Rapid and biased evolution of canalization during adaptive divergence revealed by dominance in gene expression variability during Arctic charr early development

Abstract

Adaptive evolution may be influenced by canalization, the buffering of developmental processes from environmental and genetic perturbations, but how this occurs is poorly understood. Here, we explore how gene expression variability evolves in diverging and hybridizing populations, by focusing on the Arctic charr (Salvelinus alpinus) of Thingvallavatn, a classic case of divergence between feeding habitats. We report distinct profiles of gene expression variance for both coding RNAs and microRNAs between the offspring of two contrasting morphs (benthic/limnetic) and their hybrids reared in common conditions and sampled at two key points of cranial development. Gene expression variance in the hybrids is substantially affected by maternal effects, and many genes show biased expression variance toward the limnetic morph. This suggests that canalization, as inferred by gene expression variance, can rapidly diverge in sympatry through multiple gene pathways, which are associated with dominance patterns possibly biasing evolutionary trajectories and mitigating the effects of hybridization on adaptive evolution.