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Review
. 2021 Nov 5;13(11):evab234.
doi: 10.1093/gbe/evab234.

Genic Selection Within Prokaryotic Pangenomes

Affiliations
Review

Genic Selection Within Prokaryotic Pangenomes

Gavin M Douglas et al. Genome Biol Evol. .

Abstract

Understanding the evolutionary forces shaping prokaryotic pangenome structure is a major goal of microbial evolution research. Recent work has highlighted that a substantial proportion of accessory genes appear to confer niche-specific adaptations. This work has primarily focused on selection acting at the level of individual cells. Herein, we discuss a lower level of selection that also contributes to pangenome variation: genic selection. This refers to cases where genetic elements, rather than individual cells, are the entities under selection. The clearest examples of this form of selection are selfish mobile genetic elements, which are those that have either a neutral or a deleterious effect on host fitness. We review the major classes of these and other mobile elements and discuss the characteristic features of such elements that could be under genic selection. We also discuss how genetic elements that are beneficial to hosts can also be under genic selection, a scenario that may be more prevalent but not widely appreciated, because disentangling the effects of selection at different levels (i.e., organisms vs. genes) is challenging. Nonetheless, an appreciation for the potential action and implications of genic selection is important to better understand the evolution of prokaryotic pangenomes.

Keywords: gene’s eye view; genic selection; horizontal gene transfer; mobile genetic elements; pangenome; selfish DNA.

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Figures

<sc>Fig</sc>. 1
Fig. 1
Examples of genetic transmission biases that can lead to genic selection. (a) Meiotic drive: a classical example of genic selection. This phenomenon generally occurs due to certain alleles that manipulate the meiosis process to ensure that they have higher rates of survival in eukaryotic male gametes (shown in blue). (b) Horizontal gene transfer also leads to biased transmission of certain genes, which have increased rates of transmission compared with genes that are solely vertically transmitted in a population of bacterial cells (ovals). In this example, red cells represent those that encode a MGE that can rapidly spread horizontally in the population (small arrows). Such biases in transmission can lead to genic selection for genes that are highly horizontally mobile. In extreme cases of both phenomena, genic selection can lead to genes that have deleterious effects on the host, but that nonetheless have high rates of transmission. In both (a) and (b), the large horizontal arrow denotes the passage of a short period of time (i.e., less than one generation).
<sc>Fig</sc>. 2
Fig. 2
Example of a self-propagating system associated with certain MGEs: the general type II restriction modification system. This restriction modification system can enforce postsegregational killing, much like a toxin–antitoxin system. In each cell the blunted arrow indicates enzyme inhibition whereas the regular arrow indicates enzymatic action.
<sc>Fig</sc>. 3
Fig. 3
Illustrative examples of fixation probabilities for a rare MGE in a population with varying horizontal transmission rates and adaptive benefits to the host. These probabilities are based on the findings that selection (s) and horizontal transmission (β) can proportionally contribute to a mobile element’s probability of fixation (P), which was formalized in the equation: P = 2(s + β) (Tazzyman and Bonhoeffer 2013). We computed the fixation probability based on varying the values of the horizontal transfer rate and selection coefficient in this equation to generate these curves. These examples highlight that classifying an accessory gene as adaptive or selfish is overly simplistic: in many cases slightly host-beneficial genes might be spread faster than expected given the organism-level benefit conferred.

References

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