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

View ORCID ProfileLaurel R. Yohe, Leith B. Leiser-Miller, Zofia A. Kaliszewska, Paul Donat, Sharlene E. Santana, Liliana M. Dávalos
doi: https://doi.org/10.1101/2020.12.31.424977
Laurel R. Yohe
1Department of Earth and Planetary Sciences, Yale University, 210 Whitney Ave. New Haven, CT 06511, USA
2Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building Stony Brook, NY 11794, USA
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  • ORCID record for Laurel R. Yohe
  • For correspondence: laurel.yohe@yale.edu
Leith B. Leiser-Miller
3Department of Biology, Life Sciences Building 4W, University of Washington, Seattle, WA, 98195, USA
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Zofia A. Kaliszewska
3Department of Biology, Life Sciences Building 4W, University of Washington, Seattle, WA, 98195, USA
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Paul Donat
2Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building Stony Brook, NY 11794, USA
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Sharlene E. Santana
3Department of Biology, Life Sciences Building 4W, University of Washington, Seattle, WA, 98195, USA
4Burke Museum of Natural History and Culture, University of Washington, 4300 15th Ave NE, Seattle, WA, 98105, USA
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Liliana M. Dávalos
2Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building Stony Brook, NY 11794, USA
5Consortium for Inter-Disciplinary Environmental Research, School of Marine and Atmospheric Sciences, Stony Brook University, 129 Dana Hall, Stony Brook, NY 11794, USA
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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 sentences The 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • E-mail Addresses: LRY: laurel.yohe{at}yale.edu

    LBM: leithmiller1{at}gmail.com

    ZAK: zakalisz{at}gmail.com

    PD: paul.donat{at}stonybrook.edu

    SES: ssantana{at}uw.edu

    LMD: liliana.davalos{at}stonybrook.edu

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 03, 2021.
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Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat
Laurel R. Yohe, Leith B. Leiser-Miller, Zofia A. Kaliszewska, Paul Donat, Sharlene E. Santana, Liliana M. Dávalos
bioRxiv 2020.12.31.424977; doi: https://doi.org/10.1101/2020.12.31.424977
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Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat
Laurel R. Yohe, Leith B. Leiser-Miller, Zofia A. Kaliszewska, Paul Donat, Sharlene E. Santana, Liliana M. Dávalos
bioRxiv 2020.12.31.424977; doi: https://doi.org/10.1101/2020.12.31.424977

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