Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

Abstract

Mammalian olfactory 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 and OR repertoires 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 more specialized OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed leaf-nosed bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous versus duplicated receptors among Carollia species, and identified orthologous receptors and associated paralogs to explore the diversity and redundancy of the receptor gene repertoire. The most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two more generalist species (sowelli, perspicillata), but we discovered a few unique sets of ORs within C. castanea with exceptional redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit 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 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 plays a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants.Impact Statement—though it asks for 3-4 sentencesThe sense of smell is essential to how many animals detect food, yet few studies have demonstrated how dietary evolution has shaped olfactory receptor genes, 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 of Piper plants. 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.

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

“…Based on our results, we now hypothesize that standing variation in highly evolvable OR genes and morphology is fine-tuned in plant-visiting phyllostomid bats. Indeed, a recent analysis recently noted a refinement of OR diversity at shallower evolutionary scales within a sympatric genus (Yohe et al 2021). A complex interplay of hypervariable morphology (Fig.…”

“…Indeed, a recent analysis recently noted a refinement of OR diversity at shallower evolutionary scales within a sympatric genus (Yohe et al. 2021). A complex interplay of hypervariable morphology (Fig.…”

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

“…Comparative analyses have provided great insights into the role of OR or VR repertoire evolution in diversification and ecological adaptations (e.g. dietary specialisation (Hayden et al 2014; Yohe et al 2021) or adaptation to different life-styles (Shi and Zhang 2007; Hayden et al 2010; Khan et al 2015; Jiao et al 2019). At microevolutionary scales, studies are scarce due to the difficulty of analysing these gene families and linking their genetic variation to relevant adaptive phenotypes and selective regimes (but see (Smadja et al 2012; Li et al 2015; Poelstra et al 2018; Auer et al 2020).…”

Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism

“…How VOCs are perceived by bats, and to what extent their responses to scents are innate or learned also remain unknown. While the C. perspicillata olfactory receptor repertoire appears nondescript compared to those of non-frugivorous phyllostomids, C. castanea repertoires are distinctive even within the genus, likely contributing to Piper specialization [67]. This may have important consequences for the proposed coevolution with chemical fruit traits.…”