Speciation by Symbiosis: the Microbiome and Behavior

J Dylan Shropshire, Seth R Bordenstein


Species are fundamental units of comparison in biology. The newly discovered importance and ubiquity of host-associated microorganisms are now stimulating work on the roles that microbes can play in animal speciation. We previously synthesized the literature and advanced concepts of speciation by symbiosis with notable attention to hybrid sterility and lethality. Here, we review recent studies and relevant data on microbes as players in host behavior and behavioral isolation, emphasizing the patterns seen in these analyses and highlighting areas worthy of additional exploration. We conclude that the role of microbial symbionts in behavior and speciation is gaining exciting traction and that the holobiont and hologenome concepts afford an evolving intellectual framework to promote research and intellectual exchange between disciplines such as behavior, microbiology, genetics, symbiosis, and speciation. Given the increasing centrality of microbiology in macroscopic life, microbial symbiosis is arguably the most neglected aspect of animal and plant speciation, and studying it should yield a better understanding of the origin of species.


Feb 1, 1978·Journal of Dental Research·R Pianotti, G Pitts
Oct 22, 1982·Science·W D Hamilton, M Zuk
Aug 1, 1995·Insect Molecular Biology·E Zchori-FeinD Rosen
Sep 16, 1998·Proceedings of the National Academy of Sciences of the United States of America·C R Woese
Nov 5, 1999·Annual Review of Microbiology·Richard StouthamerGregory D D Hurst
Jun 15, 2000·Proceedings. Biological Sciences·James P RandersonL D Hurst
Aug 9, 2001·Journal of Clinical Periodontology·M Morita, H L Wang
Apr 1, 1990·Proceedings of the National Academy of Sciences of the United States of America·R StouthamerW D Hamilton
Sep 25, 2003·Proceedings of the National Academy of Sciences of the United States of America·Charles LinnWendell Roelofs
Oct 14, 2003·PLoS Biology·Christian BraendleDavid L Stern
Mar 12, 2004·Annual Review of Entomology·W S Leal
Apr 17, 2004·Proceedings of the National Academy of Sciences of the United States of America·Emily A Dyson, Gregory D D Hurst
May 20, 2004·Journal of Evolutionary Biology·F ValaM W Sabelis
May 29, 2004·FEBS Letters·Gregor D GilfillanPeter B Becker
Aug 13, 2004·Proceedings. Biological Sciences·Masato HirokiYoshiomi Kato
Nov 24, 2004·Die Naturwissenschaften·Geoffrey E Hill, Kristy L Farmer
May 25, 2005·Journal of Experimental Botany·J A W MorganP J White
Jul 22, 2005·Journal of Evolutionary Biology·B A PannebakkerJacques J M van Alphen
Dec 7, 2005·Evolution; International Journal of Organic Evolution·Arndt TelschowJohn H Werren
Mar 30, 2006·Evolution; International Journal of Organic Evolution·Katerina KoukouStamatis N Alahiotis
Jul 5, 2006·Evolution; International Journal of Organic Evolution·S M ShusterT G Whitham
Oct 13, 2006·PLoS Biology·John JaenikeMiranda S Minhas
Feb 6, 2007·Current Biology : CB·Sylvain CharlatGregory D D Hurst
Jun 8, 2007·Microbiology and Molecular Biology Reviews : MMBR·Michael W TaylorMichael Wagner
Nov 22, 2007·Proceedings. Biological Sciences·Kerry M OliverMartha S Hunter
Feb 28, 2008·Proceedings. Biological Sciences·Kazuko NakanishiYasuhisa Kunimi
Mar 25, 2008·Colloids and Surfaces. B, Biointerfaces·Yuki TsuchiyaHisao Morisaki
May 24, 2008·Science·Ruth E LeyJeffrey I Gordon
May 31, 2008·Science·William O H HughesFrancis L W Ratnieks
Jun 14, 2008·FEMS Microbiology Reviews·Ilana Zilber-Rosenberg, Eugene Rosenberg
Aug 21, 2008·Annual Review of Genetics·Laura R SerbusWilliam Sullivan
Aug 21, 2008·Proceedings. Biological Sciences·Tetsuya Adachi-HagimoriRichard Stouthamer
Sep 17, 2008·Nature Reviews. Microbiology·John H WerrenMichael E Clark
