Skip to main content

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home
  • Log in
  • My Cart

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
Research Article

Symbiotic bacteria appear to mediate hyena social odors

Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, and Thomas M. Schmidt
  1. Departments of aMicrobiology and Molecular Genetics and
  2. cZoology and
  3. bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824

See allHide authors and affiliations

PNAS December 3, 2013 110 (49) 19832-19837; https://doi.org/10.1073/pnas.1306477110
Kevin R. Theis
Departments of aMicrobiology and Molecular Genetics and
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: theiskev@msu.edu
Arvind Venkataraman
Departments of aMicrobiology and Molecular Genetics and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jacquelyn A. Dycus
Departments of aMicrobiology and Molecular Genetics and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Keith D. Koonter
Departments of aMicrobiology and Molecular Genetics and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Emily N. Schmitt-Matzen
Departments of aMicrobiology and Molecular Genetics and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Aaron P. Wagner
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kay E. Holekamp
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
cZoology and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Thomas M. Schmidt
Departments of aMicrobiology and Molecular Genetics and
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  1. Edited by E. Peter Greenberg, University of Washington, Seattle, WA, and approved October 15, 2013 (received for review April 6, 2013)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Online Impact

 

Article Information

vol. 110 no. 49 19832-19837
DOI: 
https://doi.org/10.1073/pnas.1306477110
PubMed: 
24218592

Published By: 
National Academy of Sciences
Print ISSN: 
0027-8424
Online ISSN: 
1091-6490
History: 
  • Published in issue December 3, 2013.
  • Published first November 11, 2013.


Author Information

  1. Kevin R. Theisa,b,1,
  2. Arvind Venkataramana,
  3. Jacquelyn A. Dycusa,
  4. Keith D. Koontera,
  5. Emily N. Schmitt-Matzena,
  6. Aaron P. Wagnerb,
  7. Kay E. Holekampb,c,2, and
  8. Thomas M. Schmidta,b,2
  1. Departments of aMicrobiology and Molecular Genetics and
  2. cZoology and
  3. bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
  1. Edited by E. Peter Greenberg, University of Washington, Seattle, WA, and approved October 15, 2013 (received for review April 6, 2013)

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: theiskev{at}msu.edu.
  • ↵2K.E.H. and T.M.S. contributed equally to this work.

  • Author contributions: K.R.T., A.V., K.E.H., and T.M.S. designed research; K.R.T., A.V., J.A.D., K.D.K., E.N.S.-M., and A.P.W. performed research; K.R.T., A.V., and J.A.D. analyzed data; and K.R.T., A.V., J.A.D., A.P.W., K.E.H., and T.M.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KC705471–KC706325).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306477110/-/DCSupplemental.

Cited By...

  • 106 Citations
  • 117 Citations
  • Google Scholar

This article has been cited by the following articles in journals that are participating in Crossref Cited-by Linking.

  • Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes
    Seth R. Bordenstein, Kevin R. Theis, Matthew K. Waldor
    PLOS Biology 2015 13 8
  • Control of Brain Development, Function, and Behavior by the Microbiome
    Timothy R. Sampson, Sarkis K. Mazmanian
    Cell Host & Microbe 2015 17 5
  • The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis?
    Roman M. Stilling, Marcel van de Wouw, Gerard Clarke, Catherine Stanton, Timothy G. Dinan, John F. Cryan
    Neurochemistry International 2016 99
  • The Microbiome and Host Behavior
    Helen E. Vuong, Jessica M. Yano, Thomas C. Fung, Elaine Y. Hsiao
    Annual Review of Neuroscience 2017 40 1
  • Microbial endocrinology: the interplay between the microbiota and the endocrine system
    Hadar Neuman, Justine W. Debelius, Rob Knight, Omry Koren, Ehud Banin
    FEMS Microbiology Reviews 2015 39 4
  • Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents
    Scott F. Gilbert, Thomas C. G. Bosch, Cristina Ledón-Rettig
    Nature Reviews Genetics 2015 16 10
  • The pathogenBatrachochytrium dendrobatidisdisturbs the frog skin microbiome during a natural epidemic and experimental infection
    Andrea J. Jani, Cheryl J. Briggs
    Proceedings of the National Academy of Sciences 2014 111 47
  • Speciation by Symbiosis: the Microbiome and Behavior
    J. Dylan Shropshire, Seth R. Bordenstein
    mBio 2016 7 2
  • The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective
    Sofia Cussotto, Kiran V. Sandhu, Timothy G. Dinan, John F. Cryan
    Frontiers in Neuroendocrinology 2018 51
  • Social behavior and the microbiome
    Elizabeth A Archie, Jenny Tung
    Current Opinion in Behavioral Sciences 2015 6
  • Microbes and animal olfactory communication: Where do we go from here?
    Vanessa O. Ezenwa, Allison E. Williams
    BioEssays 2014 36 9
  • Microbiota and the social brain
    Eoin Sherwin, Seth R. Bordenstein, John L. Quinn, Timothy G. Dinan, John F. Cryan
    Science 2019 366 6465
  • Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership
    S. Leclaire, J. F. Nielsen, C. M. Drea
    Behavioral Ecology 2014 25 4
  • The raison d'être of chemical ecology
    Robert A. Raguso, Anurag A. Agrawal, Angela E. Douglas, Georg Jander, André Kessler, Katja Poveda, Jennifer S. Thaler
    Ecology 2015 96 3
  • A place for host–microbe symbiosis in the comparative physiologist's toolbox
    Kevin D. Kohl, Hannah V. Carey
    The Journal of Experimental Biology 2016 219 22
  • Microbiomes of Streptophyte Algae and Bryophytes Suggest That a Functional Suite of Microbiota Fostered Plant Colonization of Land
    J. J. Knack, L. W. Wilcox, P.-M. Delaux, J.-M. Ané, M. J. Piotrowski, M. E. Cook, J. M. Graham, L. E. Graham
    International Journal of Plant Sciences 2015 176 5
  • Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals
    Martin A. Stoffel, Barbara A. Caspers, Jaume Forcada, Athina Giannakara, Markus Baier, Luke Eberhart-Phillips, Caroline Müller, Joseph I. Hoffman
    Proceedings of the National Academy of Sciences 2015 112 36
  • Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice
    Roman M Stilling, Gerard M Moloney, Feargal J Ryan, Alan E Hoban, Thomaz FS Bastiaanssen, Fergus Shanahan, Gerard Clarke, Marcus J Claesson, Timothy G Dinan, John F Cryan
    eLife 2018 7
  • Rethinking “mutualism” in diverse host-symbiont communities
    Alexandra A. Mushegian, Dieter Ebert
    BioEssays 2016 38 1
  • A Volatile Relationship: Profiling an Inter-Kingdom Dialogue Between two Plant Pathogens, Ralstonia Solanacearum and Aspergillus Flavus
    Joseph E. Spraker, Kelsea Jewell, Ludmila V. Roze, Jacob Scherf, Dora Ndagano, Randolph Beaudry, John E. Linz, Caitilyn Allen, Nancy P. Keller
    Journal of Chemical Ecology 2014 40 5
  • Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors
    Douglas S. Pearce, Brian A. Hoover, Sarah Jennings, Gabrielle A. Nevitt, Kathryn M. Docherty
    Microbiome 2017 5 1
