and not, of course, the possibility of directed mutagenesis. All such effects are dismissed as poorly supported or of minor consequence. Case closed: “no radical revision of our understanding of the mechanism of adaptive variation is needed”, as the last sentence of the summary says.

In summary, what should we say about epigenetics, Lamarck and all the rest? First, let me tell you: Haldane and Huxley are not Darwin and Wallace. They added something fundamental to Darwin’s brilliantly right, but incomplete, idea. The Modern synthesis made a fundamental act of integration of genetic heredity, population dynamics and evolution by natural selection. Is it complete, finished? certainly not. Is adding some new element (say, epigenetic inheritance, in spite of our trio’s skepticism) equivalent to disproving the Modern synthesis, or even Darwin – and going back to Lamarck? In other terms, should incompleteness of a more advanced theory force us to fall back to the previous one, even more incomplete and erroneous?
And then again, speaking precisely of epigenetic inheritance: Darwin did not have any clue of how inheritance of traits worked, and yet his theory was powerfully right. Now, why should epigenetics – a variation on the theme of Mendelism and a ripple in the ocean of solid facts supporting the Modern synthesis – make a century of population and evolutionary genetics wrong?

But let me be absolutely clear: I do not overlook the importance of epigenetic inheritance in the determination of traits and fitness. After all, if I am – say – a tree, my seeds will likely fall (with some notable exception) all around me, and they will probably undergo the same environmental conditions as myself. It is probably fitness-wise useful to provide my seeds with the same gene expression setup as I have, because it is likely to be the one that allowed me to successfully reproduce in the place where I live – and so it may help my progeny to sort it out. This hypothesis requires solid proof of course, but I would not dismiss it too quickly. To me, epigenetic inheritance could be viewed as a clever way to transmit gene regulation (not genetic variation) down to the next generation, and this may be adaptive, the same way phenotypic plasticity can be adaptive.

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On the contrary, one may also say: how can this stuff be relevant at all? After all, if it were so important, some important deviation of observation from theory should have appeared earlier in the history of modern genetics. This is certainly a sensible argument, except for two points: (a) we are very good at ignoring small but non-zero deviations and (b) as a professor of genetics in Milan, Italy used to say a long time ago: “there can be no genetics (as a research field) without genetic variation“. In other terms, we can only research effects that lead to the segregation of traits, and we are unable by construction to spot mechanisms that lead to uniformity. Epigenetic inheritance seems to produce equal patterns in all of an individual’s progeny, and so sits right in the middle of genetics’ blind spot.

So, in the end, by what means could new discoveries really hurt the Modern synthesis? I’d say that they should prove that new things escape the fundamental forces of evolution. If they exist, vary, and evolve in spite of selection, drift, migration, recombination, and non-random mating, then we have a problem.

My guess is this is unlikely to happen, and that we will discover that the reality of biological adaptation is more beautifully complex than we thought. If values of traits as determined by epigenetic inheritance – or the mechanism itself of epigenetic inheritance – can be proven to undergo selection for increased fitness, then this will be yet another nice addition of the Modern synthesis.

*nowadays the ‘epigenetic’ buzzword is used by some people to describe, well, gene regulation. We should not indulge in such lack of precision: good old regulation, operated by transcription factors and other proteins and RNAs and cued by the intracellular signalling of environmental factors, has nothing to do with epigenetic inheritance.

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