Disentangling the effects of selection and loss bias on gene dynamics

Abstract

We combine mathematical modeling of genome evolution with comparative analysis of prokaryotic genomes to estimate the relative contributions of selection and intrinsic loss bias to the evolution of different functional classes of genes and mobile genetic elements (MGE). An exact solution for the dynamics of gene family size was obtained under a linear duplication-transfer-loss model with selection. With the exception of genes involved in information processing, particularly translation, which are maintained by strong selection, the average selection coefficient for most nonparasitic genes is low albeit positive, compatible with observed positive correlation between genome size and effective population size. Free-living microbes evolve under stronger selection for gene retention than parasites. Different classes of MGE show a broad range of fitness effects, from the nearly neutral transposons to prophages, which are actively eliminated by selection. Genes involved in antiparasite defense, on average, incur a fitness cost to the host that is at least as high as the cost of plasmids. This cost is probably due to the adverse effects of autoimmunity and curtailment of horizontal gene transfer caused by the defense systems and selfish behavior of some of these systems, such as toxin-antitoxin and restriction modification modules. Transposons follow a biphasic dynamics, with bursts of gene proliferation followed by decay in the copy number that is quantitatively captured by the model. The horizontal gene transfer to loss ratio, but not duplication to loss ratio, correlates with genome size, potentially explaining increased abundance of neutral and costly elements in larger genomes.

How genetic parasites persist despite the purge of natural selection

“…To overcome this limitation, we used a phylogenomic reconstruction tool (COUNT) [46] that infers the distribution of gene gains and losses along the branches of a phylogenetic tree to obtain maximum likelihood estimates of the duplication, HGT, and loss rates under the assumption of neutrality [44,45]. Given such "neutral-equivalent" estimates, it is possible to recover the selection coefficient provided that the real value of at least one parameter is known.…”

“…-The interdependence between the cost of 58001-p5 Box plots were generated by pooling multiple gene families from the same class of parasites; the central mark of each box indicates the median, and the bottom and top edges indicate the 25th and 75th percentiles. The HGT rates were obtained from comparative genomics data as explained in [44,45]. The gray line in the background is the minimum HGT rate per copy required for parasite persistence (β * ).…”

“…Here we review a model that was recently applied to disentangle the factors that limit the spread of genetic parasites in microbial populations [44]. We modify the original model to account for the addictive nature of TAs, which allows us to estimate the effects of TAs on the fitness of the host.…”

“…For costly genes, the relative selection coefficient σ quantifies the relative importance of selection versus spontaneous deletions in controlling the gene copy number. Starting from an initial population with no copies of the gene, the solution of the model follows a negative binomial distribution [44] …”

Homologous recombination substantially delays sequence but not gene content divergence of prokaryotic populations

“…The evolution of gene content in closely related genomes has been recently investigated by mathematical modeling and comparative genomics 25–28 . These analyses have shown that the fraction of genes shared by a pair of genomes decays exponentially with time as the genomes diverge, and that genes can be classified in two categories based on their turnover rates 26 .…”