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Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding

Moritz Blumer, Tom Brown, Mariella Bontempo Freitas, Ana Luiza Destro, Juraci A. Oliveira, Ariadna Morales, Tilman Schell, Carola Greve, Martin Pippel, David Jebb, Nikolai Hecker, Alexis-Walid Ahmed, Bogdan Kirilenko, Maddy Foote, Axel Janke, Burton K. Lim, Michael Hiller
doi: https://doi.org/10.1101/2021.10.18.462363
Moritz Blumer
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
3Center for Systems Biology Dresden, 01307 Dresden, Germany
4Goethe-University, Faculty of Biosciences, Max-von-Laue-Str. 9, 60438 Frankfurt, Germany
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Tom Brown
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
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Mariella Bontempo Freitas
5Federal University of Viçosa, Department of Animal Biology, Viçosa, Brazil
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Ana Luiza Destro
5Federal University of Viçosa, Department of Animal Biology, Viçosa, Brazil
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Juraci A. Oliveira
6Federal University of Viçosa, Department of General Biology, Viçosa, Brazil
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Ariadna Morales
4Goethe-University, Faculty of Biosciences, Max-von-Laue-Str. 9, 60438 Frankfurt, Germany
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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Tilman Schell
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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Carola Greve
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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Martin Pippel
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
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David Jebb
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
3Center for Systems Biology Dresden, 01307 Dresden, Germany
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Nikolai Hecker
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
3Center for Systems Biology Dresden, 01307 Dresden, Germany
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Alexis-Walid Ahmed
4Goethe-University, Faculty of Biosciences, Max-von-Laue-Str. 9, 60438 Frankfurt, Germany
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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Bogdan Kirilenko
4Goethe-University, Faculty of Biosciences, Max-von-Laue-Str. 9, 60438 Frankfurt, Germany
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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Maddy Foote
9Native Bat Conservation Program, Toronto Zoo, 361A Old Finch Avenue, Toronto, Canada
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Axel Janke
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
10Senckenberg Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325 Frankfurt am Main, Germany
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Burton K. Lim
11Royal Ontario Museum, Department of Natural History, 100 Queen’s Park, M5S 2C6 Toronto, Ontario, Canada
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Michael Hiller
1Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany
2Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
3Center for Systems Biology Dresden, 01307 Dresden, Germany
4Goethe-University, Faculty of Biosciences, Max-von-Laue-Str. 9, 60438 Frankfurt, Germany
7LOEWE Centre for Translational Biodiversity Genomics, Senckenberganlage 25, 60325 Frankfurt, Germany
8Senckenberg Research Institute, Senckenberganlage 25, 60325 Frankfurt, Germany
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  • For correspondence: Michael.Hiller@senckenberg.de
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Abstract

Feeding exclusively on blood, vampire bats represent the only obligate sanguivorous lineage among mammals. To uncover genomic changes associated with adaptations to this unique dietary specialization, we generated a new haplotype-resolved reference-quality genome of the common vampire bat (Desmodus rotundus) and screened 26 bat species for genes that were specifically lost in the vampire bat lineage. We discovered previously-unknown gene losses that relate to metabolic and physiological changes, such as reduced insulin secretion (FFAR1, SLC30A8), limited glycogen stores (PPP1R3E), and a distinct gastric physiology (CTSE). Other gene losses likely reflect the biased nutrient composition (ERN2, CTRL) and distinct pathogen diversity of blood (RNASE7). Interestingly, the loss of REP15 likely helped vampire bats to adapt to high dietary iron levels by enhancing iron excretion and the loss of the 24S-hydroxycholesterol metabolizing enzyme CYP39A1 could contribute to their exceptional cognitive abilities. Finally, losses of key cone phototransduction genes (PDE6H, PDE6C) suggest that these strictly-nocturnal bats completely lack cone-based vision. These findings enhance our understanding of vampire bat biology and the genomic underpinnings of adaptations to sanguivory.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted October 19, 2021.
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Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding
Moritz Blumer, Tom Brown, Mariella Bontempo Freitas, Ana Luiza Destro, Juraci A. Oliveira, Ariadna Morales, Tilman Schell, Carola Greve, Martin Pippel, David Jebb, Nikolai Hecker, Alexis-Walid Ahmed, Bogdan Kirilenko, Maddy Foote, Axel Janke, Burton K. Lim, Michael Hiller
bioRxiv 2021.10.18.462363; doi: https://doi.org/10.1101/2021.10.18.462363
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Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding
Moritz Blumer, Tom Brown, Mariella Bontempo Freitas, Ana Luiza Destro, Juraci A. Oliveira, Ariadna Morales, Tilman Schell, Carola Greve, Martin Pippel, David Jebb, Nikolai Hecker, Alexis-Walid Ahmed, Bogdan Kirilenko, Maddy Foote, Axel Janke, Burton K. Lim, Michael Hiller
bioRxiv 2021.10.18.462363; doi: https://doi.org/10.1101/2021.10.18.462363

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