12Fast-moving animals need fast-acting sensory systems. Flying insects have thus evolved exceptionally 13 quick visual (1) and olfactory processing ability (2). For example, flighted insects can track the temporal 14 structure of turbulent odor plumes at rates above 100 Hz (3). The evolutionary lability of such sensory 15 systems, however, remains unknown. We test for rapid evolutionary shifts in olfactory processing speed 16 associated with flight loss, through neurobiological comparisons of sympatric flighted versus flightless 17 lineages within a wing-polymorphic stonefly species. Our analyses of sensory responses reveal that 18 recently-evolved flightless lineages have substantially degraded olfactory acuity. By comparing flighted 19 versus flightless ecotypes with similar genetic backgrounds (4), we eliminate other confounding factors 20 that might have affected the evolution of their olfactory reception mechanisms. Our detection of 21 different patterns of degraded olfactory sensitivity and speed in independently wing-reduced lineages 22highlights parallel evolution of sensory degeneration. These reductions in sensory ability also echo the 23 rapid vestigialization of wings themselves (4, 5), and represent a neurobiological parallel to the 24 convergent phenotypic shifts seen under sharp selective gradients in other systems (e.g. parallel loss of 25 vision in diverse cave fauna (6)). Our study provides the first direct evidence for the hypothesis that 26flight poses a selective pressure on the speed of olfactory receptor neurons. Our findings also emphasize 27 the energetic costs of rapid olfaction, and the key role of natural selection in shaping dramatic 28 neurobiological shifts. 29 30 31Significance Statement 32Flying insects move fast and have therefore evolved exceptionally quick-acting sensory systems. The 33speed with which such neurobiological shifts can evolve, however, remains unclear. Under the 'use it 34 or lose it' hypothesis, loss of flight should lead to degradation of this fast sensory processing ability. 35 We test for evolutionary reductions in olfactory acuity linked to flight loss, through neurobiological 36 comparisons of flightless versus flighted lineages within a wing-polymorphic insect. Our analyses 37 reveal that newly wing-reduced populations have substantially degraded olfactory acuity, with parallel 38 reductions in this sensory ability detected in independently flightless lineages. These findings reveal 39 that flight poses strong selective pressure for rapid olfaction, and highlight the potential of natural 40 selection in rapidly shaping adaptive shifts in animal sensory systems. 41 42The origin of flight posed novel challenges for animals' sensory systems, including the need for rapid 43 processing of environmental information. Major sensory shifts were needed to compensate for the fact 44 that flying animals move faster and therefore experience more rapid changes in sensory stimuli (vision: 45 (7, 8); olfaction: (2)). This need for rapid sensing seems to be particularly ...