Differential epigenetic regulation underlies evolutionary transition of seasonal migration

Seasonal migratory animals can evolve residency through adaptation. The threshold model of quantitative genetics predicts that residency evolves from migrants when genetic variation for lower liability, or a latent state underlying migratory propensity, is positively selected. However, it is unknown what cellular and molecular regulations underlie this process. The hypothalamus, which regulates physiology and behaviour of vertebrates by integrating internal and environmental conditions, is a strong candidate structure where migratory propensity may be regulated. To understand the hypothalamic molecular regulation underlying the evolutionary change to residency, we use the Eurasian blackcap system comprising ancestral migratory and derived resident populations. By combining a common-garden experiment with single-cell epigenetics, we compare genomic regions with open chromatin between migratory and resident populations and seasons. We find that the seasonal change in chromatin accessibility is reduced in residents across major cell types. This suggests that the evolutionary transition to residency involves a reduction in the amplitude of seasonal change in epigenetic states in multiple hypothalamic cell types, which may collectively represent migratory liability. Environmental shifts, such as deglaciation for blackcaps, may play an important role in exposing and selecting variation in the seasonal reaction norm of liability underlying the evolution of seasonal plastic traits. This article is part of the theme issue 'Ecological epigenetics at the intersection of behaviour and life history variation in non-model animals'.