Adaptive evolution of olfactory degeneration in recently flightless insects

Abstract

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 ...

Floral and Bird Excreta Semiochemicals Attract Western Carpenter Ants

“…Foragers would likely accrue significant energy savings for themselves and for their entire colony if they were able to sense olfactory cues from both carbohydrate and protein sources, and to engage in long-distance orientation toward them. If forager ants had reduced olfactory acuity, like other flightless insects (Neupert et al, 2020), they might not be able to recognize the specific odor profiles of multiple food sources but might still be able to locate them by responding to key odorants shared between food sources. Working with Western carpenter ants as a model species, we show that foragers are capable of long-distance orientation toward both carbohydrate and protein food sources.…”

“…Our prediction that foraging ants are reliant upon a simple olfactory search 'image' for nectar odor cues was not supported by the data. The prediction was inspired by previous reports that flightless insects have poor olfactory acuity (Neupert et al, 2020). With a simple search image, 'featuring' only those floral constituents that are shared between plants, foraging ants would be able to locate and exploit multiple and diverse nectar sources.…”

“…If worker ants had reduced olfactory acuity, like other flightless insects (Neupert et al, 2020), they would not likely be able to recognize the specific odor profiles of diverse food sources but might still be able to locate them by responding to key odorants shared between these sources. For example, many inflorescences that provide essential carbohydrates to pollinators share linalool and α-pinene as floral attractants (Knudsen et al, 2006;Nicolson, 2011).…”

Genomic signatures of parallel alpine adaptation in recently evolved flightless insects

“…Putative functions of such genes were determined using the UniProtKB database (https://www.uniprot.org/). In addition to focusing on genes potentially associated with flight loss, we also searched for genes potentially associated with additional alpine adaptations, including potential olfactory shifts (Neupert et al, 2020), increased body size (McCulloch & Waters, 2018a), delayed emergence (McCulloch & Waters, 2018b), increased longevity (McLellan, 1999) and increased fecundity (Guerra, 2011), as well as genes that might potentially be involved in reproductive isolation among sympatric ecotypes (e.g., sexual development; Kroos, McCulloch, Foster, et al, 2021; McCulloch, Foster, Dutoit, et al, 2019; Waters, & McCulloch, 2021).…”