Skip to main content
SpringerLink
Log in
Book cover

Reproductive Sciences in Animal Conservation pp 225–240Cite as

Reproductive Microbiomes in Wild Animal Species: A New Dimension in Conservation Biology

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1200))

Abstract

Communities of microbes have coevolved in animal organisms and are found in almost every part of the body. Compositions of those communities (microbiota) as well as their genomes and genes (microbiomes) are critical for functional regulations of the body organ systems—the digestive or ‘gut’ microbiome being the most described so far. Based on extensive research in humans, microbiomes in the reproductive tract may play a role in reproductive functions and pregnancy. However, in wild animal species, those microbiomes have been poorly studied, and as a result, little is known about their involvement in fertility or parental/offspring health. This emerging research area is highly relevant to conservation biology from captive breeding management to successful reintroduction or maintenance of wild populations. The objective of this chapter is to review current knowledge about reproductive microbiomes in healthy wild animal species. While recognizing the current technical limits of microbial identification in all animal species, we also explore the link between microbial communities (within female or male reproductive systems) and fertility, from conception to birth outcome. In addition, it is critical to understanding how reproductive microbiomes are affected by environmental factors (including captivity, contact with other individuals, or changes in the ecosystem) to optimize conservation efforts. Thus, reproductive microbiomes represent a novel dimension in conservation biology that will likely gain importance in the future.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Alfano M, Ferrarese R, Locatelli I, et al. Testicular microbiome in azoospermic men-first evidence of the impact of an altered microenvironment. Hum Reprod. 2018;33:1212–7. https://doi.org/10.1093/humrep/dey116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altmäe S. Commentary: uterine microbiota: residents, tourists, or invaders? Front Immunol. 2018;9:1874.

    Article  Google Scholar 

  • Apprill A. Marine animal microbiomes: toward understanding host–microbiome interactions in a changing ocean. Front Mar Sci. 2017;4 https://doi.org/10.3389/fmars.2017.00222.

  • Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.

    Article  Google Scholar 

  • Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J. The microbiome of animals: implications for conservation biology. Int J Genomics. 2016;2016:1–7. https://doi.org/10.1155/2016/5304028.

    Article  CAS  Google Scholar 

  • Baker JM, Chase DM, Herbst-Kralovetz MM. Uterine microbiota: residents, tourists, or invaders? Front Immunol. 2018;9 https://doi.org/10.3389/fimmu.2018.00208.

  • Browne AS, Kelly CR. Fecal transplant in inflammatory bowel disease. Gastroenterol Clin N Am. 2017;46:825–37.

    Article  Google Scholar 

  • Campbell LJ, Hammond SA, Price SJ, Sharma MD, Garner TWJ, Birol I, Helbing CC, Wilfert L, Griffiths AGF. A novel approach to wildlife transcriptomics provides evidence of disease-mediated differential expression and changes to the microbiome of amphibian populations. Mol Ecol. 2018;27:1413–27.

    Article  CAS  Google Scholar 

  • Carneiro LC, Cronin JG, Sheldon IM. Mechanisms linking bacterial infections of the bovine endometrium to disease and infertility. Reprod Biol. 2016;16:1–7.

    Article  Google Scholar 

  • Chaban B, Links MG, Jayaprakash T, et al. Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle. Microbiome. 2014;2:23.

    Article  Google Scholar 

  • Chen C, Song X, Wei W, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017;8:875. https://doi.org/10.1038/s41467-017-00901-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Fox S, Pemberton D, Hogg C, Papenfuss AT, Belov K. The Tasmanian devil microbiome-implications for conservation and management. Microbiome. 2015;3:76.

    Article  Google Scholar 

  • Cicinelli E, De Ziegler D, Nicoletti R, Tinelli R, Saliani N, Resta L, Bellavia M, De Vito D. Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis. Gynecol Obstet Investig. 2009;68:108–15.

    Article  Google Scholar 

  • Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25:3776–800.

    Article  Google Scholar 

  • Davidson RM, Epperson LE. Microbiome sequencing methods for studying human diseases. Methods Mol Biol. 2018;1706:77–90.

    Article  CAS  Google Scholar 

  • DiGiulio DB, Callahan BJ, McMurdie PJ, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci. 2015;112:11060–5.

