Abstract
Biological systems evolved to be functionally robust in uncertain environments, but also highly adaptable. Such robustness is partly achieved by genetic redundancy, where the failure of a specific component through mutation or environmental challenge can be compensated by duplicate components capable of performing, to a limited extent, the same function. Highly variable environments require very robust systems. Conversely, predictable environments should not place a high selective value on robustness. Here we test this hypothesis by investigating the evolutionary dynamics of genetic redundancy in extremely reduced genomes, found mostly in intracellular parasites and endosymbionts. By combining data analysis with simulations of genome evolution we show that in the extensive gene loss suffered by reduced genomes there is a selective drive to keep the diversity of protein families while sacrificing paralogy. We show that this is not a by-product of the known drivers of genome reduction and that there is very limited convergence to a common core of families, indicating that the repertoire of protein families in reduced genomes is the result of historical contingency and niche-specific adaptations. We propose that our observations reflect a loss of genetic redundancy due to a decreased selection for robustness in a predictable environment.
Highlights
Living organisms evolved to be functional in frequently harsh and variable environments, buffering internal molecular noise, genetic variation and unpredictable environmental fluctuations
Biosynthetic genes are frequently lost. It has been a matter of debate what decides whether a gene can be lost in evolution, and intracellular bacteria have been used as model systems to study these processes
We propose that when adopting an intracellular lifestyle, these bacteria extensively lost duplicated genes
Summary
Living organisms evolved to be functional in frequently harsh and variable environments, buffering internal molecular noise, genetic variation and unpredictable environmental fluctuations. Such ability is termed robustness [1]. One common source of robustness is genetic redundancy, in which one or more genes can perform the same function [2]. The exact contribution of genetic redundancy to the robustness of biological systems has, been a subject of considerable debate. After duplication the two copies will have identical functions and the loss of one by the accumulation of mutations is buffered by the other, having no fitness cost [3]
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