Canalization masks high levels of cryptic epigenetic and transcriptional plasticity in butterflies

Abstract

Phenotypic plasticity is a common adaptation to heterogeneous environments. While it is well documented that trait plasticity can rapidly evolve, little is known about the developmental mechanisms that underlie variation in plasticity. Here, we compare diverged populations of the common buckeye butterfly (Junonia coenia): one population with canalized wing patterns that are insensitive to environmental conditions and another population that has distinctive seasonal color patterns. In common garden trials we were surprised to find dramatically elevated levels of transcriptional and chromatin accessibility plasticity during wing development of the canalized population compared to the seasonally plastic population. Further, using machine learning analysis of accessible chromatin sequences, we observed a broad heterochronic shift in motifs enriched in plastic putative regulatory elements to earlier stages of development in the canalized population, which we speculate may cause phenotype-related gene expression to move outside a wing color critical period. Together, our data lead us to propose a model where cryptic genetic processes are masked by a shift in chromatin remodeling, which in turn could produce a capacitor-like effect to maintain developmental genetic variation in the canalized population.