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Mechanism of Evolution by Genetic Assimilation Equivalence and Independence of Genetic Mutation and Epigenetic Modulation in Phenotypic Expression

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Mechanism of Evolution by Genetic Assimilation Equivalence and Independence of Genetic Mutation and Epigenetic Modulation in Phenotypic Expression bioRxiv preprint doi: https://doi.org/10.1101/242206; this version posted January 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Noname manuscript No. (will be inserted by the editor) Mechanism of evolution by genetic assimilation Equivalence and independence of genetic mutation and epigenetic modulation in phenotypic expression Ken Nishikawa · Akira R. Kinjo Received: date / Accepted: date Abstract Conrad H. Waddington discovered the phe- epigenetically induced phenotypic changes depend on nomenon of genetic assimilation through a series of ex- genetic mutations. Furthermore, we argue that trans- periments on fruit flies. In those experiments, artifi- generational epigenetic inheritance is not required for cially exerted environmental stress induced plastic phe- evolution by genetic assimilation. notypic changes in the fruit flies, but after some gen- Keywords Epigenome · Phenotype-driven evolution · erations the same phenotypic mutant started to ap- Phenotypic plasticity · Evo-Devo · Evolutionary pear without the environmental stress. Both the ini- Synthesis · Simulation tial state (where many individuals in the first gener- ation exhibited the phenotypic changes) and the final state (where the phenotypic changes were genetically 1 Introduction: Phenotype-driven evolution fixed) are experimental facts. However, it remains un- clear how the phenotypic change in the first generation In the 1950s, Waddington discovered the phenomenon becomes genetically fixed in the central process of ge- of genetic assimilation (Waddington 1957). Some envi- netic assimilation itself. We have argued that the key ronmental stress artificially exerted on fruit flies during to understanding the mechanism of genetic assimila- a certain developmental stage induces plastic pheno- tion lies in epigenetics, and proposed the \cooperative typic changes in the adult flies. By artificially selecting model" in which the evolutionary process depends on these phenotypic mutants over some generations, the both genetic and epigenetic factors. Evolutionary simu- fruit flies eventually come to express the mutant phe- lations based on the cooperative model reproduced the notype even without the environmental stress. That is, process of genetic assimilation. Detailed analysis of the the mutant phenotype is genetically fixed or assimilated trajectories has revealed genetic assimilation is a pro- (Scharloo 1991). We can observe the following charac- cess in which epigenetically induced phenotypic changes teristics in genetic assimilation: are incrementally and statistically replaced with multi- (a) A strong environmental stress induces phenotypic ple minor genetic mutations through natural selection. changes in multiple individuals of a population. In this scenario, epigenetic and genetic changes may be (b) The mutant phenotype in the first generation be- considered as mutually independent but equivalent in comes, after a series of artificial selection over gen- terms of their effects on phenotypic changes. This find- erations, genetically fixed (genetic assimilation). ing rejects the common (and confused) hypothesis that (c) Genetic assimilation completes in a relatively small number of generations. In other words, genetic as- K. Nishikawa similation is a rapid evolutionary process. National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan. Waddington's experiments were carried out for at least E-mail: [email protected] two types of mutant phenotypes, cross-veinless wing A. R. Kinjo (Waddington 1953) and bithorax (Waddington 1956), Institute for Protein Research, Osaka University, both of which demonstrated genetic assimilation. Fur- 3-2 Yamadaoka, Suita, Osaka 565-0871, Japan. thermore, they were performed based on a then-well- E-mail: [email protected] known phenomenon called \phenocopy" (Goldschmidt bioRxiv preprint doi: https://doi.org/10.1101/242206; this version posted January 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 2 Ken Nishikawa, Akira R. Kinjo 1938) which is a phenomenon that external stimuli dur- In this sense, genetic assimilation is clearly an example ing ontogenesis induce phenotypic changes in the same of evolution. The Evolutionary Synthesis cannot fully generation that are indistinguishable from known ge- explain the phenomenon because the initial phenotypic netic mutants. The initial phenotypic change is there- change is not due to genetic mutations. On