Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat
Authors: Yohe Laurel R. , Leiser-Miller Leith B. , Kaliszewska Zofia A. , Donat Paul , Santana Sharlene E. , Dávalos Liliana M. 
Published: January 2021

Mammalianolfactory receptors(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 andORrepertoires is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinctORrepertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of more specializedORrepertoires has never been tested. Using targeted sequence capture, we sequenced theORrepertoires of three sympatric species of short-tailed leaf-nosed bats (Carollia), which vary in their degree of specialization on the fruits ofPiperplants. We characterized orthologous versus duplicated receptors amongCarolliaspecies, and identified orthologous receptors and associated paralogs to explore the diversity and redundancy of the receptor gene repertoire. The most dedicatedPiperspecialist,Carollia castanea, had lowerORdiversity compared to the two more generalist species (sowelli, perspicillata), but we discovered a few unique sets ofORs withinC. castaneawith exceptional redundancy of similar gene duplicates. These unique receptors potentially enableC. castaneato detectPiperfruit odorants to an extent that the other species cannot.C. perspicillata, the species with the most generalist diet, had a larger diversity of functional receptors, suggesting the ability to detect a wider range of odorant molecules. The variation amongORs 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 plays a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants.

Impact Statement—though it asks for 3-4 sentences

The sense of smell is essential to how many animals detect food, yet few studies have demonstrated how dietary evolution has shapedolfactory receptorgenes, which encode proteins that bind to environmental scent cues, including food odorants. We compared the evolutionary history of olfactory receptor repertoires in three co-occurring neotropical bat species along a spectrum of dietary specialization on the fruits ofPiperplants. We found the more generalist species possessed a more diverse olfactory receptor profile, potentially reflecting an ability to detect more diverse arrays of fruit scent compounds, while the specialist had a narrower profile that demonstrated more redundancy. By introducing creative approaches to measure diversity in large gene families and connecting diet specialization and molecular diversity, this study makes an unprecedented contribution to evolutionary biology.