Clock-linked genes underlie seasonal migratory timing in a diurnal raptor

Seasonal migration is a dynamic natural phenomenon that allows organisms to exploit favorable habitats across the annual cycle. While the morphological, physiological, and behavioral changes associated with migratory behavior are well characterized, the genetic basis of migration and its link to endogenous biological timekeeping pathways is poorly understood. Historically, genome-wide research has focused on genes of large effect, whereas many genes of small effect may work together to regulate complex traits like migratory behavior. Here, we explicitly relax stringent outlier detection thresholds and, as a result, discover how multiple biological timekeeping genes are important to migratory timing in an iconic raptor species, the American Kestrel (Falco sparverius). To validate the role of candidate loci in migratory timing, we genotyped Kestrels captured across autumn migration and found significant associations between migratory timing and genetic variation in metabolic and light input pathway genes that modulate biological clocks (TOP1, PHLPP1, CPNE4, and PEAK1). Further, we demonstrate that migrating individuals originated from a single panmictic source population, suggesting the existence of distinct early and late migratory genotypes (i.e. chronotypes). Overall, our results provide empirical support for the existence of a within population-level polymorphism in genes underlying migratory timing in a diurnally migrating raptor.