    Article  CAS  Google Scholar 

  • Fettweis JM, Serrano MG, Sheth NU, Mayer CM, Glascock AL, Brooks JP, Jefferson KK, Buck GA. Species-level classification of the vaginal microbiome. BMC Genomics. 2012;13(Suppl 8):S17.

    PubMed  PubMed Central  Google Scholar 

  • Franasiak JM, Werner MD, Juneau CR, Tao X, Landis J, Zhan Y, Treff NR, Scott RT. Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit. J Assist Reprod Genet. 2016;33:129–36.

    Article  CAS  Google Scholar 

  • Gajer P, Brotman RM, Bai G, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 2012;4:132ra52.

    Article  Google Scholar 

  • Garcia-Grau I, Simon C, Moreno I. Uterine microbiome—low biomass and high expectations. Biol Reprod. 2018; https://doi.org/10.1093/biolre/ioy257.

  • Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science. 2016;352:539–44.

    Article  CAS  Google Scholar 

  • Geuking MB, Köller Y, Rupp S, McCoy KD. The interplay between the gut microbiota and the immune system. Gut Microbes. 2014;5:411–8.

    Article  Google Scholar 

  • Goltsman DSA, Sun CL, Proctor DM, et al. Metagenomic analysis with strain-level resolution reveals fine-scale variation in the human pregnancy microbiome. bioRxiv. 2018; https://doi.org/10.1101/266700.

  • Gomez-Gallego C, Garcia-Mantrana I, Salminen S, Collado MC. The human milk microbiome and factors influencing its composition and activity. Semin Fetal Neonatal Med. 2016;21:400–5.

    Article  Google Scholar 

  • Grice EA, Segre JA. The human microbiome: our second genome. Annu Rev Genomics Hum Genet. 2012;13:151–70.

    Article  CAS  Google Scholar 

  • Hanning I, Diaz-Sanchez S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome. 2015;3:51.

    Article  Google Scholar 

  • Heil BA, Thompson SK, Kearns TA, Davolli GM, King G, Sones JL. Metagenetic characterization of the resident equine uterine microbiome using multiple techniques. J Equine Vet Sci. 2018;66:111.

    Article  Google Scholar 

  • Hird SM. Evolutionary biology needs wild microbiomes. Front Microbiol. 2017;8 https://doi.org/10.3389/fmicb.2017.00725.

  • Holt WVWV, Brown JLJL, Comizzoli P. Reproductive science as an essential component of conservation biology. Adv Exp Med Biol. 2014;753:3–14.

    Article  Google Scholar 

  • Hou D, Zhou X, Zhong X, Settles ML, Herring J, Wang L, Abdo Z, Forney LJ, Xu C. Microbiota of the seminal fluid from healthy and infertile men. Fertil Steril. 2013;100:1261–9.

    Article  Google Scholar 

  • Javurek AB, Spollen WG, Ali AMM, Johnson SA, Lubahn DB, Bivens NJ, Bromert KH, Ellersieck MR, Givan SA, Rosenfeld CS. Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status. Sci Rep. 2016;6 https://doi.org/10.1038/srep23027.

  • Jiménez RR, Sommer S. The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers Conserv. 2017;26:763–86.

    Article  Google Scholar 

  • Leblanc M, Causey R. Clinical and subclinical endometritis in the mare: both threats to fertility. Reprod Domest Anim. 2009;44:10–22.

    Article  Google Scholar 

  • Macpherson AJ, de Agüero MG, Ganal-Vonarburg SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017;17:508–17.

    Article  CAS  Google Scholar 

  • Mändar R. Microbiota of male genital tract: impact on the health of man and his partner. Pharmacol Res. 2013;69:32–41.

    Article  Google Scholar 

  • Mändar R, Punab M, Borovkova N, et al. Complementary seminovaginal microbiome in couples. Res Microbiol. 2015;166:440–7.

    Article  Google Scholar 

  • Marie A, Courchay M. Molecular characterization of the penile microbiome of Dorper rams (Ovis aries). Thesis presented in fulfilment of the requirements for the degree of masters in the Faculty of Science at Stellenbosch University; 2017.

    Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TCG, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A. 2013;110:3229–36.

