Abstract
Models for the evolution of various phenotypes are sometimes constructed with an assumption that mutational effects will be symmetrically distributed about a static mean. This model produces a memory effect that over long evolutionary times results in an expectation that randomized sequences underlying the genetic architecture of the trait will on average retain the ancestral phenotype. This expectation is unrealistic and also inconsistent with our current understanding of processes of molecular evolution.
References
Bank C, Ewing GB, Ferrer-Admettla A, Foll M, Jensen JD (2014) Thinking too positive? revisiting current methods of population genetic selection inference. Trends Genet 30(12):540–546. https://doi.org/10.1016/j.tig.2014.09.010
Forster R, Adami C, Wilke CO (2006) Selection for mutational robustness in finite populations. J Theor Biol 243(2):181–190. https://doi.org/10.1016/j.jtbi.2006.06.020
Goldstein RA (2013) Population size dependence of fitness effect distribution and substitution rate probed by biophysical model of protein thermostability. Genome Biol Evol 5(9):1584–1593. https://doi.org/10.1093/gbe/evt110
Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s finches. Science 313(5784):224–226. https://doi.org/10.1126/science.1128374
Hill MS, Vande Zande P, Wittkopp PJ (2021) Molecular and evolutionary processes generating variation in gene expression. Nat Rev Genet 22(4):203–215. https://doi.org/10.1038/s41576-020-00304-w
Hodgins-Davis A, Duveau F, Walker EA, Wittkopp PJ (2019) Empirical measures of mutational effects define neutral models of regulatory evolution in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 116(42):21085–21093. https://doi.org/10.1073/pnas.1902823116
Koch EM (2019) The effects of demography and genetics on the neutral distribution of quantitative traits. Genetics 211(4):1371–1394. https://doi.org/10.1534/genetics.118.301839
Krieger G, Lupo O, Wittkopp P, Barkai N (2022) Evolution of transcription factor binding through sequence variations and turnover of binding sites. Genome Res 32(6):1099–1111. https://doi.org/10.1101/gr.276715.122
Metzger BPH, Wittkopp PJ (2019) Compensatory trans-regulatory alleles minimizing variation in TDH3 expression are common within saccharomyces cerevisiae. Evol Lett 3(5):448–461. https://doi.org/10.1002/evl3.137
Muñoz-Gómez SA, Bilolikar G, Wideman JG, Geiler-Samerotte K (2021) Constructive neutral evolution 20 years later. J Mol Evol 89(3):172–182. https://doi.org/10.1007/s00239-021-09996-y
Neme R, Tautz D (2016) Fast turnover of genome transcription across evolutionary time exposes entire non-coding DNA to de novo gene emergence. Elife 5:e09977. https://doi.org/10.7554/eLife.09977
Orlenko A, Hermansen RA, Liberles DA (2016a) Flux control in glycolysis varies across the tree of life. J Mol Evol 82(2–3):146–161. https://doi.org/10.1007/s00239-016-9731-2
Orlenko A, Teufel AI, Chi PB, Liberles DA (2016b) Selection on metabolic pathway function in the presence of mutation-selection-drift balance leads to rate-limiting steps that are not evolutionarily stable. Biol Direct 8(11):31. https://doi.org/10.1186/s13062-016-0133-6
Paris M, Kaplan T, Li XY, Villalta JE, Lott SE, Eisen MB (2013) Extensive divergence of transcription factor binding in drosophila embryos with highly conserved gene expression. PLoS Genet 9(9):e1003748. https://doi.org/10.1371/journal.pgen.1003748
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49:169–181. https://doi.org/10.1007/PL00006540
Tamuri AU, dos Reis M, Goldstein RA (2012) Estimating the distribution of selection coefficients from phylogenetic data using sitewise mutation-selection models. Genetics 190(3):1101–1115. https://doi.org/10.1534/genetics.111.136432
Yona AH, Alm EJ, Gore J (2018) Random sequences rapidly evolve into de novo promoters. Nat Commun 9(1):1530. https://doi.org/10.1038/s41467-018-04026-w
Acknowledgements
I thank members of CCGG journal club at Temple for discussing these ideas with me during a journal club presentation. I thank David Alverez-Ponce and Jody Hey for reading and commenting on an advanced draft of this piece. I also thank comments from two anonymous reviewers and Associate Editor Michelle Meyer, who handled the manuscript.
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Handling editor: Michelle Meyer.
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Liberles, D.A. The Memory Problem for Neutral Mutational Models of Evolution. J Mol Evol 91, 2–5 (2023). https://doi.org/10.1007/s00239-022-10084-y
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DOI: https://doi.org/10.1007/s00239-022-10084-y