A systems biology view of evolutionary genetics

Evolution reflects the ability of subpopulations of organisms to acquire heritable change, usually so as to occupy a new environmental niche, but the molecular details of how such changes occur are still unclear. The evolutionary synthesis of the neo-Darwinists of the 1940s viewed evolutionary change as arising through novel mutations in genes that are assimilated within a population due to selection, perhaps under allopatric conditions [1, 2]. As mutation rates are low, so is the speed of change, but because evolutionary time scales are long, there had seemed to be plenty of time for mutational change to underpin adaptation and speciation. There are two concerns with this view. First, professional breeders, as Darwin well knew, can produce heritable variants very rapidly, and something similar appears to happen in nature when a single species penetrates a new geographical area and diversifies to occupy a variety of ecological niches, giving rise to what are known as species flocks [3]. Second, the fossil record shows that evolutionary progress is distinctly non-linear, with long periods of slow speciation being followed by extinctions and the relatively fast appearance of novel forms [4]. Here, the neo-Darwinian explanation is that mutation rates do not change after an extinction, but that selection pressures decrease with the opening up of new evolutionary niches so that organisms developing novel mutations have a better chance of colonising them. The neo-Darwinian approach of waiting for a new or for an existing gene mutation to become common and so affect a trait is inevitably slow. Contemporary knowledge allows us to see a much faster way of achieving variation and builds on two observations: first, modern systems biology makes it clear that traits depend on the output properties of one or more gene networks (e.g. for growth or for differentiation) not one or a few genes, and mutations in any one of these proteins can affect the network outputs; second, there is a lot more intrinsic variation in a population than had seemed until recently. This paper considers the implications of the realisation that there are many more opportunities for variation than was once thought.