    Article  CAS  Google Scholar 

  • Menke S, Meier M, Sommer S. Shifts in the gut microbiome observed in wildlife faecal samples exposed to natural weather conditions: lessons from time-series analyses using next-generation sequencing for application in field studies. Methods Ecol Evol. 2015;6:1080–7.

    Article  Google Scholar 

  • Merrifield DL, Rodiles A. The fish microbiome and its interactions with mucosal tissues. In: Peatman E, editor. Mucosal health in aquaculture. San Diego: Academic Press; 2015. p. 273–95.

    Chapter  Google Scholar 

  • Metcalf JL, Song SJ, Morton JT, et al. Evaluating the impact of domestication and captivity on the horse gut microbiome. Sci Rep. 2017;7:15497.

    Article  Google Scholar 

  • Miller EA, Livermore JA, Alberts SC, Tung J, Archie EA. Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons. Microbiome. 2017;5:8. https://doi.org/10.1186/s40168-017-0228-z.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moreno I, Codoñer FM, Vilella F, et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am J Obstet Gynecol. 2016;215:684–703. https://doi.org/10.1016/j.ajog.2016.09.075.

    Article  PubMed  Google Scholar 

  • Morimoto J, Simpson SJ, Ponton F. Direct and trans-generational effects of male and female gut microbiota in Drosophila melanogaster. Biol Lett. 2017;13:20160966. https://doi.org/10.1098/rsbl.2016.0966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuman H, Debelius JW, Knight R, Koren O. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev. 2015;39:509–21.

    Article  Google Scholar 

  • O’Callaghan TF, Ross RP, Stanton C, Clarke G. The gut microbiome as a virtual endocrine organ with implications for farm and domestic animal endocrinology. Domest Anim Endocrinol. 2016;56:S44–55.

    Article  Google Scholar 

  • Pamer EG. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science. 2016;352:535–8.

    Article  CAS  Google Scholar 

  • Pelzer E, Gomez-Arango LF, Barrett HL, Nitert MD. Review: maternal health and the placental microbiome. Placenta. 2017;54:30–7.

    Article  CAS  Google Scholar 

  • Power ML, Quaglieri C, Schulkin J. Reproductive microbiomes: a new thread in the microbial network. Reprod Sci. 2017;24:1482–92.

    Article  Google Scholar 

  • Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci. 2011;108:4680–7.

    Article  CAS  Google Scholar 

  • Redford KH, Segre JA, Salafsky N, Del Rio CM, Mcaloose D. Conservation and the microbiome. Conserv Biol. 2012;26:195–7.

    Article  Google Scholar 

  • Roggenbuck M, Schnell IB, Blom N, Bælum J, Bertelsen MF, Pontén TS, Sørensen SJ, Gilbert MTP, Graves GR, Hansen LH. The microbiome of new world vultures. Nat Commun. 2014; https://doi.org/10.1038/ncomms6498.

  • Schwartz MH, Wang H, Pan JN, Clark WC, Cui S. Microbiome characterization by high-throughput transfer RNA sequencing and modification analysis. Nat Commun. 2018;9:5353. https://doi.org/10.1038/s41467-018-07675-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirota I, Zarek SM, Segars JH. Potential influence of the microbiome on infertility and assisted reproductive technology. Semin Reprod Med. 2014;32:35–42.

    Article  Google Scholar 

  • Smith KE, Garza AL, Robinson C, Ashley RL, Ivey SL.WS Influence of sampling location and pregnancy on composition of the microbiome associated with the reproductive tract of the ewe. Journal of Animal Science, suppl. 2016 Supplement 5; 94: 498. https://doi.org/10.2527/jam2016-1039

    Article  Google Scholar 

  • Soares MC, Cable J, Lima-Maximino M, Maximino C, Xavier R. Using fish models for assessing the role of sociality on the microbiome: the next step for translational microbiome research? 2018; https://doi.org/10.20944/PREPRINTS201809.0387.V1.

  • Spear GT, Gilbert D, Sikaroodi M, Doyle L, Green L, Gillevet PM, Landay AL, Veazey RS. Identification of rhesus macaque genital microbiota by 16S pyrosequencing shows similarities to human bacterial vaginosis: implications for use as an animal model for HIV vaginal infection. AIDS Res Hum Retrovir. 2010;26:193–200.

