Experimental evolution of evolvability

Barnett, Michael; Zeller, Lena; Rainey, Paul B.

doi:10.1101/2024.05.01.592015

Cited by 3 publications

(1 citation statement)

References 81 publications

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“…However, rarely are hotspots associated with a selectable phenotypic change that allow determination of specific substitutions rates (Barnett, Zeller, & Rainey, 2024;Kapel, Caballero, & MacLean, 2022;Sankar et al, 2016;Viswanathan, Lacirignola, Hurley, & Lovett, 2000). In the case of C565T, an estimate of the mutation rate was made possible following the fortuitous identification that the mutation altered transcription from rpoSp, and that this mutation rate was shown to be dependent on the presence of PsrA.…”

Section: Discussionmentioning

confidence: 99%

An extreme mutational hotspot innlpDdepends on transcriptional induction ofrpoS

Farr,

Vasileiou,

Lind

et al. 2024

Preprint

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Mutation rate varies within and between genomes. Within genomes, tracts of nucleotides, including short sequence repeats and palindromes, can cause localised elevation of mutation rate. Additional mechanisms remain poorly understood. Here we report an instance of extreme mutational bias inPseudomonas fluorescensSBW25 associated with a single base-pair change innlpD.These mutants frequently evolve in static microcosms, and have a cell-chaining (CC) phenotype. Analysis of 153 replicate populations revealed 137 independent instances of a C565T loss-of-function mutation at codon 189 (CAG to TAG (Q189*)). Fitness measures of alternativenlpDmutants showed molecular parallelism to be unconnected to selective advantage. Recognising that transcription can be mutagenic, and that codon 189 overlaps with a predicted promoter (rpoSp) for the adjacent stationary phase sigma factor,rpoS, transcription across this promoter region was measured. This confirmedrpoSpis induced in stationary phase and that C565T mutation caused significant elevation of transcription. The latter provided opportunity to determine the C565T mutation rate using a reporter-gene fused torpoSp. Fluctuation assays demonstrate the C565T mutation rate to be 5,700-fold higher than expected. InPseudomonas, transcription ofrpoSrequires the positive activator PsrA, which we show also holds for SBW25. Fluctuation assays performed in a ΔpsrAbackground showed a 60-fold reduction in mutation rate confirming that the elevated rate of mutation at C565T mutation rate is dependent on induction of transcription. This hotspot suggests a generalisable phenomenon where the induction of transcription causes elevated mutation rates within defining regions of promoters.

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Section: Discussionmentioning

confidence: 99%

An extreme mutational hotspot innlpDdepends on transcriptional induction ofrpoS

Farr,

Vasileiou,

Lind

et al. 2024

Preprint

Self Cite

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Evolutionary dynamics of nascent multicellular lineages

Doulcier,

Remigi,

Rexin

et al. 2024

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The evolution of multicellular organisms involves the emergence of cellular collectives that eventually become units of selection in their own right. The process can be facilitated by ecological conditions that impose heritable variance in fitness on nascent collectives with long-term persistence depending on capacity of competing lineages to transition reliably between soma- and germ-like stages of proto-life cycles. Prior work with experimental bacterial populations showed rapid increases in collective-level fitness with capacity to switch between life cycle phases being a particular focus of selection. Here we report experiments in which the most successful lineage from the earlier study was further propagated for 10 life cycle generations under regimes that required different investment in the soma-like phase. To explore the adaptive significance of switching, a control was included in which reliable transitioning between life cycle phases was abolished. The switch proved central to maintenance of fitness. Moreover, in a non-switch treatment, where solutions to producing a robust and enduring soma-phase were required, evolution of mutL-dependent switching emerged de novo. A newly developed computational pipeline (colgen) was used to display the moment-by-moment evolutionary dynamics of lineages providing rare visual evidence of the roles of chance, history and selection. Colgen, underpinned by a Bayesian model, was further used to propagate hundreds of mutations back through temporal genealogical series, predict lineages and time points corresponding to changes of likely adaptive significance, and in one instance, via a combination of targeted sequencing, genetics and analyses of fitness consequences, adaptive significance of a single mutation was demonstrated. Overall, our results shed light on the mechanisms by which collectives adapt to new selective challenges and demonstrate the value of genealogy-centered approaches for investigating the dynamics of lineage-level selection.

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Direct and indirect selection in a proofreading polymerase

Husain,

Sachdeva,

Ravasio

et al. 2024

Preprint

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The traits that affect evolvability are subject to indirect selection, as these traits affect the course of evolution over many generations rather than the direct replicative fitness of an individual. However, the evolution of evolvability-determining traits is often difficult to study because putative evolvability alleles often have confounding direct fitness effects of unknown origin and size. Here, we study theoretically and experimentally the evolution of mutation rates in proofreading polymerases with orthogonal control of direct and indirect selection. Mutagenic DNA polymerases enjoy a long-time fitness advantage by enhancing the rate of acquiring beneficial mutations. However, this is offset by a short-time fitness penalty, which we trace to a counterintuitive trade-off between mutation rates and activity in proofreading polymerases. Since these fitness effects act on different timescales, no one number characterizes the fitness of a mutator allele. We find unusual dynamic features in the resulting evolutionary dynamics, such as kinetic exclusion, selection by dynamic environments, and Rock-Paper-Scissors dynamics in the absence of ecology. Our work has implications for the evolution of mutation rates and more broadly, evolution in the context of an anti-correlation between mutation rates and short term fitness.

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Experimental evolution of evolvability

Cited by 3 publications

References 81 publications

An extreme mutational hotspot innlpDdepends on transcriptional induction ofrpoS

An extreme mutational hotspot innlpDdepends on transcriptional induction ofrpoS

Evolutionary dynamics of nascent multicellular lineages

Direct and indirect selection in a proofreading polymerase

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