Abstract
BackgroundThe relative contributions of natural selection and random genetic drift are a major source of debate in the study of gene expression evolution, which is hypothesized to serve as a bridge from molecular to phenotypic evolution. It has been suggested that the conflict between views is caused by the lack of a definite model of the neutral hypothesis, which can describe the long-run behavior of evolutionary change in mRNA abundance. Therefore previous studies have used inadequate analogies with the neutral prediction of other phenomena, such as amino acid or nucleotide sequence evolution, as the null hypothesis of their statistical inference.Methodology/Principal FindingsIn this study, we introduced two novel theoretical models, one based on neutral drift and the other assuming natural selection, by focusing on a common property of the distribution of mRNA abundance among a variety of eukaryotic cells, which reflects the result of long-term evolution. Our results demonstrated that (1) our models can reproduce two independently found phenomena simultaneously: the time development of gene expression divergence and Zipf's law of the transcriptome; (2) cytological constraints can be explicitly formulated to describe long-term evolution; (3) the model assuming that natural selection optimized relative mRNA abundance was more consistent with previously published observations than the model of optimized absolute mRNA abundances.Conclusions/SignificanceThe models introduced in this study give a formulation of evolutionary change in the mRNA abundance of each gene as a stochastic process, on the basis of previously published observations. This model provides a foundation for interpreting observed data in studies of gene expression evolution, including identifying an adequate time scale for discriminating the effect of natural selection from that of random genetic drift of selectively neutral variations.
Highlights
It has long been hypothesized that phenotypic evolution is more often based on evolutionary changes in gene expression regulation than on sequence changes in proteins [1]
Some researchers have argued that the majority of evolutionary changes in the mRNA abundance is selectively neutral and likely to be of little or no functional significance [17,18,21,22,24,25,26], while others have argued that natural selection has a substantial effect on gene expression evolution [7,23]
Our model assumes that (1) the mRNA abundance is affected by mutations proportional to the abundance before mutation; (2) the number of expressed genes and total number of mRNA molecules in a cell type is nearly constant throughout a specific evolutionary process; (3) the mRNA abundance of each gene has a lower limit near 1.0 copy/cell; and (4) the mRNA abundance of each gene suitable for its function is determined by its relative relationship to other genes, i.e., fi.fj
Summary
It has long been hypothesized that phenotypic evolution is more often based on evolutionary changes in gene expression regulation than on sequence changes in proteins [1]. The main conflict between researchers over gene expression evolution is the relative contribution of random genetic drift and natural selection to evolutionary changes in mRNA abundance. In a comparison of populations of the marine killifish Fundulus adapting to different habitat temperatures, much of the variation in expression level was correlated with phylogeny regardless of the habitat temperature they adapted to [17,18,24,25] This result can be explained by the neutral hypothesis. Previous studies have used inadequate analogies with the neutral prediction of other phenomena, such as amino acid or nucleotide sequence evolution, as the null hypothesis of their statistical inference
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