Contemporary Evolution of Reproductive Isolation and Phenotypic Divergence in Sympatry along a Migratory Divide

Abstract

Understanding the influence of human-induced changes on the evolutionary trajectories of populations is a fundamental problem [1, 2]. The evolution of reproductive isolation in sympatry is rare, relying on strong selection along steep ecological gradients [3-7]. Improved wintering conditions owing to human activities promoted the recent establishment of a migratory divide in Central European blackcaps (Sylvia atricapilla) [8, 9]. Here, we show that differential migratory orientation facilitated reproductive isolation of sympatric populations within <30 generations. The genetic divergence in sympatry exceeds that of allopatric blackcaps separated by 800 km and is associated with diverse phenotypic divergence. Blackcaps migrating along the shorter northwestern route have rounder wings and narrower beaks and differ in beak and plumage color from sympatric southwest-migrating birds. We suggest that distinct wing and beak morphologies are ecomorphological adaptations resulting from divergent, multifarious selection regimes during migration. We hypothesize that restricted gene flow accelerates the evolution of adaptive phenotypic divergence toward the contrasting selection regimes. Similar adaptive processes can occur in more than 50 bird species that recently changed their migratory behavior [10, 11] or in species with low migratory connectivity. Our study thus illustrates how ecological changes can rapidly drive the contemporary evolution of ecotypes.