Abstract
Recent discoveries show that early in life effects often have long-lasting influences, sometimes even spanning several generations. Such intergenerational effects of early life events appear not easily reconcilable with strict genetic inheritance. However, an integrative evolutionary medicine of early life effects needs a sound view of inheritance in development and evolution. Here, we show how to articulate the gene-centred and non-gene-centred visions of inheritance. We first recall the coexistence of two gene concepts in scientific discussions, a statistical one (focused on patterns of parent–offspring resemblance, and implicitly including non-DNA-sequence-based resemblance), and a molecular one (based on the DNA sequence). We then show how all the different mechanisms of inheritance recently discovered can be integrated into an inclusive theory of evolution where different mechanisms would enable adaptation to changing environments at different timescales. One surprising consequence of this integrative vision of inheritance is that early in life effects start much earlier than fertilization.This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.
Highlights
The current mainstream view of inheritance in evolution is that the only real source of heredity lies in the DNA sequence, in particular in the germline that is considered fully isolated from the rest of the organism and its environment, ‘sealed off from the outside world’ [1]
We show here how the recent fascinating discoveries that in particular integrate early in life effects have some Lamarckian flavour and how integrating them into the modern synthesis of evolution has the potential to reconcile our neo-Darwinism with the Lamarckian element into a single inclusive evolutionary synthesis, which closely resembles the Darwinism of the origin
We stress the importance of this emerging approach for medicine in general and for early in life effects in particular. We illustrate how these considerations have the potential to open major avenues to establish new therapies for many of the inherited human disorders, most of which originate in the early part of an individual’s life or of its ancestors’ life. We show how this emerging inclusive evolutionary synthesis rejuvenates Darwinism from neo-Darwinism and how the inclusive vision of inheritance that emerges from recent discoveries leads us to accept a neo-Lamarckian component within a Darwinian framework
Summary
The current mainstream view of inheritance in evolution is that the only real source of heredity lies in the DNA sequence, in particular in the germline that is considered fully isolated from the rest of the organism and its environment, ‘sealed off from the outside world’ [1] In this genocentric view of inheritance, early in life environmental effects can strongly affect an organism for its whole lifespan, but such effects cannot percolate into the generation. That finding triggered major debates, notably about missing heritability, the fact that estimates of heritability in population genetics or epidemiology are almost always much higher than those obtained in genome-wide association studies [3 –7] The ubiquity of this discrepancy on its own suggests that a genes-only view of heredity may be far from sufficient to explain trait inheritance. We show how this emerging inclusive evolutionary synthesis rejuvenates Darwinism from neo-Darwinism and how the inclusive vision of inheritance that emerges from recent discoveries leads us to accept a neo-Lamarckian component within a Darwinian framework
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