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Abstract Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants. 

Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats ( Carollia spp.) and plants ( Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper . Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper , our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity. 

Sensory systems perform fitness‐relevant functions, and specialized sensory structures allow organisms to accomplish challenging tasks. However, broad comparative analyses of sensory morphologies and their performance are lacking for diverse mammalian radiations.

Neotropical leaf‐nosed bats (Phyllostomidae) are one of the most ecologically diverse mammal groups; including a wide range of diets and foraging behaviours, and extreme morphological variation in external sensory structures used in echolocation (nose leaf and pinnae).

We coupled 3D geometric morphometrics and acoustic field recordings under a phylogenetic framework to investigate the mechanisms underlying the diversification of external sensory morphologies in phyllostomids, and explored the potential implications of sensory morphological diversity to functional outputs and dietary ecology.

We found that the nose leaf consists of two evolutionary modules—spear and horseshoe—suggesting that modularity enabled morphological and functional diversification of this structure.

We found a significant association between some aspects of nose leaf shape and maximum frequency and bandwidth of echolocation calls, but not between pinnae shape and echolocation call parameters. This may be explained by the use of multiple sensory modes across phyllostomids and plasticity of some echolocation call parameters.

Species with different diets significantly differed in nose leaf shape, specifically in spear breadth, presence of a midrib, and cupping and anterior rotation of the horseshoe. This may relate to different levels of prey type specificity within each diet. Pinnae shape significantly differed between species that consume non‐mobile, non‐evasive prey (broad rounded, cupped pinnae) and mobile, evasive prey (flattened pinnae with a sharp tapering apex). This may reflect the use of different sound cues to detect prey.

Our results give insight into the morphological evolution of external sensory structures in bats, and highlight new links between morphological diversity and ecology.

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