Evolutionary potential of natal dispersal in multiple blue tit populations while accounting for spatial autocorrelation among relatives

Mathis Ballet , Amélie Fargevieille, Christophe De Franceschi, Benjamin Penaud, anne charmantier, Laura Gervais

Natal dispersal is a key driver of ecological and evolutionary dynamics in populations. However, our understanding of genetic mechanisms underlying inter-individual variation in dispersal behaviour is still incomplete, despite their crucial role in the evolutionary potential and persistence of wild populations. Here, we investigate the genetic basis of natal dispersal distance in four blue tit (Cyanistes caeruleus) populations monitored for 26 to 48 years, using multi-generational social pedigrees and Restriction-site Association DNA sequencing genomic data. We combine quantitative genetic analyses (2,718 individuals), a permutation-based approach and genome-wide associations analyses (139 individuals). We find some evidence for additive genetic variance in natal dispersal distance, with heritability varying from 0.03 [<0.001-0.11] to 0.13 [<0.001-0.22] and evolvability ranging from 0.09 to 0.16. Permutation tests and power analyses reveal that spatial arrangement of nest boxes can generate spurious estimates of additive genetic variance in three of our four focal populations. We identified four single-nucleotide polymorphisms associated with natal dispersal distance, related with central nervous, metabolism and endocrine systems, which are key determinants of movement abilities. Overall, our study suggests that natal dispersal exhibits evolutionary potential, although this signal is partially obscured by spatial autocorrelation, potentially constraining population persistence under increasing habitat loss and fragmentation.