Adaptive evolution of olfactory degeneration in recently flightless insects

Fast-moving animals need fast-acting sensory systems. Flying insects have thus evolved exceptionally quick visual (1) and olfactory processing ability (2). For example, flighted insects can track the temporal structure of turbulent odor plumes at rates above 100 Hz (3). The evolutionary lability of such sensory systems, however, remains unknown. We test for rapid evolutionary shifts in olfactory processing speed associated with flight loss, through neurobiological comparisons of sympatric flighted versus flightless lineages within a wing-polymorphic stonefly species. Our analyses of sensory responses reveal that recently-evolved flightless lineages have substantially degraded olfactory acuity. By comparing flighted versus flightless ecotypes with similar genetic backgrounds (4), we eliminate other confounding factors that might have affected the evolution of their olfactory reception mechanisms. Our detection of different patterns of degraded olfactory sensitivity and speed in independently wing-reduced lineages highlights parallel evolution of sensory degeneration. These reductions in sensory ability also echo the rapid vestigialization of wings themselves (4, 5), and represent a neurobiological parallel to the convergent phenotypic shifts seen under sharp selective gradients in other systems (e.g. parallel loss of vision in diverse cave fauna (6)). Our study provides the first direct evidence for the hypothesis that flight poses a selective pressure on the speed of olfactory receptor neurons. Our findings also emphasize the energetic costs of rapid olfaction, and the key role of natural selection in shaping dramatic neurobiological shifts. Significance StatementFlying insects move fast and have therefore evolved exceptionally quick-acting sensory systems. The speed with which such neurobiological shifts can evolve, however, remains unclear. Under the use it or lose it hypothesis, loss of flight should lead to degradation of this fast sensory processing ability. We test for evolutionary reductions in olfactory acuity linked to flight loss, through neurobiological comparisons of flightless versus flighted lineages within a wing-polymorphic insect. Our analyses reveal that newly wing-reduced populations have substantially degraded olfactory acuity, with parallel reductions in this sensory ability detected in independently flightless lineages. These findings reveal that flight poses strong selective pressure for rapid olfaction, and highlight the potential of natural selection in rapidly shaping adaptive shifts in animal sensory systems.