A generation-time effect on the rate of molecular evolution in bacteria

Abstract

Molecular evolutionary rate varies significantly among species and a strict global molecular clock has been rejected across the tree of life. Generation time is one primary life-history trait that influences the molecular evolutionary rate. Theory predicts that organisms with shorter generation times evolve faster because of the accumulation of more DNA replication errors per unit time. Although the generation-time effect has been demonstrated consistently in plants and animals, the evidence of its existence in bacteria is lacking. The bacterial phylum Firmicutes offers an excellent system for testing generation-time effect because some of its members can enter a dormant, nonreproductive endospore state in response to harsh environmental conditions. It follows that spore-forming bacteria would--with their longer generation times--evolve more slowly than their nonspore-forming relatives. It is therefore surprising that a previous study found no generation-time effect in Firmicutes. Using a phylogenetic comparative approach and leveraging on a large number of Firmicutes genomes, we found sporulation significantly reduces the genome-wide spontaneous DNA mutation rate and protein evolutionary rate. Contrary to the previous study, our results provide strong evidence that the evolutionary rates of bacteria, like those of plants and animals, are influenced by generation time.

Evolution with a seed bank: The population genetic consequences of microbial dormancy

“…This hypothesis was tested by analyzing a large collection of Firmicutes genomes, which included some isolates that had the ability to form endospores and other isolates that had lost the ability to form endospores (Weller & Wu, ). The rate of amino acid and synonymous substitutions for non‐endospore‐forming isolates was significantly elevated relative to endospore‐forming taxa and the phylogenetic branch length declined as the number of endospore‐forming genes within a genome increased (Figure a; Weller & Wu, ). These results suggest that rates of evolution increase when a lineage loses the ability to enter dormancy via sporulation.…”

“…To resolve this potential issue, the ability for microorganisms to remain in a dormant state for long periods of time has been proposed as an explanation for the existence of ORFans (González-Casanova F I G U R E 5 (a) The evolutionary distance (calculated as the root-to-tip sum on the branch of the phylogeny) declines as the number of sporulation-associated genes increases among Firmicutes taxa, a common group of bacteria found in soils and hosts. The publically available data presented here are from the Firmicutes phylogeny of conserved genes (Weller & Wu, 2015). (b) The evolutionary distance (calculated as the JC69 corrected distance) decreases as the average length of time that an individual spends in the seed bank increases (see Supplementary Materials).…”

Microbial community assembly in marine sediments

“…These processes hinge on community growth or a succession of multiple generations for genetic changes to settle in a population (Weller & Wu 2015). Highly dynamic environments with higher growth rates are prone to higher rates of HGT and de novo mutations that introduce novel traits into populations and drive speciation events.…”

Genome-scale rates of evolutionary change in bacteria

“…Both generation time and population size have been shown to scale negatively with the substitution rate in a range of organisms (Bromham, 2009). For example, because of differences in generation time, spore-forming bacteria evolve more slowly over time than those that do not form spores (Weller & Wu, 2015). Similarly, lineages undergoing adaptive evolution are expected to accumulate substitutions more rapidly than those subject to purifying selection (Eyre-Walker & Keightley, 2007).…”