Evaluating the impact of domestication and captivity on the horse gut microbiome.
- Comparative Study
- Journal Article
- Research Support
- Non-U.S. Gov't
- Research Support
- U.S. Gov't
- Non-P.H.S.
Summary
This research article studies how domestication and captivity affect the diversity and composition of bacteria in the gut of horses. The scientists found a more diverse bacterial community in wild horses compared to domesticated ones, and a drastically reduced variety in captive-born animals.
Effect of Domestication and Captivity on Gut Microbiome
The article investigates the impact of domestication and captivity, which can significantly alter a mammal’s diet and living conditions, on the biodiversity and composition of gut microbes in horses. The gut microbiome refers to the collection of microbes and their respective genes that reside in the gastrointestinal tract, acting as an additional genome. This “second genome” is crucial as it carries out vital functions for the host.
- The researchers used Przewalski’s horse (PH; Equus ferus przewalskii), the only existing horse species that humans have not successfully domesticated, and the common domestic horse (E. f. caballus) which live in neighboring natural grasslands, as their case study.
- The scientists performed a comparative study on the fecal microbiomes (indicators of gut microbiomes) of the two types of horses and discovered that the PH horse’s gut hosted a disparate and more diverse bacterial community compared to the domestic ones.
Role of Diet in Gut Microbiome Diversity
The researchers believe the difference in gut microbiome diversity may partly be due to different diets, which was indicated by the trnL marker data.
- The trnL marker is a tool used in studying plant diversity and diet. In the context of their research, the scientists used it to gauge the variety and types of plants in the horses’ diets.
- Due to their different living conditions, the wild and domesticated horses have varying diets. While wild horses predominantly eat grass, domestic horses are often provided manufactured feeds.
- These diet variations, the researchers suggest, may be responsible for the difference in gut microbiome composition and diversity between the wild and domesticated horses.
Impact of Captivity on Gut Microbiome Diversity
The research also found that captivity significantly affects gut microbiome diversity.
- Within the PH population, the research revealed a stark difference between those born free in natural reserves and those born in captivity in European zoos.
- The captive-born horses had remarkably less diverse gut microbes compared to those born in the wild. This may be due to the restricted diet and sedentary lifestyle in zoos compared to the diet variety and physical activity in nature.
- These findings reinforce the hypothesis that anthropogenic forces, such as captivity, can dramatically alter the gut microbiome of mammals.
Implications for Conservation Management
These results have significant implications for the conservation management of endangered mammals.
- If domestication and captivity can drastically change a mammal’s gut microbiome, then this could have serious consequences for their health and survival.
- Understanding these changes are vital for conservation management as it could help develop strategies that mitigate these effects and thus aid the preservation and propagation of endangered species.
Cite This Article
Publication
Researcher Affiliations
- Department of Animal Sciences, Colorado State University, Fort Collins, CO, USA.
- Department of Pediatrics, University of California San Diego, San Diego, CA, USA.
- Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA.
- Department of Pediatrics, University of California San Diego, San Diego, CA, USA.
- Department of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA.
- Department of Chemical and Biological Engineering, University of Colorado at Boulder, Boulder, CO 80309, Colorado, USA.
- National High-Throughput DNA Sequencing Center, University of Copenhagen, Øster Farimagsgade 2D entrance E, 1353 K, Copenhagen, Denmark.
- Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldade 5-7, 1350 K, Copenhagen, Denmark.
- Association pour le cheval de Przewalski: TAKH, Station biologique de la Tour du Valat, 13200, Arles, France.
- Association pour le cheval de Przewalski: TAKH, Station biologique de la Tour du Valat, 13200, Arles, France.
- Laboratoire d'Ecologie Alpine (LECA), Centre National de la Recherche Scientifique and Université Grenoble-Alpes, Grenoble, France.
- Laboratoire d'Ecologie Alpine (LECA), Centre National de la Recherche Scientifique and Université Grenoble-Alpes, Grenoble, France.
- Department of Pediatrics, University of California San Diego, San Diego, CA, USA.
- Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldade 5-7, 1350 K, Copenhagen, Denmark.
- Department of Pediatrics, University of California San Diego, San Diego, CA, USA.
- Department of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA.
- Center for Microbiome Innovation, University of California San Diego, La Jolla, California, USA.
- Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, USA.
- Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldade 5-7, 1350 K, Copenhagen, Denmark. ludovic.orlando@univ-tlse3.fr.
- Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse (AMIS), CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, 31000, Toulouse, France. ludovic.orlando@univ-tlse3.fr.
MeSH Terms
- Animals
- Animals, Wild / microbiology
- Domestication
- Feces / microbiology
- Female
- France
- Gastrointestinal Microbiome
- Horses / microbiology
- Livestock / microbiology
- Male
- Mongolia
Conflict of Interest Statement
References
- McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ. Animals in a bacterial world, a new imperative for the life sciences.. Proc Natl Acad Sci U S A 2013 Feb 26;110(9):3229-36.
- Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z, Wang B, Magris M, Hidalgo G, Contreras M, Noya-Alarcón Ó, Lander O, McDonald J, Cox M, Walter J, Oh PL, Ruiz JF, Rodriguez S, Shen N, Song SJ, Metcalf J, Knight R, Dantas G, Dominguez-Bello MG. The microbiome of uncontacted Amerindians.. Sci Adv 2015 Apr 3;1(3).
- Martínez I, Stegen JC, Maldonado-Gómez MX, Eren AM, Siba PM, Greenhill AR, Walter J. The gut microbiota of rural papua new guineans: composition, diversity patterns, and ecological processes.. Cell Rep 2015 Apr 28;11(4):527-38.
- Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, Zech Xu Z, Van Treuren W, Knight R, Gaffney PM, Spicer P, Lawson P, Marin-Reyes L, Trujillo-Villarroel O, Foster M, Guija-Poma E, Troncoso-Corzo L, Warinner C, Ozga AT, Lewis CM. Subsistence strategies in traditional societies distinguish gut microbiomes.. Nat Commun 2015 Mar 25;6:6505.
- Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, Turroni S, Biagi E, Peano C, Severgnini M, Fiori J, Gotti R, De Bellis G, Luiselli D, Brigidi P, Mabulla A, Marlowe F, Henry AG, Crittenden AN. Gut microbiome of the Hadza hunter-gatherers.. Nat Commun 2014 Apr 15;5:3654.
- Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI. Human gut microbiome viewed across age and geography.. Nature 2012 May 9;486(7402):222-7.
- Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity.. Nature 2006 Dec 21;444(7122):1022-3.
- Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, Kim SG, Li H, Gao Z, Mahana D, Zárate Rodriguez JG, Rogers AB, Robine N, Loke P, Blaser MJ. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences.. Cell 2014 Aug 14;158(4):705-721.
- Kamada N, Seo SU, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease.. Nat Rev Immunol 2013 May;13(5):321-35.
- Zeder MA. The Domestication of Animals. Journal of Anthropological Research 2012;68:161–190.
- Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI. Evolution of mammals and their gut microbes.. Science 2008 Jun 20;320(5883):1647-51.
- Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.. Science 2011 May 20;332(6032):970-4.
- Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R. Cohabiting family members share microbiota with one another and with their dogs.. Elife 2013 Apr 16;2:e00458.
- Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, Beaumont M, Van Treuren W, Knight R, Bell JT, Spector TD, Clark AG, Ley RE. Human genetics shape the gut microbiome.. Cell 2014 Nov 6;159(4):789-99.
- Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, Jónsson H, Bar-Gal GK, Albrechtsen A, Vieira FG, Petersen B, Ginolhac A, Seguin-Orlando A, Magnussen K, Fages A, Gamba C, Lorente-Galdos B, Polani S, Steiner C, Neuditschko M, Jagannathan V, Feh C, Greenblatt CL, Ludwig A, Abramson NI, Zimmermann W, Schafberg R, Tikhonov A, Sicheritz-Ponten T, Willerslev E, Marques-Bonet T, Ryder OA, McCue M, Rieder S, Leeb T, Slatkin M, Orlando L. Evolutionary Genomics and Conservation of the Endangered Przewalski's Horse.. Curr Biol 2015 Oct 5;25(19):2577-83.
- Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
- Volf J, Kus E, Prokopova L. General Studbook of the Przewalski Horse. (Zoological Garden Prague, 1991).
- Zimmermann W. International Przewalski’s Horse Studbook (Equus ferus przewalskii). ((Cologne Zoo), 2014).
- BENIRSCHKE K, MALOUF N, LOW RJ, HECK H. CHROMOSOME COMPLEMENT: DIFFERENCES BETWEEN EQUUS CABALLUS AND EQUUS PRZEWALSKII, POLIAKOFF.. Science 1965 Apr 16;148(3668):382-3.
- Hyde ER, Navas-Molina JA, Song SJ, Kueneman JG, Ackermann G, Cardona C, Humphrey G, Boyer D, Weaver T, Mendelson JR 3rd, McKenzie VJ, Gilbert JA, Knight R. The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat.. mSystems 2016 Jul-Aug;1(4).
- Reed KJ. Can fecal samples be used to inform about microbial communities of the equine hindgut?. Journal of Equine Veterinary Science 2017;52:52–53.
- Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding.. Nucleic Acids Res 2007;35(3):e14.
- Frese SA, Parker K, Calvert CC, Mills DA. Diet shapes the gut microbiome of pigs during nursing and weaning.. Microbiome 2015;3:28.
- Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer.. Nat Rev Microbiol 2014 Oct;12(10):661-72.
- Sabir SM, Maqsood H, Hayat I, Khan MQ, Khaliq A. Elemental and nutritional analysis of sea buckthorn (Hippophae rhamnoides ssp. turkestanica) Berries of Pakistani origin.. J Med Food 2005 Winter;8(4):518-22.
- Krejcarova J, Strakova E, Suchy P, Herzig I, Karaskova K. Sea buckthorn (Hippophae rhamnoides L.) as a potential source of nutraceutics and its therapeutic possibilities - a review. Acta Vet Brno 2015;84:257–268.
- S J. Forage plants of Mongolia. (Admon Press, 2003).
