Comparative epigenetics in animal physiology: An emerging frontier

Abstract

The unprecedented access to annotated genomes now facilitates the investigation of the molecular basis of epigenetic phenomena in phenotypically diverse animals. In this critical review, we describe the roles of molecular epigenetic mechanisms in regulating mitotically and meiotically stable spatiotemporal gene expression, phenomena that provide the molecular foundation for the intra-, inter-, and trans-generational emergence of physiological phenotypes. By focusing principally on emerging comparative epigenetic roles of DNA-level and transcriptome-level epigenetic mark dynamics in the emergence of phenotypes, we highlight the relationship between evolutionary conservation and innovation of specific epigenetic pathways, and their interplay as a priority for future study. This comparative approach is expected to significantly advance our understanding of epigenetic phenomena, as animals show a diverse array of strategies to epigenetically modify physiological responses. Additionally, we review recent technological advances in the field of molecular epigenetics (single-cell epigenomics and transcriptomics and editing of epigenetic marks) in order to (1) investigate environmental and endogenous factor dependent epigenetic mark dynamics in an integrative manner; (2) functionally test the contribution of specific epigenetic marks for animal phenotypes via genome and transcript-editing tools. Finally, we describe advantages and limitations of emerging animal models, which under the Krogh principle, may be particularly useful in the advancement of comparative epigenomics and its potential translational applications in animal science, ecotoxicology, ecophysiology, climate change science and wild-life conservation, as well as organismal health.