  • Social odours covary with bacterial community in the anal secretions of wild meerkats
    Sarah Leclaire, Staffan Jacob, Lydia K. Greene, George R. Dubay, Christine M. Drea
    Scientific Reports 2017 7 1
  • Brains, brawn and sociality: a hyaena's tale
    Kay E. Holekamp, Ben Dantzer, Gregory Stricker, Kathryn C. Shaw Yoshida, Sarah Benson-Amram
    Animal Behaviour 2015 103
  • An integrative omics perspective for the analysis of chemical signals in ecological interactions
    A. E. Brunetti, F. Carnevale Neto, M. C. Vera, C. Taboada, D. P. Pavarini, A. Bauermeister, N. P. Lopes
    Chemical Society Reviews 2018 47 5
  • The ecosystem services of animal microbiomes
    E. A. McKenney, K. Koelle, R. R. Dunn, A. D. Yoder
    Molecular Ecology 2018 27 8
  • Links between Natural Variation in the Microbiome and Host Fitness in Wild Mammals
    Taichi A. Suzuki
    Integrative and Comparative Biology 2017 57 4
  • The Extended Genotype: Microbially Mediated Olfactory Communication
    Alexandra J.R. Carthey, Michael R. Gillings, Daniel T. Blumstein
    Trends in Ecology & Evolution 2018 33 11
  • Whole gut microbiome composition of damselfish and cardinalfish before and after reef settlement
    Darren J. Parris, Rohan M. Brooker, Michael A. Morgan, Danielle L. Dixson, Frank J. Stewart
    PeerJ 2016 4
  • Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer ): In search of the role of immunity in the evolution of sociality
    Aura Raulo, Lasse Ruokolainen, Avery Lane, Katherine Amato, Rob Knight, Steven Leigh, Rebecca Stumpf, Bryan White, Karen E. Nelson, Andrea L. Baden, Stacey R. Tecot, Audrey Dussutour
    Journal of Animal Ecology 2018 87 2
  • Baby on board: olfactory cues indicate pregnancy and fetal sex in a non-human primate
    Jeremy Chase Crawford, Christine M. Drea
    Biology Letters 2015 11 2
  • Communication about social status
    Russell D Fernald
    Current Opinion in Neurobiology 2014 28
  • Reciprocal Interactions Between Gut Microbiota and Host Social Behavior
    Emmanuelle Münger, Augusto J. Montiel-Castro, Wolfgang Langhans, Gustavo Pacheco-López
    Frontiers in Integrative Neuroscience 2018 12
  • Searching for the gut microbial contributing factors to social behavior in rodent models of autism spectrum disorder
    Brittany D. Needham, Weiyi Tang, Wei-Li Wu
    Developmental Neurobiology 2018 78 5
  • Longitudinal Monitoring of Biofilm Formation via Robust Surface-Enhanced Raman Scattering Quantification of Pseudomonas aeruginosa-Produced Metabolites
    Cuong Quoc Nguyen, William John Thrift, Arunima Bhattacharjee, Saba Ranjbar, Tara Gallagher, Mahsa Darvishzadeh-Varcheie, Robert Noboru Sanderson, Filippo Capolino, Katrine Whiteson, Pierre Baldi, Allon I. Hochbaum, Regina Ragan
    ACS Applied Materials & Interfaces 2018 10 15
  • Commensal Bacteria Aid Mate-selection in the Fruit Fly, Bactrocera dorsalis
    Kamala Jayanthi Pagadala Damodaram, Arthikirubha Ayyasamy, Vivek Kempraj
    Microbial Ecology 2016 72 3
  • The musk chemical composition and microbiota of Chinese forest musk deer males
    Diyan Li, Binlong Chen, Long Zhang, Uma Gaur, Tianyuan Ma, Hang Jie, Guijun Zhao, Nan Wu, Zhongxian Xu, Huailiang Xu, Yongfang Yao, Ting Lian, Xiaolan Fan, Deying Yang, Mingyao Yang, Qing Zhu, Jessica Satkoski Trask
    Scientific Reports 2016 6 1
  • Coordinated change at the colony level in fruit bat fur microbiomes through time
    Oren Kolodny, Maya Weinberg, Leah Reshef, Lee Harten, Abraham Hefetz, Uri Gophna, Marcus W. Feldman, Yossi Yovel
    Nature Ecology & Evolution 2019 3 1
  • Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus)
    Andy Dosmann, Nassim Bahet, Deborah M. Gordon
    PeerJ 2016 4
  • The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation
    Melissah Rowe, Liisa Veerus, Pål Trosvik, Angus Buckling, Tommaso Pizzari
    Trends in Ecology & Evolution 2020 35 3
  • Histological, chemical and behavioural evidence of pedal communication in brown bears
