Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

M. Lisandra Zepeda Mendoza, Zijun Xiong, Marina Escalera-Zamudio, Anne Kathrine Runge, Julien Thézé, Daniel Streicker, Hannah K. Frank, Elizabeth Loza-Rubio, Shengmao Liu, Oliver A. Ryder, Jose Alfredo Samaniego Castruita, Aris Katzourakis, George Pacheco, Blanca Taboada, Ulrike Löber, Oliver G. Pybus, Yang Li, Edith Rojas-Anaya, Kristine Bohmann, Aldo Carmona Baez & 9 others Carlos F. Arias, Shiping Liu, Alex D. Greenwood, Mads F. Bertelsen, Nicole E. White, Michael Bunce, Guojie Zhang, Thomas Sicheritz-Pontén*, M. P.Thomas Gilbert

*Corresponding author for this work

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    Abstract

    Adaptation to specialized diets often requires modifications at both genomic and microbiome levels. We applied a hologenomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate blood-feeding (sanguivorous) mammals, to study the evolution of its complex dietary adaptation. Specifically, we assembled its high-quality reference genome (scaffold N50 = 26.9 Mb, contig N50 = 36.6 kb) and gut metagenome, and compared them against those of insectivorous, frugivorous and carnivorous bats. Our analyses showed a particular common vampire bat genomic landscape regarding integrated viral elements, a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles, and that both genetic elements harbour key traits related to the nutritional (for example, vitamin and lipid shortage) and non-nutritional (for example, nitrogen waste and osmotic homeostasis) challenges of sanguivory. These findings highlight the value of a holistic study of both the host and its microbiota when attempting to decipher adaptations underlying radical dietary lifestyles.
    Original languageEnglish
    JournalNature Ecology & Evolution
    Volume2
    Pages (from-to)659-668
    ISSN2397-334X
    DOIs
    Publication statusPublished - 2018

    Bibliographical note

    Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

    Cite this

    Zepeda Mendoza, M. L., Xiong, Z., Escalera-Zamudio, M., Runge, A. K., Thézé, J., Streicker, D., ... Gilbert, M. P. T. (2018). Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nature Ecology & Evolution, 2, 659-668. https://doi.org/10.1038/s41559-018-0476-8
    Zepeda Mendoza, M. Lisandra ; Xiong, Zijun ; Escalera-Zamudio, Marina ; Runge, Anne Kathrine ; Thézé, Julien ; Streicker, Daniel ; Frank, Hannah K. ; Loza-Rubio, Elizabeth ; Liu, Shengmao ; Ryder, Oliver A. ; Samaniego Castruita, Jose Alfredo ; Katzourakis, Aris ; Pacheco, George ; Taboada, Blanca ; Löber, Ulrike ; Pybus, Oliver G. ; Li, Yang ; Rojas-Anaya, Edith ; Bohmann, Kristine ; Carmona Baez, Aldo ; Arias, Carlos F. ; Liu, Shiping ; Greenwood, Alex D. ; Bertelsen, Mads F. ; White, Nicole E. ; Bunce, Michael ; Zhang, Guojie ; Sicheritz-Pontén, Thomas ; Gilbert, M. P.Thomas. / Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. In: Nature Ecology & Evolution. 2018 ; Vol. 2. pp. 659-668.
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    abstract = "Adaptation to specialized diets often requires modifications at both genomic and microbiome levels. We applied a hologenomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate blood-feeding (sanguivorous) mammals, to study the evolution of its complex dietary adaptation. Specifically, we assembled its high-quality reference genome (scaffold N50 = 26.9 Mb, contig N50 = 36.6 kb) and gut metagenome, and compared them against those of insectivorous, frugivorous and carnivorous bats. Our analyses showed a particular common vampire bat genomic landscape regarding integrated viral elements, a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles, and that both genetic elements harbour key traits related to the nutritional (for example, vitamin and lipid shortage) and non-nutritional (for example, nitrogen waste and osmotic homeostasis) challenges of sanguivory. These findings highlight the value of a holistic study of both the host and its microbiota when attempting to decipher adaptations underlying radical dietary lifestyles.",
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    Zepeda Mendoza, ML, Xiong, Z, Escalera-Zamudio, M, Runge, AK, Thézé, J, Streicker, D, Frank, HK, Loza-Rubio, E, Liu, S, Ryder, OA, Samaniego Castruita, JA, Katzourakis, A, Pacheco, G, Taboada, B, Löber, U, Pybus, OG, Li, Y, Rojas-Anaya, E, Bohmann, K, Carmona Baez, A, Arias, CF, Liu, S, Greenwood, AD, Bertelsen, MF, White, NE, Bunce, M, Zhang, G, Sicheritz-Pontén, T & Gilbert, MPT 2018, 'Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat', Nature Ecology & Evolution, vol. 2, pp. 659-668. https://doi.org/10.1038/s41559-018-0476-8

    Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. / Zepeda Mendoza, M. Lisandra; Xiong, Zijun; Escalera-Zamudio, Marina; Runge, Anne Kathrine; Thézé, Julien; Streicker, Daniel; Frank, Hannah K.; Loza-Rubio, Elizabeth; Liu, Shengmao; Ryder, Oliver A.; Samaniego Castruita, Jose Alfredo; Katzourakis, Aris; Pacheco, George; Taboada, Blanca; Löber, Ulrike; Pybus, Oliver G.; Li, Yang; Rojas-Anaya, Edith; Bohmann, Kristine; Carmona Baez, Aldo; Arias, Carlos F.; Liu, Shiping; Greenwood, Alex D.; Bertelsen, Mads F.; White, Nicole E.; Bunce, Michael; Zhang, Guojie; Sicheritz-Pontén, Thomas; Gilbert, M. P.Thomas.

    In: Nature Ecology & Evolution, Vol. 2, 2018, p. 659-668.

    Research output: Contribution to journalJournal articleResearchpeer-review

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    AU - Xiong, Zijun

    AU - Escalera-Zamudio, Marina

    AU - Runge, Anne Kathrine

    AU - Thézé, Julien

    AU - Streicker, Daniel

    AU - Frank, Hannah K.

    AU - Loza-Rubio, Elizabeth

    AU - Liu, Shengmao

    AU - Ryder, Oliver A.

    AU - Samaniego Castruita, Jose Alfredo

    AU - Katzourakis, Aris

    AU - Pacheco, George

    AU - Taboada, Blanca

    AU - Löber, Ulrike

    AU - Pybus, Oliver G.

    AU - Li, Yang

    AU - Rojas-Anaya, Edith

    AU - Bohmann, Kristine

    AU - Carmona Baez, Aldo

    AU - Arias, Carlos F.

    AU - Liu, Shiping

    AU - Greenwood, Alex D.

    AU - Bertelsen, Mads F.

    AU - White, Nicole E.

    AU - Bunce, Michael

    AU - Zhang, Guojie

    AU - Sicheritz-Pontén, Thomas

    AU - Gilbert, M. P.Thomas

    N1 - Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

    PY - 2018

    Y1 - 2018

    N2 - Adaptation to specialized diets often requires modifications at both genomic and microbiome levels. We applied a hologenomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate blood-feeding (sanguivorous) mammals, to study the evolution of its complex dietary adaptation. Specifically, we assembled its high-quality reference genome (scaffold N50 = 26.9 Mb, contig N50 = 36.6 kb) and gut metagenome, and compared them against those of insectivorous, frugivorous and carnivorous bats. Our analyses showed a particular common vampire bat genomic landscape regarding integrated viral elements, a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles, and that both genetic elements harbour key traits related to the nutritional (for example, vitamin and lipid shortage) and non-nutritional (for example, nitrogen waste and osmotic homeostasis) challenges of sanguivory. These findings highlight the value of a holistic study of both the host and its microbiota when attempting to decipher adaptations underlying radical dietary lifestyles.

    AB - Adaptation to specialized diets often requires modifications at both genomic and microbiome levels. We applied a hologenomic approach to the common vampire bat (Desmodus rotundus), one of the only three obligate blood-feeding (sanguivorous) mammals, to study the evolution of its complex dietary adaptation. Specifically, we assembled its high-quality reference genome (scaffold N50 = 26.9 Mb, contig N50 = 36.6 kb) and gut metagenome, and compared them against those of insectivorous, frugivorous and carnivorous bats. Our analyses showed a particular common vampire bat genomic landscape regarding integrated viral elements, a dietary and phylogenetic influence on gut microbiome taxonomic and functional profiles, and that both genetic elements harbour key traits related to the nutritional (for example, vitamin and lipid shortage) and non-nutritional (for example, nitrogen waste and osmotic homeostasis) challenges of sanguivory. These findings highlight the value of a holistic study of both the host and its microbiota when attempting to decipher adaptations underlying radical dietary lifestyles.

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    JF - Nature Ecology & Evolution

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    Zepeda Mendoza ML, Xiong Z, Escalera-Zamudio M, Runge AK, Thézé J, Streicker D et al. Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nature Ecology & Evolution. 2018;2:659-668. https://doi.org/10.1038/s41559-018-0476-8