- Alam MS, Kaur G, Jabbar Z, Javed K, Athar M. Evaluation of antioxidant activity of Salix caprea flowers.. Phytother Res 2006 Jun;20(6):479-83.
- Sulaiman GH, Hussien NN, Marzoog TR, Awad HA. Phenolic content, antioxidant, antimicrobial and cytotoxic activities of ethanolic extract of salix alba. American Journal of Biochemistry and Biotechnology 2013;9:41–46.
- Joly F, Saïdi S, Begz T, Feh C. Key resource areas of an arid grazing system of the Mongolian Gobi. Mongolian Journal of Biological Sciences 2012;10:13–24.
- Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.. Proc Natl Acad Sci U S A 2010 Jun 29;107(26):11971-5.
- Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI, Mendez K, Knight R, Clemente JC. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer.. Nat Med 2016 Mar;22(3):250-3.
- Tung J, Barreiro LB, Burns MB, Grenier JC, Lynch J, Grieneisen LE, Altmann J, Alberts SC, Blekhman R, Archie EA. Social networks predict gut microbiome composition in wild baboons.. Elife 2015 Mar 16;4.
- McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, Alexiev A, Amato KR, Metcalf JL, Kowalewski M, Avenant NL, Link A, Di Fiore A, Seguin-Orlando A, Feh C, Orlando L, Mendelson JR, Sanders J, Knight R. The Effects of Captivity on the Mammalian Gut Microbiome.. Integr Comp Biol 2017 Oct 1;57(4):690-704.
- Henderson CR. Use of an Average Numerator Relationship Matrix for Multiple-Sire Joining. J Anim Sci 1988;66:1614–1621.
- Wagner Mackenzie B, Waite DW, Taylor MW. Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences.. Front Microbiol 2015;6:130.
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
- Bates ST, Ahrendt S, Bik HM, Bruns TD, Caporaso JG, Cole J, Dwan M, Fierer N, Gu D, Houston S, Knight R, Leff J, Lewis C, Maestre JP, McDonald D, Nilsson RH, Porras-Alfaro A, Robert V, Schoch C, Scott J, Taylor DL, Parfrey LW, Stajich JE. Meeting report: fungal its workshop (october 2012).. Stand Genomic Sci 2013 Apr 15;8(1):118-23.
- Valentini A, Miquel C, Nawaz MA, Bellemain E, Coissac E, Pompanon F, Gielly L, Cruaud C, Nascetti G, Wincker P, Swenson JE, Taberlet P. New perspectives in diet analysis based on DNA barcoding and parallel pyrosequencing: the trnL approach.. Mol Ecol Resour 2009 Jan;9(1):51-60.
- Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E. obitools: a unix-inspired software package for DNA metabarcoding.. Mol Ecol Resour 2016 Jan;16(1):176-82.
- Kanz C, Aldebert P, Althorpe N, Baker W, Baldwin A, Bates K, Browne P, van den Broek A, Castro M, Cochrane G, Duggan K, Eberhardt R, Faruque N, Gamble J, Diez FG, Harte N, Kulikova T, Lin Q, Lombard V, Lopez R, Mancuso R, McHale M, Nardone F, Silventoinen V, Sobhany S, Stoehr P, Tuli MA, Tzouvara K, Vaughan R, Wu D, Zhu W, Apweiler R. The EMBL Nucleotide Sequence Database.. Nucleic Acids Res 2005 Jan 1;33(Database issue):D29-33.
- Ficetola GF, Coissac E, Zundel S, Riaz T, Shehzad W, Bessière J, Taberlet P, Pompanon F. An in silico approach for the evaluation of DNA barcodes.. BMC Genomics 2010 Jul 16;11:434.
- R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2011).
- Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities.. Appl Environ Microbiol 2005 Dec;71(12):8228-35.
- Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data.. ISME J 2010 Jan;4(1):17-27.
- Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: a tool for visualizing high-throughput microbial community data.. Gigascience 2013 Nov 26;2(1):16.
- Pawlowsky-Glahn, V., Egozcue, J. J. & Tolosana-Delgado, R. In Codawork “11 (eds J. J. Egozcue, R. Tolosana-Delgado & M. I. Ortego) (Girona, Spain, 2011).
- Morton JT, Sanders J, Quinn RA, McDonald D, Gonzalez A, Vázquez-Baeza Y, Navas-Molina JA, Song SJ, Metcalf JL, Hyde ER, Lladser M, Dorrestein PC, Knight R. Balance Trees Reveal Microbial Niche Differentiation.. mSystems 2017 Jan-Feb;2(1).
- Aitchison J. The Statistical Analysis of Compositional Data. Journal of the Royal Statistical Society. Series B (Methodological) 1982;44:139–177.
- Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R, Peddada SD. Analysis of composition of microbiomes: a novel method for studying microbial composition.. Microb Ecol Health Dis 2015;26:27663.
- Song SJ, Amir A, Metcalf JL, Amato KR, Xu ZZ, Humphrey G, Knight R. Preservation Methods Differ in Fecal Microbiome Stability, Affecting Suitability for Field Studies.. mSystems 2016 May-Jun;1(3).