    Agnieszka Sergiel, Javier Naves, Piotr Kujawski, Robert Maślak, Ewa Serwa, Damián Ramos, Alberto Fernández-Gil, Eloy Revilla, Tomasz Zwijacz-Kozica, Filip Zięba, Johanna Painer, Nuria Selva
    Scientific Reports 2017 7 1
  • Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs
    Lydia K. Greene, Kathleen E. Grogan, Kendra N. Smyth, Christine A. Adams, Skylar A. Klager, Christine M. Drea
    Royal Society Open Science 2016 3 4
  • Social Environment Has a Primary Influence on the Microbial and Odor Profiles of a Chemically Signaling Songbird
    Danielle J. Whittaker, Nicole M. Gerlach, Samuel P. Slowinski, Kyle P. Corcoran, Andrew D. Winters, Helena A. Soini, Milos V. Novotny, Ellen D. Ketterson, Kevin R. Theis
    Frontiers in Ecology and Evolution 2016 4
  • Symbiotic skin bacteria as a source for sex-specific scents in frogs
    Andrés E. Brunetti, Mariana L. Lyra, Weilan G. P. Melo, Laura E. Andrade, Pablo Palacios-Rodríguez, Bárbara M. Prado, Célio F. B. Haddad, Mônica T. Pupo, Norberto P. Lopes
    Proceedings of the National Academy of Sciences 2019 116 6
  • Animal–microbe interactions and the evolution of nervous systems
    Heather L. Eisthen, Kevin R. Theis
    Philosophical Transactions of the Royal Society B: Biological Sciences 2016 371 1685
  • Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory
    Eric Bapteste, Philippe Huneman
    BMC Biology 2018 16 1
  • Different methods for volatile sampling in mammals
    Marlen Kücklich, Manfred Möller, Andrea Marcillo, Almuth Einspanier, Brigitte M. Weiß, Claudia Birkemeyer, Anja Widdig, Walter Leal
    PLOS ONE 2017 12 8
  • Disruptive physiology: olfaction and the microbiome-gut-brain axis
    John Bienenstock, Wolfgang A. Kunze, Paul Forsythe
    Biological Reviews 2018 93 1
  • Female Chemical Signalling Underlying Reproduction in Mammals
    Holly A. Coombes, Paula Stockley, Jane L. Hurst
    Journal of Chemical Ecology 2018 44 9
  • The evolution of intelligence in mammalian carnivores
    Kay E. Holekamp, Sarah Benson-Amram
    Interface Focus 2017 7 3
  • An Introductory “How-to” Guide for Incorporating Microbiome Research into Integrative and Comparative Biology
    Kevin D. Kohl
    Integrative and Comparative Biology 2017 57 4
  • Olfactory Communication via Microbiota: What Is Known in Birds?
    Öncü Maraci, Kathrin Engel, Barbara A. Caspers
    Genes 2018 9 8
  • Individual- and Species-Specific Skin Microbiomes in Three Different Estrildid Finch Species Revealed by 16S Amplicon Sequencing
    Kathrin Engel, Jan Sauer, Sebastian Jünemann, Anika Winkler, Daniel Wibberg, Jörn Kalinowski, Andreas Tauch, Barbara A. Caspers
    Microbial Ecology 2018 76 2
  • The microbiome of the ant-built home: the microbial communities of a tropical arboreal ant and its nest
    Jane Lucas, Brian Bill, Bradley Stevenson, Michael Kaspari
    Ecosphere 2017 8 2
  • Evolution on the bright side of life: microorganisms and the evolution of mutualism
    Kristina Linnea Hillesland
    Annals of the New York Academy of Sciences 2018 1422 1
  • Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality
    Stefanie Grosser, Jan Sauer, Anneke J. Paijmans, Barbara A. Caspers, Jaume Forcada, Jochen B. W. Wolf, Joseph I. Hoffman
    Molecular Ecology 2019 28 9
  • The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs
    Lydia K. Greene, Sally L. Bornbusch, Erin A. McKenney, Rachel L. Harris, Sarah R. Gorvetzian, Anne D. Yoder, Christine M. Drea
    American Journal of Primatology 2019 81 10-11
  • E. Tobias Krause, Hans-Joachim Bischof, Kathrin Engel, Sarah Golüke, Öncü Maraci, Uwe Mayer, Jan Sauer, Barbara A. Caspers
    2018 50
  • Chemical Signals in Vertebrates 13
    Danielle J. Whittaker, Kevin R. Theis
    2016
  • Exploring Interactions between the Gut Microbiota and Social Behavior through Nutrition
    Cristian Pasquaretta, Tamara Gómez-Moracho, Philipp Heeb, Mathieu Lihoreau
    Genes 2018 9 11
  • Bacteria evoke alarm behaviour in zebrafish
