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; 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

doi:10.1038/s41559-018-0476-8

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 BaezCarlos 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

Microbes, Infections and Microbiomes

Research output: Contribution to journal › Article › peer-review

47 Citations (Scopus)

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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 language	English
Pages (from-to)	659-668
Number of pages	10
Journal	Nature Ecology and Evolution
Volume	2
Issue number	4
Early online date	19 Feb 2018
DOIs	https://doi.org/10.1038/s41559-018-0476-8
Publication status	Published - 1 Apr 2018

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology

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Zepeda Mendoza, M. L., Xiong, Z., Escalera-Zamudio, M., Runge, A. K., Thézé, J., Streicker, D., Frank, H. K., Loza-Rubio, E., Liu, S., Ryder, O. A., Samaniego Castruita, J. A., Katzourakis, A., Pacheco, G., Taboada, B., Löber, U., Pybus, O. G., Li, Y., Rojas-Anaya, E., Bohmann, K., ... Gilbert, M. P. T. (2018). Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nature Ecology and Evolution, 2(4), 659-668. https://doi.org/10.1038/s41559-018-0476-8

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title = "Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat",

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.",

author = "{Zepeda Mendoza}, {M. Lisandra} and Zijun Xiong and Marina Escalera-Zamudio and Runge, {Anne Kathrine} and Julien Th{\'e}z{\'e} and Daniel Streicker and Frank, {Hannah K.} and Elizabeth Loza-Rubio and Shengmao Liu and Ryder, {Oliver A.} and {Samaniego Castruita}, {Jose Alfredo} and Aris Katzourakis and George Pacheco and Blanca Taboada and Ulrike L{\"o}ber and Pybus, {Oliver G.} and Yang Li and Edith Rojas-Anaya and Kristine Bohmann and {Carmona Baez}, Aldo and Arias, {Carlos F.} and Shiping Liu and Greenwood, {Alex D.} and Bertelsen, {Mads F.} and White, {Nicole E.} and Michael Bunce and Guojie Zhang and Thomas Sicheritz-Pont{\'e}n and Gilbert, {M. P.Thomas}",

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doi = "10.1038/s41559-018-0476-8",

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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 and Evolution, vol. 2, no. 4, pp. 659-668. https://doi.org/10.1038/s41559-018-0476-8

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T1 - Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat

AU - Zepeda Mendoza, M. Lisandra

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

PY - 2018/4/1

Y1 - 2018/4/1

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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JO - Nature Ecology and Evolution

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

Abstract

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