Abstract
Many organisms exhibit phenotypic plasticity that changes their traits in response to their environment. Whether or not this plasticity contributes to adaptive evolution is a fundamental question in evolutionary biology because various studies report that natural populations adapt to rapid environmental changes via plasticity, which often “triggers” novel adaptive traits. While such alternative phenotypes could be induced by nongenetic perturbations that include gene expression noise or epigenetic modification caused by environmental change, it remains unknown what molecular mechanism genetically fix the alternative phenotypes as adaptive traits passed into the next generation. Here we show that a decrease in methylated CpG sites leads to loss of plasticity, which triggers genetic fixation of novel traits, in medaka fish (Oryzias latipes). We found that the gut length was correlated with the number of methylated CpG sites upstream of the Plxnb3 gene. The medaka, in which the methylated DNA region is deleted by CRISPR/Cas9, showed a loss of plasticity in gut length.
Moreover, standing variation in the promoter region of another gene, Ppp3r1, 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 phenotypic plasticity plays a role as a buffer of evolution and contributes to environmental adaptation, as previously thought, our molecular data suggest that mutation on CpG site causing the loss of phenotypic plasticity, is the trigger for a generation of novel traits.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
Main text and figures revised, adding new experiments and their results; Supplemental files updated.