the other fore considered as an acquired trait caused by the envi- hand, West-Eberhard in particular, and the Extended ronmental stress (the point (a) above). But the change Evolutionary Synthesis in general, do not explain how is somehow genetically fixed in the final stage. Wadding- the initial non-genetic phenotypic change can be genet- ton himself considered that genetic assimilation was ically fixed in the final stage. caused by \developmental plasticity" (in today's term), If we reexamine West-Eberhard's thesis in modern and explained it, rather metaphorically, as a change in terms, we notice that this is a problem of epigenet- the pathways of developmental process (which he called ics which tries to connect phenotypes with genotypes \canalization") due to the environmental change. in molecular terms. It was before the dawn of modern The standard evolutionary theory, namely the Evo- epigenetics when West-Eberhard published her mono- lutionary Synthesis, assumes individuals with an advan- graph in 2003. Thus, she was not in a historical position tageous heritable trait must preexist in the population to enjoy the fruitful and vast results of epigenetics; but in the initial stage of evolution, and the genetic mu- now we are. It is therefore our responsibility to over- tations responsible for the trait are gradually fixed in come the problem West-Eberhard challenged but failed, the population over generational changes. As such, ge- and to review the evidence underpinning the evolution- netic assimilation (where the initial phenotypic change ary mechanism of genetic accommodation (we will focus is not heritable) poses a serious difficulty on today's on genetic assimilation henceforth) in molecular terms. evolutionary theories, and it is often avoided as a \rare" In the following, we first review basic notions of epi- phenomenon (Laland et al 2014). genetics and its role in evolution as well as some at- Among several alternative theories to the Evolution- tempts to solve the aforementioned problem. However, ary Synthesis, collectively called the \Extended Evolu- we do not discuss transgenerational epigenetic inheri- tionary Synthesis" (Pigliucci and M¨uller2010), a ma- tance (TGEI) which often comes into focus when epige- jor one is Evo-Devo (M¨uller2007) which emphasizes netics is related to evolution (Jablonka and Raz 2009): the leading role of development in evolution. Evo-Devo genetic assimilation can be explained without assuming advocates a decisive role of phenotype rather than geno- TGEI. type in evolution. This view is well phrased by West- Eberhard: \Environmental induction is a major initia- tor of adaptive evolutionary change. The origin and evo- 2 Genome vs. Epigenome lution of adaptive novelty do not await mutation; on the contrary, genes are followers, not leaders, in evolution." The conventional gene-centric biology cannot properly (West-Eberhard 2003). The Evo-Devo view of evolution treat the relationship between phenotype and genotype. as represented by West-Eberhard is called \phenotype- The simple scheme that a gene determines a trait, or the driven evolution" in the present review. one-to-one correspondence between genes and traits, West-Eberhard proposed \genetic accommodation" has been rejected. Monozygotic twins, sharing the iden- as a mechanism of phenotype-driven evolution (West- tical genomes but exhibiting notable phenotypic differ- Eberhard 2003), which generalizes Waddington's notion ences, suffice as a simple counterexample against the of genetic assimilation. Her monograph (West-Eberhard gene-centric view. On the other hand, epigenetics can 2003) is full of circumstantial evidence supporting evo- consistently explain phenotypic differences resulting from lution by genetic accommodation. However, rather un- the identical genomes through ontogenesis (Fraga et al fortunately, she could not explain explicitly how a (non- 2005). Such phenomena stand out even more at the cel- heritable) phenotypic change is replaced with genetic lular level than at the individual level. That is, all the mutations as generations change (the point (b) above). cells in an individual originate from a single fertilized In order to clarify the problem, let us define \evo- egg and thus share the identical genome, nevertheless, lution" as follows: their phenotypes are extremely diverse depending on their cell types, tissues and organs. According to epi- Evolution is a process in which individuals genetics, these differences are due to the differences in that are adaptive to a given environment are nat- their \epigenomes." urally selected, and thereby fixing in the popula- The substance of epigenome is a set of chromatin tion the genotype that induces the adaptive phe- modifications consisting of
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