Abstract Importance of chance, finiteness, and history in evolution is pointed out with special reference to the neutral theory. chance, finiteness, history Many of you may agree that random encounters have shaped our personal lives. The history of humans as a whole also depends on many chance effects. Therefore, it is natural to extend this way of thinking to natural history. Even emergence of this whole universe might have happened by chance according to some astrophysicists. Life on earth have continued for more than 3.5 billion years thanks to the special molecular structure of DNA double helix (Watson and Crick 1953). This continuity is by no means solid, for one DNA or genetic lineage often become extinct, as shown by Fisher (1923) using the branching process of Watson and Galton (1875). However, Fisher did not consider the importance of this stochastic effect. For him, Darwinian natural selection was fundamental for evolution. Later, Wright (1931) pointed out the importance of random fluctuation of allele frequencies especially when the population size becomes small. However, even Wright (1931, 1982) himself never considered the power of randomness as the major driving force of evolution, except for his shifting balance theory. When Kimura (1955) derived the analytical formula for the differential equation of diffusion approximation, Wright praised this effort, while he did not appreciate Kimura’s (1968) paper that proposed the neutral theory of molecular evolution (Wright, personal communication to Kimura in 1967). It is interesting that Monod (1970) proclaimed the importance of chance in evolution, though he never cited Kimura (1968) nor King and Jukes (1969). Nei (1987) quoted two sentences from English translation of Monod (1970) in the last paragraph of the last chapter: Chance alone is at the source of every innovation, of all creation in the biosphere. Pure chance, absolutely free, but blind, at the very root of the stupendous edifice of evolution. Mutations are also generated by chance, and they are as important as the random genetic drift especially for the long-term evolution. I also remember the strong message of the last sentence of Nei (1975): it (mutation) seems to be the primary factor of evolution at both the molecular and morphological levels. In the empty space on the last page of my book copy, I wrote “Joy of mutation!” just after reading the whole book. Nei maintained this mutation-centric view, and more than 30 years later published “Mutation-driven evolution” (Nei 2013). This world is finite. Our earth is just a 40,000-km circumference sphere. Life evolved on this tiny planet. We have to face the finiteness of the living world when we think about evolution. Random fluctuation of DNA copies (allele frequencies in classic sense) is a logical consequence of this finiteness. Because evolution follows time, evolution is historical. And chance played an important role in evolutionary history, as already noted by Darwin (1859). This is why I often mention three words—chance, finiteness, and history—in my talks and books (Saitou 2009, 2016), as well as the title for this perspective. I wrote a personal memoir on the neutral theory including how I encountered that theory (Saitou 1994), and would like to mention some later developments from my own viewpoint in the following. First of all, following the advances in sequencing technology from late 1990s, determination of genome sequences of many organisms opened the new research field “evolutionary genomics” (e.g., see Saitou 2013). Now it is rather routine to compare whole genome sequences of many eukaryotic species by downloading these sequences from databases (e.g., Babarinde and Saitou 2016). Thanks to next generation sequencers, even a small number of people can now determine a mammalian genome sequence with a small budget (e.g., Matsunami et al. 2018). From direct comparison of protein or RNA coding gene regions with noncoding regions of many genomes, it became clear that the majority of intergenic regions and introns are in fact “junk” DNA, as predicted by Ohno (1972). Most protein coding gene sequences showed lower nonsynonymous substitutions than synonymous ones, which “are truly neutral with respect to natural selection” (King and Jukes 1969). Of course, there are many exceptions to this pure neutral evolution view. There are many rather short sequences which are evolutionarily conserved in almost all eukaryotic genomes (e.g., Hettiarachchi and Saitou 2016), and most probably they are functional through controlling gene expression. These conserved noncoding sequences may be the bridge between evolution at the molecular level and evolution at the macroscopic or morphological level. Let us consider the special situation in Japan. Because of Kimura’s influence, many molecular evolutionists emerged in Japan, but they often write books on evolution in Japanese (e.g., Kimura 1988; Ohta 2009; Saitou 2011; Miyata 2014). Of course, Kimura himself published “The neutral theory of molecular evolution” (Kimura 1983). I was often scolded by Dr Masatoshi Nei, my PhD supervisor, for not writing a book in English. I thus wrote one textbook (Saitou 2013) based on my textbook written in Japanese (Saitou 2007). It was natural for me to dedicate that English book to Dr Nei. There are many good quality books written by Japanese molecular evolutionists in Japanese. I recently became the series editor of Springer “Evolutionary Studies”, and its first book was published (Saitou 2017). This book includes many Japanese authors as well as eminent molecular evolutionists including Dr Dan Graur. I hope many researchers whose native tongue is not English can obtain a wider audience for their contributions to this Evolutionary Studies Series in the near future. I am glad to complete this short note while I am staying in Houston, which was once the stronghold of neutralists in 1970s and 1980s. I was already a devoted neutralist in my undergraduate days, so I carefully chose Dr Masatoshi Nei as my academic supervisor, who was in the Center for Demographic and Population Genetics, the University of Texas Health Science Center at Houston. This neutrality thinking is in some sense inherited by Professor Yun-Xin Fu’s group at Human Genetics Center here in Houston, who are specialized in coalescent theory applications to various evolutionary phenomena (e.g., Liu and Fu 2015). DNA replication automatically generates a genealogy of DNA molecules, and through accumulation of mutations on those DNA genealogies, species phylogeny will emerge. Darwin (1859) was right when he described evolution as “descent with modification”. References Babarinde IA , Saitou N. 2016 . Genomic locations of conserved noncoding sequences and their proximal protein-coding genes in mammalian expression dynamics . Mol Biol Evol . 33 ( 7 ): 1807 – 1817 . Google Scholar CrossRef Search ADS PubMed Darwin C. 1859 . Origin of species . London : John Murray . Fisher RA. 1923 . On the dominance ratio . Proc Roy Soc Edinburgh 42 : 321 – 341 . Google Scholar CrossRef Search ADS Hettiarachchi N , Saitou N. 2016 . GC content heterogeneity transition of conserved noncoding sequences occurred at the emergence of vertebrates . Genome Biol Evol . 8 ( 11 ): 3377 – 3392 . Google Scholar CrossRef Search ADS PubMed Watson WW , Galton F. 1875 . On the probability of the extinction of families . 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Data Brief 16 : 43 – 46 . Google Scholar CrossRef Search ADS PubMed Miyata T. 2014 . Organismal evolution viewed from molecules—History of organisms deciphered through DNA (in Japanese). Tokyo : Kodansha . Monod J. 1970 . Le Hasard et la Nécessité: essai sur la philosophie naturelle de la biologie moderne. Paris : LeSeuil . Nei M. 1975 . Molecular population genetics and evolution . Amsterdam : North-Holland . Nei M. 1987 . Molecular evolutionary genetics . New York : Columbia University Press . Nei M. 2013 . Mutation-driven evolution . Oxford, UK : Oxford University Press . Ohno S. 1972 . So much “junk” DNA in our genome . Brookhaven Symp Biol . 23 : 366 – 370 . Google Scholar PubMed Ohta T. 2009 . Nearly neutral theory of molecular evolution—Evolutionary model of chance and selection (in Japanese). Tokyo : Kodansha . Saitou N. 1994 . A note on the neutralism . Jpn. J. Genet 69 ( 5 ): 503 – 512 . Google Scholar CrossRef Search ADS PubMed Saitou N. 2007 . 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Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: firstname.lastname@example.org This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
Molecular Biology and Evolution – Oxford University Press
Published: Apr 24, 2018
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