Epigenetic inheritance and reproductive mode in plants and animals

• Published in: Trends in ecology & evolution (Amsterdam) Vol. 36; no. 12; pp. 1124 - 1140
• Main Authors: Anastasiadi, Dafni, Venney, Clare J., Bernatchez, Louis, Wellenreuther, Maren
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.12.2021
• Subjects: adaptive plasticity; Animals; DNA Methylation; Epigenesis, Genetic; epigenetic inheritance; epigenomic variation; Epigenomics; Germ Cells; Inheritance Patterns; Phenotype; reproductive mode; transgenerational inheritance; DNA methylation; epigenomic variation; reproductive mode; transgenerational inheritance; adaptive plasticity; epigenetic inheritance
• ISSN: 0169-5347; 1872-8383
• DOI: 10.1016/j.tree.2021.08.006

Epigenetic inheritance is another piece of the puzzle of nongenetic inheritance, although the prevalence, sources, persistence, and phenotypic consequences of heritable epigenetic marks across taxa remain unclear. We systematically reviewed over 500 studies from the past 5 years to identify trends in the frequency of epigenetic inheritance due to differences in reproductive mode and germline development. Genetic, intrinsic (e.g., disease), and extrinsic (e.g., environmental) factors were identified as sources of epigenetic inheritance, with impacts on phenotype and adaptation depending on environmental predictability. Our review shows that multigenerational persistence of epigenomic patterns is common in both plants and animals, but also highlights many knowledge gaps that remain to be filled. We provide a framework to guide future studies towards understanding the generational persistence and eco-evolutionary significance of epigenomic patterns. Epigenetic mechanisms can alter gene expression and allow species to respond rapidly to their environments by modifying their phenotypes.Reproductive mode (i.e., sexual versus asexual, oviparity versus viviparity in animals) and germline development commonly predict the persistence of epigenetic marks.The consequences of persistent epigenomic variation vary depending on the sources (intrinsic, genetic, extrinsic).Environmental predictability is a key factor for determining the consequences of epigenetic inheritance on phenotype and fitness.We provide a roadmap for future studies to further our understanding of the extent and evolutionary importance of epigenetic inheritance by quantifying: (i) persistence across generations, (ii) contributions to phenotype and fitness, and (iii) cross-taxa comparisons.