    Article  CAS  Google Scholar 

  • Spear G, Rothaeulser K, Fritts L, Gillevet PM, Miller CJ. In captive rhesus macaques, cervicovaginal inflammation is common but not associated with the stable polymicrobial microbiome. PLoS One. 2012;7:e52992.

    Article  CAS  Google Scholar 

  • Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9:279–90.

    Article  CAS  Google Scholar 

  • Stumpf RM, Wilson BA, Rivera A, Yildirim S, Yeoman CJ, Polk JD, White BA, Leigh SR. The primate vaginal microbiome: comparative context and implications for human health and disease. Am J Phys Anthropol. 2013;152:119–34.

    Article  Google Scholar 

  • Stumpf RM, Gomez A, Amato KR, Yeoman CJ, Polk JD, Wilson BA, Nelson K, White BA, Leigh SR. Microbiomes, metagenomics, and primate conservation: new strategies, tools, and applications. Biol Conserv. 2016;199:56–66.

    Article  Google Scholar 

  • Theis KR, Romero R, Winters AD, et al. Does the human placenta delivered at term have a microbiota? Results of cultivation, quantitative real-time PCR, 16S rRNA gene sequencing, and metagenomics. Am J Obstet Gynecol. 2019;220:267.e1–267.e39.

    Article  Google Scholar 

  • 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;2015:1–18.

    Google Scholar 

  • Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized Gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.

    Article  Google Scholar 

  • Uchihashi M, Bergin IL, Bassis CM, Hashway SA, Chai D, Bell JD. Influence of age, reproductive cycling status, and menstruation on the vaginal microbiome in baboons (Papio anubis). Am J Primatol. 2015;77:563–78.

    Article  CAS  Google Scholar 

  • Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev. 2012;70:S38–44.

    Article  Google Scholar 

  • van Nood E, Dijkgraaf MGW, Keller JJ. Duodenal infusion of feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:2143–5.

    Article  Google Scholar 

  • van Veelen HPJ, Falcao Salles J, Tieleman BI. Multi-level comparisons of cloacal, skin, feather and nest-associated microbiota suggest considerable influence of horizontal acquisition on the microbiota assembly of sympatric woodlarks and skylarks. Microbiome. 2017;5:156.

    Article  Google Scholar 

  • Vital M, Harkema JR, Rizzo M, Tiedje J, Brandenberger C. Alterations of the murine gut microbiome with age and allergic airway disease. J Immunol Res. 2015;2015:1–8.

    Article  Google Scholar 

  • Wasimuddin MS, Melzheimer J, Thalwitzer S, Heinrich S, Wachter B, Sommer S. Gut microbiomes of free-ranging and captive Namibian cheetahs: diversity, putative functions and occurrence of potential pathogens. Mol Ecol. 2017;26:5515–27.

    Article  CAS  Google Scholar 

  • Williams CL, Ybarra AR, Meredith AN, Durrant BS, Tubbs CW. Gut microbiota and phytoestrogen-associated infertility in southern white rhinoceros. MBio. 2019;10 https://doi.org/10.1128/mBio.00311-19.

  • Yang X, Cheng G, Li C, et al. The normal vaginal and uterine bacterial microbiome in giant pandas (Ailuropoda melanoleuca). Microbiol Res. 2017;199:1–9.

    Article  Google Scholar 

  • Yildirim S, Yeoman CJ, Janga SC, Thomas SM, Ho M, Leigh SR, Consortium PM, White BA, Wilson BA, Stumpf RM. Primate vaginal microbiomes exhibit species specificity without universal lactobacillus dominance. ISME J. 2014;8:2431–44.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    Pierre Comizzoli & M. Power

Authors
  1. Pierre Comizzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Power
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre Comizzoli .

Editor information

Editors and Affiliations

  1. Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    Pierre Comizzoli

  2. Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA, USA

    Janine L. Brown

  3. Academic Unit of Reproductive and Developmental Medicine, The University of Sheffield, Sheffield, UK

    William V. Holt

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Comizzoli, P., Power, M. (2019). Reproductive Microbiomes in Wild Animal Species: A New Dimension in Conservation Biology. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_8

Download citation

Publish with us

Policies and ethics

Search

Navigation