    Joanne Shu Ming Chia, Elena S. Wall, Caroline Lei Wee, Thomas A. J. Rowland, Ruey-Kuang Cheng, Kathleen Cheow, Karen Guillemin, Suresh Jesuthasan
    Nature Communications 2019 10 1
  • Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication
    Christine M. Drea
    Philosophical Transactions of the Royal Society B: Biological Sciences 2020 375 1800
  • Evolving Ecosystems: Inheritance and Selection in the Light of the Microbiome
    Santiago Sandoval-Motta, Maximino Aldana, Alejandro Frank
    Archives of Medical Research 2017 48 8
  • Experimental evidence that symbiotic bacteria produce chemical cues in a songbird
    Danielle J. Whittaker, Samuel P. Slowinski, Jonathan M. Greenberg, Osama Alian, Andrew D. Winters, Madison M. Ahmad, Mikayla J. E. Burrell, Helena A. Soini, Milos V. Novotny, Ellen D. Ketterson, Kevin R. Theis
    The Journal of Experimental Biology 2019 222 20
  • Experimentally broken faecal sacs affect nest bacterial environment, development and survival of spotless starling nestlings
    Manuel Azcárate‐García, Magdalena Ruiz‐Rodríguez, Silvia Díaz‐Lora, Cristina Ruiz‐Castellano, Juan José Soler
    Journal of Avian Biology 2019 50 3
  • The Quest for a Universal Theory of Life
    Carol E. Cleland
    2019
  • Association with a sea anemone alters the skin microbiome of clownfish
    Zoe A. Pratte, Nastassia V. Patin, Mary E. McWhirt, Alicia M. Caughman, Darren J. Parris, Frank J. Stewart
    Coral Reefs 2018 37 4
  • A Risky Business? Habitat and Social Behavior Impact Skin and Gut Microbiomes in Caribbean Cleaning Gobies
    Raquel Xavier, Renata Mazzei, Marcos Pérez-Losada, Daniela Rosado, Joana L. Santos, Ana Veríssimo, Marta C. Soares
    Frontiers in Microbiology 2019 10
  • Body site-specific microbiota reflect sex and age-class among wild spotted hyenas
    Connie A Rojas, Kay E Holekamp, Andrew D Winters, Kevin R Theis
    FEMS Microbiology Ecology 2020 96 2
  • Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques
    Brigitte M. Weiß, Marlen Kücklich, Ruth Thomsen, Stefanie Henkel, Susann Jänig, Lars Kulik, Claudia Birkemeyer, Anja Widdig
    Behavioral Ecology and Sociobiology 2018 72 4
  • Conserving the holobiont
    Alexandra J. R. Carthey, Daniel T. Blumstein, Rachael V. Gallagher, Sasha G. Tetu, Michael R. Gillings, Alison Bennett
    Functional Ecology 2020 34 4
  • Normalizing Gas-Chromatography-Mass Spectrometry Data: Method Choice can Alter Biological Inference
    Michael J. Noonan, Helga V. Tinnesand, Christina D. Buesching
    BioEssays 2018 40 6
  • The role of the microbiome in the neurobiology of social behaviour
    Amar Sarkar, Siobhán Harty, Katerina V.‐A. Johnson, Andrew H. Moeller, Rachel N. Carmody, Soili M. Lehto, Susan E. Erdman, Robin I. M. Dunbar, Philip W. J. Burnet
    Biological Reviews 2020 95 5
  • Carrion Ecology, Evolution, and Their Applications
    M Benbow, Jennifer Pechal, Rachel Mohr
    2015
  • Chemical Signals in Vertebrates 13
    Christina D. Buesching, H. Veronica Tinnesand, YungWa Sin, Frank Rosell, Terry Burke, David W. Macdonald
    2016
  • Sexual responses of male rats to odours from female rats in oestrus are not affected by female germ-free status
    Birte L. Nielsen, Nathalie Jérôme, Audrey Saint-Albin, Fatima Joly, Sylvie Rabot, Nicolas Meunier
    Behavioural Brain Research 2019 359
  • Chemical Signals in Vertebrates 13
    Kevin R. Theis, Arvind Venkataraman, Aaron P. Wagner, Kay E. Holekamp, Thomas M. Schmidt
    2016
  • Cooperation and Conflict Within the Microbiota and Their Effects On Animal Hosts
    Alexandre R. T. Figueiredo, Jos Kramer
    Frontiers in Ecology and Evolution 2020 8
  • Genetic variation at MHC class II loci influences both olfactory signals and scent discrimination in ring-tailed lemurs
    Kathleen E. Grogan, Rachel L. Harris, Marylène Boulet, Christine M. Drea
    BMC Evolutionary Biology 2019 19 1
  • Mammalian watchdog targets bacteria
