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The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch

Michel, Alice J. and Ward, Lewis M. and Goffredi, Shana K. and Dawson, Katherine S. and Baldassarre, Daniel T. and Brenner, Alec and Gotanda, Kiyoko M. and McCormack, John E. and Mullin, Sean W. and O’Neill, Ariel and Tender, Gabrielle S. and Uy, J. Albert C. and Yu, Kristie and Orphan, Victoria J. and Chaves, Jaime A. (2018) The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome, 6 . Art. No. 167. ISSN 2049-2618. PMCID PMC6146768. http://resolver.caltech.edu/CaltechAUTHORS:20180919-102939169

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Abstract

Background: Darwin’s finches are a clade of 19 species of passerine birds native to the Galápagos Islands, whose biogeography, specialized beak morphologies, and dietary choices—ranging from seeds to blood—make them a classic example of adaptive radiation. While these iconic birds have been intensely studied, the composition of their gut microbiome and the factors influencing it, including host species, diet, and biogeography, has not yet been explored. Results: We characterized the microbial community associated with 12 species of Darwin’s finches using high-throughput 16S rRNA sequencing of fecal samples from 114 individuals across nine islands, including the unusual blood-feeding vampire finch (Geospiza septentrionalis) from Darwin and Wolf Islands. The phylum-level core gut microbiome for Darwin’s finches included the Firmicutes, Gammaproteobacteria, and Actinobacteria, with members of the Bacteroidetes at conspicuously low abundance. The gut microbiome was surprisingly well conserved across the diversity of finch species, with one exception—the vampire finch—which harbored bacteria that were either absent or extremely rare in other finches, including Fusobacterium, Cetobacterium, Ureaplasma, Mucispirillum, Campylobacter, and various members of the Clostridia—bacteria known from the guts of carnivorous birds and reptiles. Complementary stable isotope analysis of feathers revealed exceptionally high δ15N isotope values in the vampire finch, resembling top marine predators. The Galápagos archipelago is also known for extreme wet and dry seasons, and we observed a significant seasonal shift in the gut microbial community of five additional finch species sampled during both seasons. Conclusions: This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1186/s40168-018-0555-8DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146768PubMed CentralArticle
ORCID:
AuthorORCID
Ward, Lewis M.0000-0002-9290-2567
Dawson, Katherine S.0000-0001-8856-4609
Yu, Kristie0000-0001-6735-3968
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2018 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Received: 29 May 2018; Accepted: 5 September 2018; Published: 19 September 2018. We are grateful to Sofia Carvajal, Kurt Gielow, Sarah Knutie, Andres Leon, Simón Villamar, Angela Hansen, Sabrina McNew, Ashley Saulsberry, Carlos Vera, Ruben Heleno, Manuel Nogales, and Sandra Hervías for the invaluable assistance in the field; Alexis Pasulka, David Case, and Stephanie Connon for the assistance in lab and advice with the data analysis, as well as other members of the Caltech GE/Bi/ESE_246 molecular geobiology and Bi/GE_105 Evolution course including Rob Phillips, Courtney Chen, Anne Christian, Bianca Lepe, Kristin Anderson, Tristan Murphy, Matthew Smalley, and Tiffany Zhou; and to Parque Nacional Galápagos and Galápagos Science Center for their logistical support. All samples were collected under the Contrato Marco de Acceso a los Recursos Genéticos MAE-DNB-CM-2016-0041 and Galápagos National Park permit PC-0615. Funds were provided by GAIAS-USFQ Grant to JAC, the Gordon and Betty Moore Foundation through grant GMBF3780 to VJO, NSF-Postdoctoral Grant to DTB, Instrumental Crowdfunding, Le Fonds Québécois de la Recherche sur la Nature et les Technologies Postdoctoral Fellowship, a British Ornithologists’ Union Research Grant to KMG, and a NASA Earth and Space Science Fellowship to LMW. We also acknowledge support from Terence Barr and Caltech's Center for Environmental Microbial Interactions (CEMI). Availability of data and materials: Raw reads were deposited and are available through the Sequence Read Archive under accession number SRP130314. Authors’ contributions: AJM, LMW, SKG, and VJO analyzed the data and wrote the manuscript. KSD collected the stable isotope data and assisted with the interpretation. AJM, LMW, SKG, VJO, SM extracted DNA and prepared samples for sequencing. AB, JEM, SM, AO, GT, and KY helped analyze the data. DTB, KMG, ACU, and JAC collected fecal samples and observation data on finches on the Galápagos and assisted with the writing of the manuscript. All authors read and approved the final manuscript. Alice J. Michel and Lewis M. Ward contributed equally to this work. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. The authors declare that they have no competing interests.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funders:
Funding AgencyGrant Number
University San Francisco de QuitoUNSPECIFIED
Gordon and Betty Moore FoundationGMBF3780
NSF Postdoctoral FellowshipUNSPECIFIED
Instrumental CrowdfundingUNSPECIFIED
Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT)UNSPECIFIED
British Ornithologists’ UnionUNSPECIFIED
NASA Earth and Space Science FellowshipUNSPECIFIED
Terence BarrUNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Subject Keywords:Galápagos Islands; Darwin’s finches; Blood-feeding; Microbiome; Geospiza
PubMed Central ID:PMC6146768
Record Number:CaltechAUTHORS:20180919-102939169
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180919-102939169
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:89754
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:19 Sep 2018 17:57
Last Modified:20 Mar 2019 21:20

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