Jan 10, 2009·Science·Lauren J CatorRonald R Hoy
Apr 4, 2009·Nature Reviews. Immunology·June L Round, Sarkis K Mazmanian
Aug 8, 2009·Evolution; International Journal of Organic Evolution·Ken KraaijeveldJacques J M van Alphen
Nov 19, 2009·Journal of Agricultural and Food Chemistry·Jang-Eun LeeYoung-Shick Hong
Oct 13, 2010·Proceedings of the National Academy of Sciences of the United States of America·Andrew K BensonDaniel Pomp
Nov 3, 2010·Proceedings of the National Academy of Sciences of the United States of America·Gil SharonEugene Rosenberg
Nov 26, 2010·Science·Tsutomu TsuchidaTakema Fukatsu
Nov 26, 2010·PLoS Biology·Howard OchmanPhilip Hugenholtz
Oct 1, 1998·Trends in Ecology & Evolution·D Penn, W K Potts
Mar 17, 2011·Nature Reviews. Microbiology·Aymé SporRuth E Ley
Apr 29, 2011·Fly·John RingoDaniel Segal
Aug 13, 2011·Current Biology : CB·John P McCutcheon, Carol D von Dohlen
Dec 14, 2011·Seminars in Immunology·M J McFall-NgaiElizabeth A Harvie
May 1, 2012·Trends in Ecology & Evolution·Robert M Brucker, Seth R Bordenstein
Jun 8, 2012·Science·Jeremy K NicholsonSven Pettersson
Jun 16, 2012·Nature·Tanya YatsunenkoJeffrey I Gordon
Jul 17, 2012·Nature·Marcus J ClaessonPaul W O'Toole
Jul 25, 2012·Proceedings of the National Academy of Sciences of the United States of America·Patrick H DegnanHoward Ochman
Oct 16, 2012·Science·Vanessa O EzenwaJoao B Xavier
Nov 13, 2012·Trends in Ecology & Evolution·Anne LizéZenobia Lewis
Nov 28, 2012·Current Biology : CB·Qian LiStephen D Liberles
Dec 12, 2012·PloS One·Robert M Brucker, Seth R Bordenstein
Jan 3, 2013·FEMS Microbiology Ecology·A Gordon JamesRalph Calvert
Feb 9, 2013·Proceedings of the National Academy of Sciences of the United States of America·M J McFall-NgaiJennifer J Wernegreen
Feb 13, 2013·The Quarterly Review of Biology·Scott F GilbertAlfred I Tauber
Jun 29, 2013·Genome Biology·Thomas R TurnerPhilip S Poole
Aug 27, 2013·PLoS Biology·Lisa J Funkhouser, Seth R Bordenstein
Sep 5, 2013·Proceedings of the National Academy of Sciences of the United States of America·Sören FranzenburgSebastian Fraune
Sep 17, 2013·Zoology : Analysis of Complex Systems, ZACS·Robert M Brucker, Seth R Bordenstein
Nov 12, 2013·BMC Microbiology·Karl Mathias WegnerAlexander Eiler
Nov 13, 2013·Proceedings of the National Academy of Sciences of the United States of America·Kevin R TheisThomas M Schmidt
Dec 7, 2013·Molecular Ecology·Jon G SandersNaomi E Pierce
Dec 18, 2013·Nature·Lawrence A DavidPeter J Turnbaugh
Jan 30, 2014·Proceedings of the National Academy of Sciences of the United States of America·Nuri KodamanPelayo Correa
Apr 1, 2014·Ecology and Evolution·Sarah PolinYannick Outreman
Apr 20, 2014·The Journal of Experimental Biology·Isvarya VenuReuven Dukas
May 31, 2014·Integrative and Comparative Biology·Susan L Balenger, Marlene Zuk
Jun 13, 2014·Gut Microbes·Zenobia LewisAnne Lizé
Jul 6, 2014·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Vanessa O Ezenwa, Allison E Williams
Aug 17, 2014·Applied and Environmental Microbiology·Chris CallewaertNico Boon
Nov 25, 2014·Cell·Julia K GoodrichRuth E Ley
Mar 17, 2015·ELife·Jenny TungElizabeth A Archie
May 15, 2015·Cell Host & Microbe·Timothy R Sampson, Sarkis K Mazmanian
Jun 19, 2015·The Journal of Experimental Biology·M J McFall-Ngai
Aug 19, 2015·PLoS Biology·Seth R Bordenstein, Kevin R Theis
Sep 12, 2015·Science·Edward J van Opstal, Seth R Bordenstein
Sep 16, 2015·Nature Reviews. Genetics·Scott F GilbertCristina Ledón-Rettig
Sep 17, 2015·Genome Biology·Ran BlekhmanAndrew G Clark
Oct 30, 2015·Science·A P AlivisatosUnified Microbiome Initiative Consortium
Nov 9, 2015·Journal of Experimental Botany·Gabriele BergMartina Köberl
Nov 10, 2015·Journal of Evolutionary Biology·Devin ArbuthnottD E L Promislow
Dec 15, 2015·The American Naturalist·Odrade NouguéThomas Lenormand