    Parag Kundu, Sven Pettersson
    Nature 2014 512 7515
  • Microbes take charge
    Amber Dance
    Proceedings of the National Academy of Sciences 2014 111 6
  • Microbiota Changes in the Musk Gland of Male Forest Musk Deer During Musk Maturation
    Yimeng Li, Tianxiang Zhang, Lei Qi, Shuang Yang, Shanghua Xu, Muha Cha, Meishan Zhang, Zhixin Huang, Juan Yu, Defu Hu, Shuqiang Liu
    Frontiers in Microbiology 2018 9
  • Microbiota composition of the dorsal patch of reproductive male Leptonycteris yerbabuenae
    Osiris Gaona, Daniel Cerqueda-García, Luisa I. Falcón, Guillermo Vázquez-Domínguez, Patricia M. Valdespino-Castillo, Carla-Ximena Neri-Barrios, Brenda A Wilson
    PLOS ONE 2019 14 12
  • Characterization of toll-like receptors 1–10 in spotted hyenas
    Andrew S. Flies, Matthew T. Maksimoski, Linda S. Mansfield, Mary L. Weldele, Kay E. Holekamp
    Veterinary Research Communications 2014 38 2
  • Chemical Signals in Vertebrates 13
    Thomas E. Goodwin, Innocent H. Harelimana, Laura J. MacDonald, Daniel B. Mark, Aline Umuhire Juru, Qin Yin, James A. Engman, Randall A. Kopper, Cheryl F. Lichti, Samuel G. Mackintosh, James D. Shoemaker, Mark V. Sutherland, Alan J. Tackett, Bruce A. Schulte
    2016
  • Chemical characterisation of potential pheromones from the shoulder gland of the Northern yellow-shouldered-bat, Sturnira parvidens (Phyllostomidae: Stenodermatinae)
    Chris G. Faulkes, J. Stephen Elmore, David A. Baines, Brock Fenton, Nancy B. Simmons, Elizabeth L. Clare
    PeerJ 2019 7
  • Chemical profiles reflect heterozygosity and seasonality in a tropical lekking passerine bird
    Danielle J. Whittaker, Meredith Kuzel, Mikayla J.E. Burrell, Helena A. Soini, Milos V. Novotny, Emily H. DuVal
    Animal Behaviour 2019 151
  • Leveraging non-human primates for exploring the social transmission of microbes
    Sahana Kuthyar, Melissa B Manus, Katherine R Amato
    Current Opinion in Microbiology 2019 50
  • Pregnancy is detected via odour in a wild cooperative breeder
    J. Mitchell, M. A. Cant, H. J. Nichols
    Biology Letters 2017 13 11
  • Using fish models to investigate the links between microbiome and social behaviour: The next step for translational microbiome research?
    Marta C. Soares, Jo Cable, Monica G. Lima‐Maximino, Caio Maximino, Raquel Xavier
    Fish and Fisheries 2019
  • Why Evolve Reliance on the Microbiome for Timing of Ontogeny?
    C. Jessica E. Metcalf, Lucas P. Henry, María Rebolleda-Gómez, Britt Koskella, Stephen Stearns, David S. Guttman
    mBio 2019 10 5
  • Bacteria isolated from Bengal cat (Felis catus × Prionailurus bengalensis) anal sac secretions produce volatile compounds potentially associated with animal signaling
    Mei S. Yamaguchi, Holly H. Ganz, Adrienne W. Cho, Thant H. Zaw, Guillaume Jospin, Mitchell M. McCartney, Cristina E. Davis, Jonathan A. Eisen, David A. Coil, Marcos Egea-Cortines
    PLOS ONE 2019 14 9
  • Chemical Signals in Vertebrates 14
    Chris Newman, Christina D. Buesching
    2019
  • Comparative chemical analysis of body odor in great apes
    Susann Jänig, Brigitte M. Weiß, Claudia Birkemeyer, Anja Widdig
    American Journal of Primatology 2019
  • Hologenomics: Systems-Level Host Biology
    Kevin R. Theis
    mSystems 2018 3 2
  • Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes
    Eva C. Wikberg, Diana Christie, Pascale Sicotte, Nelson Ting
    Animal Behaviour 2020 163
  • Sociality: The Behaviour of Group-Living Animals
    Ashley Ward, Mike Webster
    2016
  • Vaginal microbiome analysis of buffalo (Bubalus bubalis) during estrous cycle using high-throughput amplicon sequence of 16S rRNA gene
    Srinivasan Mahalingam, Dhanasekaran Dharumadurai, Govindaraju Archunan
    Symbiosis 2019 78 1
  • Bacterial Volatile Compounds: Functions in Communication, Cooperation, and Competition
    Tina Netzker, Evan M.F. Shepherdson, Matthew P. Zambri, Marie A. Elliot
    Annual Review of Microbiology 2020 74 1
