Gene expression is the main driver of purifying selection in large penguin populations
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Abstract
Purifying selection is the most pervasive type of selection, as it constantly removes deleterious mutations arising in populations, directly scaling with population size. Highly expressed genes appear to accumulate fewer deleterious mutations between divergent species’ lineages (known as E-R anticorrelation), pointing towards gene expression as an additional driver of purifying selection. However, estimates of the effect of gene expression on segregating deleterious variants in natural populations are scarce, as is an understanding of the relative contribution of population size and gene expression to purifying selection. Here, we analyse genomic and transcriptomic data from two natural populations of closely related sister species with different demographic histories, the Emperor penguin ( Aptenodytes forsteri ) and the King penguin ( A. patagonicus) , and show that purifying selection at the population-level depends on gene expression rate, resulting in very high selection coefficients at highly expressed genes. Leveraging realistic forward simulations, we estimate that the top 10% of the most highly expressed genes in a genome experience a selection pressure corresponding to an average selection coefficient of -0.1, which decreases to a selection coefficient of -0.01 for the top 50%. Gene expression rate can be regarded as a fundamental parameter of protein evolution in natural populations, maintaining selection effective even at small population size. We suggest it could be used as a proxy for gene selection coefficients, which are notoriously difficult to derive in non-model species under real-world conditions.
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Given the general importance of protein expression levels, in cells it is widely accepted that gene expression levels are often a target of natural selection and that most mutations affecting gene expression levels are therefore likely to be deleterious [1]. However, it is perhaps less obvious that the strength of selection on the regulated genes themselves may be influenced by their expression levels. This might be due to harmful effects of misfolded proteins, for example, when higher protein concentrations exist in cells [2]. Recent studies have suggested that highly expressed genes accumulate fewer deleterious mutations; thus a positive relationship appears to exist between gene expression levels and the relative strength of purifying selection [3].
The recommended paper by Trucchi et al. [4] examines the relationship between gene …
Given the general importance of protein expression levels, in cells it is widely accepted that gene expression levels are often a target of natural selection and that most mutations affecting gene expression levels are therefore likely to be deleterious [1]. However, it is perhaps less obvious that the strength of selection on the regulated genes themselves may be influenced by their expression levels. This might be due to harmful effects of misfolded proteins, for example, when higher protein concentrations exist in cells [2]. Recent studies have suggested that highly expressed genes accumulate fewer deleterious mutations; thus a positive relationship appears to exist between gene expression levels and the relative strength of purifying selection [3].
The recommended paper by Trucchi et al. [4] examines the relationship between gene expression, purifying selection and a third variable -- effective population size -- in populations of two species of penguin with different population sizes, the Emperor penguin (Aptenodytes forsteri) and the King penguin (A. patagonicus). Using transcriptomic data and computer simulations modeling selection, they examine patterns of nonsynonymous and synonymous segregating polymorphisms (p) across genes in the two populations, concluding that even in relatively small populations purifying selection has an important effect in eliminating deleterious mutations.
References
1] Gilad Y, Oshlack A, and Rifkin SA. 2006. Natural selection on gene expression. Trends in Genetics 22: 456-461. https://doi.org/10.1016/j.tig.2006.06.002
[2] Yang JR, Liao BY, Zhuang SM, and Zhang J. 2012. Protein misinteraction avoidance causes highly expressed proteins to evolve slowly. Proceedings of the National Academy of Sciences 109: E831-E840. https://doi.org/10.1073/pnas.1117408109
[3] Duret L, and Mouchiroud D (2000). Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Molecular Biology and Evolution 17; 68-070. https://doi.org/10.1093/oxfordjournals.molbev.a026239[4] Trucchi E, Massa P, Giannelli F, Latrille T, Fernandes FAN, Ancona L, Stenseth NC, Obiol JF, Paris J, Bertorelle G, and Le Bohec, C. 2023. Gene expression is the main driver of purifying selection in large penguin populations. bioRxiv 2023.08.08.552445, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.08.08.552445
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