Jun 22, 2016·PeerJ·Peter BaasMatthew D Wallenstein
Sep 8, 2016·PeerJ·J Dylan ShropshireSeth R Bordenstein
Oct 11, 2016·Frontiers in Microbiology·Jessica DittmerRobert M Brucker
Oct 18, 2016·Evolution; International Journal of Organic Evolution·Janette W Boughman, Richard Svanbäck
Feb 9, 2017·Memórias do Instituto Oswaldo Cruz·Miguel A SaldañaGrant L Hughes
Mar 18, 2017·Journal of Theoretical Biology·Maureen A O'Malley
Mar 6, 2018·Genetics and Molecular Biology·Karen Luisa Haag
Jan 20, 2018·Genome Biology and Evolution·Amelia R I LindseyIrene L G Newton
Nov 25, 2017·Frontiers in Immunology·Juris A Grasis
Oct 13, 2018·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Philip T LeftwichTracey Chapman
Mar 23, 2019·Annals of the New York Academy of Sciences·James A Shapiro
Aug 29, 2019·Physiological Reviews·J F CryanT G Dinan
Nov 2, 2019·Science·Eoin SherwinJ F Cryan
Aug 3, 2020·Insect Molecular Biology·X L Zheng
Jul 14, 2020·Molecular Biology and Evolution·Corinna BreusingRoxanne A Beinart
Aug 2, 2017·Journal of Genetics·Renee M Borges
May 31, 2018·BMC Evolutionary Biology·Kym D PerrySimon W Baxter
Nov 14, 2019·Archives of Microbiology·Dandan Wang, Cong Wei
May 30, 2017·Frontiers in Microbiology·Tyler J Carrier, Adam M Reitzel
Aug 11, 2020·Frontiers in Microbiology·Ruxin DuanNingxin Wang
Dec 27, 2016·Frontiers in Cellular and Infection Microbiology·Elisabeth HodilleOana Dumitrescu
Nov 8, 2017·Proceedings of the National Academy of Sciences of the United States of America·Philip T LeftwichTracey Chapman
Jul 14, 2017·Microbial Ecology·Anne Duplouy, Oskar Brattström
Nov 25, 2018·BMC Microbiology·Francesca ScolariAnna Rodolfa Malacrida
May 15, 2020·Biological Reviews of the Cambridge Philosophical Society·Javier Suárez, Adrian Stencel
May 10, 2017·Chromosome Research : an International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology·Raquel Toribio-FernándezMiguel Pita
Nov 20, 2018·Biological Reviews of the Cambridge Philosophical Society·Martina Prazeres, Willem Renema
Apr 30, 2019·Frontiers in Plant Science·Mohsen HajheidariMarcel Bucher
Aug 20, 2020·BMC Evolutionary Biology·Sara J DunajRobert M Brucker

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