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 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 OR repertoires with narrower diversity 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 versus 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, 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 underlies patterns of ecological interactions between bats and plants.

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical 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.…”

When morphology does not fit the genomes: the case of rodent olfaction

“…In this context, it is challenging to interpret how the number of OR genes impact the olfactory capabilities. For this, it will be critical to map the level of gene expression and their composition on the olfactory turbinals [15,58].…”

“…At the genomic level, OR genes encode the most represented chemosensory receptors in mammals, and constitute the largest multigenic superfamily categorized into about 13 gene families [3,9,10]. Moreover, the number of functional and pseudogenized OR genes and their composition vary highly along mammalian phylogeny [3,9] and with species ecology [9][10][11][12][13][14][15]. This is for example the case for diet [10,13,15] or ecological lifestyle [11,14,16,17].…”

“…Moreover, the number of functional and pseudogenized OR genes and their composition vary highly along mammalian phylogeny [3,9] and with species ecology [9][10][11][12][13][14][15]. This is for example the case for diet [10,13,15] or ecological lifestyle [11,14,16,17]. Therefore, OR genes are expected to covary with morphological olfactory-related proxies such as olfactory turbinals.…”

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 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).…”