Mechanisms underlying the loss of migratory behaviour in a long-lived bird

ABSTRACT Human-induced environmental changes are shifting the migration patterns of birds worldwide. Species are adjusting migration timings, shortening and diversifying migratory routes, or even completely disrupting migration and transitioning towards residency. Whilst the ultimate causes driving changes in migratory patterns are well established, the underlying mechanisms by which migratory species adapt to environmental change remain unclear. Here, we studied the mechanisms driving the recent and rapid loss of migratory behaviour in Iberian white storks Ciconia ciconia , a long-lived and previously fully migratory species through the African-Eurasian flyway. We combined 25 years of census data, GPS-tracking data from 213 individuals (80 adults and 133 first-year juveniles) followed for multiple years, and whole-genome sequencing, to disentangle whether within- (phenotypic flexibility) or between- (developmental plasticity or microevolution, through selection) individual shifts in migratory behaviour over time can explain the observed population-level changes towards residency. Between 1995 and 2020, the proportion of individuals no longer migrating and remaining in Southern Europe year-round increased dramatically, from 18% to 68-83%. We demonstrate that this behavioural shift is likely explained by developmental plasticity. Within first-year birds, 98% crossed the Strait of Gibraltar towards their African wintering grounds, in Morocco or Sub-Saharan Africa. However, the majority shifted towards a non-migratory strategy as they aged - the proportion of migrants decreased to 67% and 33%, on their second and third year of life, respectively - suggesting that migratory behaviour is determined during ontogeny. Supporting these findings, only 19% of GPS-tracked adults migrated. Moreover, we did not find evidence of phenotypic flexibility, as adults were highly consistent in migratory behaviour over multiple years (only 3 individuals changed strategy between years, out of 113 yearly transitions), nor of selection acting on genetic variation, since genomes of migrants and residents are essentially undifferentiated. Our results suggest that through developmental plasticity, traits that are plastic during specific windows of development, become fixed during adulthood. Thus, inter-generational shifts in the frequency of migratory and non-migratory young individuals could drive population changes in migratory behaviour. This can provide a fast mechanism for long-lived migratory birds to respond to rapid human-driven environmental changes.