  • Chemical cues of female fertility states in a non-human primate
    Marlen Kücklich, Brigitte M. Weiß, Claudia Birkemeyer, Almuth Einspanier, Anja Widdig
    Scientific Reports 2019 9 1
  • Fecal microbiota transplantation provides new insight into wildlife conservation
    Wei Guo, Ke Ren, Ruihong Ning, Caiwu Li, Hemin Zhang, Desheng Li, Lin Xu, Fenghui Sun, Min Dai
    Global Ecology and Conservation 2020 24
  • Gut microbiota in a host–brood parasite system: insights from common cuckoos raised by two warbler species
    Lucie Schmiedová, Jakub Kreisinger, Milica Požgayová, Marcel Honza, Jean-François Martin, Petr Procházka
    FEMS Microbiology Ecology 2020 96 9
  • The Connections Between Ecology and Infectious Disease
    M. Eric Benbow, Jennifer L. Pechal, Jeffery K. Tomberlin, Heather R. Jordan
    2018 5
  • Unclear Intentions: Eavesdropping in Microbial and Plant Systems
    María Rebolleda-Gómez, Corlett Wolfe Wood
    Frontiers in Ecology and Evolution 2019 7
  • Skin bacterial microflora of two closely related mountain newts (Salamandridae) – the Yellow‐spotted mountain newt Neurergus derjugini and the Kaiser's mountain newt Neurergus kaiseri – in the wild and in a breeding facility highlight new conservation perspectives
    S. Vaissi, M. Sharifi, A. Hernandez, S. Nikpey, M. Taran
    International Zoo Yearbook 2019 53 1
  • Autoclaving Nest-Material Remains Influences the Probability of Ectoparasitism of Nestling Hoopoes (Upupa epops)
    Mónica Mazorra-Alonso, Manuel Martín-Vivaldi, Juan Manuel Peralta-Sánchez, Juan José Soler
    Biology 2020 9 10
  • Burying Beetle Parents Adaptively Manipulate Information Broadcast from a Microbial Community
    Stephen T. Trumbo, Paula K. B. Philbrick, Johannes Stökl, Sandra Steiger
    The American Naturalist 2021 197 3
  • Microbial Transmission
    Chloé Vigliotti, Cédric Bicep, Eric Bapteste, Philippe Lopez, Eduardo Corel
    2019
  • Microbiomes
    Eugene Rosenberg
    2021 2
  • Microbiomes of Soils, Plants and Animals
    Anne Lizé, Zenobia Lewis
    2020
  • Neurological and cognitive significance of probiotics: a holy grail deciding individual personality
    Muhammad Afzal, Sayyeda Farwa Mazhar, Sadia Sana, Muhammad Naeem, Muhammad Hidayat Rasool, Muhammad Saqalein, Muhammad Atif Nisar, Maria Rasool, Muhammad Bilal, Abdul Arif Khan, Mohsin Khurshid
    Future Microbiology 2020 15 11
  • Significance of cervico-vaginal microbes in bovine reproduction and pheromone production – A hypothetical review
    M. Srinivasan, M. Adnane, G. Archunan
    Research in Veterinary Science 2021 135
  • Smelly microbes help hyenas to communicate
    Brian Owens
    Nature 2013
  • Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species
    Wenliang Zhou, Dunwu Qi, Ronald R. Swaisgood, Le Wang, Yipeng Jin, Qi Wu, Fuwen Wei, Yonggang Nie
    The ISME Journal 2021
  • Testing the “(Neo-)Darwinian” Principles against Reticulate Evolution: How Variation, Adaptation, Heredity and Fitness, Constraints and Affordances, Speciation, and Extinction Surpass Organisms and Species
    Nathalie Gontier
    Information 2020 11 7
  • Whose trait is it anyways? Coevolution of joint phenotypes and genetic architecture in mutualisms
    Anna M. O’Brien, Chandra N. Jack, Maren L. Friesen, Megan E. Frederickson
    Proceedings of the Royal Society B: Biological Sciences 2021 288 1942
  • With a Little Help from My Friends: Microbial Partners in Integrative and Comparative Biology—An Introduction to the Symposium
    Kevin D. Kohl, M. Denise Dearing
    Integrative and Comparative Biology 2017 57 4
  • You Talking to Me? Says the Enteric Nervous System (ENS) to the Microbe. How Intestinal Microbes Interact with the ENS
    Mauro Giuffrè, Rita Moretti, Giuseppina Campisciano, Alexandre Barcelos Morais da Silveira, Vincenzo Maria Monda, Manola Comar, Stefano Di Bella, Roberta Maria Antonello, Roberto Luzzati, Lory Saveria Crocè
    Journal of Clinical Medicine 2020 9 11

