DNA methylation site loss for plasticity-led novel trait genetic fixation

Abstract

<jats:p>Many organisms exhibit phenotypic plasticity that changes their traits in response to their environment. Although whether or not this plasticity contributes to adaptive evolution is a fundamental question in evolutionary biology, various studies report that natural populations adapt to rapid environmental changes via plasticity, which leads to novel adaptive traits as "triggers." Namely, phenotypic plasticity has considered allowing an accumulation of genetic mutations to fix the alternative phenotypes induced by nongenetic perturbations that include gene expression noise or epigenetic modification caused by environmental change. However, because the molecular mechanism of phenotypic plasticity is unknown, verification of the process from phenotypic plasticity to genetic fixation remains insufficient. Here we show that decrease in methylated CpG sites leads to loss of plasticity, which triggers genetic fixation of novel traits, in medaka fish (<jats:italic>Oryzias latipes</jats:italic>). We found that the gut length was correlated with the number of methylated CpG sites upstream of the <jats:italic>Plxnb3</jats:italic> gene, which is involved in the developmental process of nerve axons. The medaka, in which the methylated DNA region is deleted by CRISPR/Cas9, showed a loss of plasticity in gut length and a lower survival rate caused by nonoptimal feeding environments. Moreover, standing variation in the promoter region of another gene, <jats:italic>Ppp3r1</jats:italic>, which is also related to nerve axon development, raised the gene expression and made a longer gut stably in wild medaka groups that lost the gut-length plasticity. Furthermore, our phylogenetic analysis revealed the timing of these evolutionary events, indicating that the loss of phenotypic plasticity by nucleotide substitutions initiates the process of genetic fixation of the novel trait. That is, while the CpG island plays a role as a buffer of evolution through phenotypic plasticity and contributes to environmental adaptation, as previously thought, our molecular data suggest that mutation, not phenotypic plasticity, is the trigger for a generation of novel traits.</jats:p>

A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive

“…Recent findings are increasingly solidifying the view that plasticity is genetically variable: whether studied as crossing reaction norms, molecular mechanisms (Aubin‐Horth and Renn 2009 ), epigenetically controlled changes in expression (Katsumura et al. 2020 ), or IGEs arising from the social environment (Bailey et al. 2017 ).…”