Experimental evolution of evolvability

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Abstract

Capacity to generate adaptive variation can evolve by natural selection. However, the idea that mutation becomes biased toward specific adaptive outcomes is controversial. Here, using experimental bacterial populations, we report the evolution of enhanced evolvability via localised hyper-mutation. Key to realisation was a lineage-level birth-death dynamic, where lineage success depended upon capacity to mutate between two phenotypic states, each optima in a cycling environment. The evolved mechanism is analogous to “contingency loci” in pathogenic bacteria, whose origin was previously unclear. Subsequent evolution showed lineages with localised hyper-mutability were more likely to acquire additional adaptive mutations. Our results provide a detailed mechanistic account of the adaptive evolution of evolvability.

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  1. Capacity to generate adaptive variation can evolve by natural selection. However, the idea that mutation becomes biased toward specific adaptive outcomes is controversial. Here, using experimental bacterial p

    I greatly enjoyed reading this preprint. The dissection of the origin of the de novo contingency locus was very cool.

  2. Central to our findings was a selective process where lineages better able to generate, by mutation, adaptive phenotypic variants, replaced those that were less proficient (Figure 1). In one metapopulation, a single lineage emerged with capacity to transition rapidly between phenotypic states via expansion and contraction of a short nucleotide repeat in a manner precisely analogous to that of contingency loci in pathogenic bacteria

    Do you have any thoughts on why global mutator alleles underpinned evolvability in two populations, and a local mechanism in the other? Seems that increased mutation rates are a common by-product of experimental evolution (e.g. instances in the LTEE). There is a nice paper in yeast that has demonstrated that mutator alleles tend to be favoured in cases where local population size is high (which allows selection to more efficiently act on the beneficial variants they produce). Might be relevant here: Sign of selection on mutation rate modifiers depends on population size, Raynes et al.,2018

  3. As the number of repeats increased, the rate at which transitions occurred visibly increased (Figure 3E).

    What a cool result. This reminds me of the observation in stickleback that the independent evolution of loss of pelvic hindfins tends to target the same locus because of the specific molecular characteristics of that stretch of sequence. This may be of relevance to this study: DNA fragility in the parallel evolution of pelvic reduction in stickleback fish, Xie et al. 2019.

  4. The selective regime employed was contrived, with selection on lineages being strictly enforced. Such stringent conditions are likely limited in nature. However, microbial pathogens faced with the challenge of persistence in face of the host immune response, will experience strong lineage-level selection, with repeated transitions through selective bottlenecks [38]. As we have shown here, precisely these conditions can promote the evolution of evolvability.

    It seem to me that the key component of the experimental selection regime is that individual level and lineage level selection were allowed to act in separate consecutive timesteps, shielding lineage level selection from being swamped out by 'short-sighted' individual level selection. I wonder how likely this scenario is to play out in circumstances such as pathogen evolution where I would imagine that both levels of selection should still be acting concurrently. I agree however that the presence of contingency loci implies that some form of ecological conditions likely exist that allows for this to happen.