Article usage

Article usage: November 2013 to March 2021

AbstractFullPdf
Nov 201344829595
Dec 20134639119414
Total 201391211281009
Jan 201462974102
Feb 20144004898
Mar 20143533281
Apr 20144481844
May 20142351730
Jun 201414715101
Jul 20141412641
Aug 20141873454
Sep 20142366667
Oct 20142144858
Nov 20141743837
Dec 20141191729
Total 20143283433742
Jan 20151131725
Feb 2015913720
Mar 20151252827
Apr 20151081343
May 20151442540
Jun 20152162023
Jul 20152981440
Aug 2015235927
Sep 20151891145
Oct 20152692328
Nov 20151724438
Dec 20152872344
Total 20152247264400
Jan 20162732551
Feb 20161431639
Mar 20161183255
Apr 2016851532
May 2016621532
Jun 20161141717
Jul 20161111122
Aug 201677912
Sep 20161262530
Oct 20161142726
Nov 20161152431
Dec 2016901124
Total 20161428227371
Jan 20171202024
Feb 20171553873
Mar 20171793648
Apr 20171291831
May 20171212960
Jun 20171101612
Jul 2017862118
Aug 2017831718
Sep 20171602747
Oct 20171383434
Nov 2017921824
Dec 2017742220
Total 20171447296409
Jan 2018963932
Feb 20181087426
Mar 201814611044
Apr 201814912732
May 20181566528
Jun 20181758022
Jul 20181297813
Aug 2018926320
Sep 2018976045
Oct 2018408730
Nov 2018458331
Dec 2018257929
Total 20181258945352
Jan 2019307776
Feb 2019406126
Mar 2019485329
Apr 2019337925
May 2019346028
Jun 2019277525
Jul 2019366729
Aug 2019278023
Sep 2019395735
Oct 2019376033
Nov 20195910144
Dec 20193011413
Total 2019440884386
Jan 2020407428
Feb 2020378338
Mar 2020516927
Apr 2020367232
May 2020556037
Jun 2020472321
Jul 2020466824
Aug 2020494034
Sep 2020425043
Oct 20205115043
Nov 2020717832
Dec 2020486623
Total 2020573833382
Jan 2021476346
Feb 2021487842
Mar 2021020
Total 20219514388
Total1989241534139
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Symbiotic bacteria appear to mediate hyena social odors
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Bacteria appear to mediate hyena social odors
Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, Thomas M. Schmidt
Proceedings of the National Academy of Sciences Dec 2013, 110 (49) 19832-19837; DOI: 10.1073/pnas.1306477110

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Bacteria appear to mediate hyena social odors
Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, Thomas M. Schmidt
Proceedings of the National Academy of Sciences Dec 2013, 110 (49) 19832-19837; DOI: 10.1073/pnas.1306477110
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley

Article Classifications

  • Biological Sciences
  • Ecology
Proceedings of the National Academy of Sciences: 110 (49)
Table of Contents

Submit

Sign up for Article Alerts

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Setting sun over a sun-baked dirt landscape
Core Concept: Popular integrated assessment climate policy models have key caveats
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Model of the Amazon forest
News Feature: A sea in the Amazon
Did the Caribbean sweep into the western Amazon millions of years ago, shaping the region’s rich biodiversity?
Image credit: Tacio Cordeiro Bicudo (University of São Paulo, São Paulo, Brazil), Victor Sacek (University of São Paulo, São Paulo, Brazil), and Lucy Reading-Ikkanda (artist).
Syrian archaeological site
Journal Club: In Mesopotamia, early cities may have faltered before climate-driven collapse
Settlements 4,200 years ago may have suffered from overpopulation before drought and lower temperatures ultimately made them unsustainable.
Image credit: Andrea Ricci.
Steamboat Geyser eruption.
Eruption of Steamboat Geyser
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Listen
Past PodcastsSubscribe
Birds nestling on tree branches
Parent–offspring conflict in songbird fledging
Some songbird parents might improve their own fitness by manipulating their offspring into leaving the nest early, at the cost of fledgling survival, a study finds.
Image credit: Gil Eckrich (photographer).

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Subscribers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates
  • FAQs
  • Accessibility Statement
  • Rights & Permissions
  • About
  • Contact

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490