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The epigenetic basis of evolution

Journal

PROGRESS IN BIOPHYSICS & MOLECULAR BIOLOGY
Volume 178, Issue -, Pages 57-69

Publisher

PERGAMON-ELSEVIER SCIENCE LTD
DOI: 10.1016/j.pbiomolbio.2023.01.005

Keywords

Sperm-mediated transgenerational inheritance; Embryonic totipotency; LINE-1; Epigenetics; Evolution

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An increasing amount of data show that epigenetics plays key roles in evolutionary processes. This manuscript aims to gather experimental evidence supporting the involvement of epigenetic factors and networks during embryogenesis in inducing variation, which is crucial for evolution as a global process. This process occurs through the flow of RNA-based information carried by somatic cells exposed to environmental stimuli and delivered to oocytes by spermatozoa, as well as the permissive environments provided by zygotes and totipotent early embryos. These environments promote the emergence of evolutionarily significant phenotypic novelties driven by RNA information, making random genomic mutations and natural selection unnecessary.
An increasing body of data are revealing key roles of epigenetics in evolutionary processes. The scope of this manuscript is to assemble in a coherent frame experimental evidence supporting a role of epigenetic factors and networks, active during embryogenesis, in orchestrating variation-inducing phenomena underlying evolution, seen as a global process. This process unfolds over two crucial levels: i) a flow of RNA-based information predominantly small regulatory RNAs released from somatic cells exposed to environmental stimuli - taken up by spermatozoa and delivered to oocytes at fertilization and ii) the highly permissive and variation-prone environments offered by zygotes and totipotent early embryos. Totipotent embryos provide a variety of biological tools favouring the emergence of evolutionarily significant phenotypic novelties driven by RNA information. Under this light, neither random genomic mutations, nor the sieving role of natural selection are required, as the sperm-delivered RNA cargo conveys specific information and acts as phenotypic-inducer of defined environmentally acquired traits.

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