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Co-niche construction between hosts and symbionts: ideas and evidence

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Abstract

Symbiosis is a process that can generate evolutionary novelties and can extend the phenotypic niche space of organisms. Symbionts can act together with their hosts to co-construct host organs, within which symbionts are housed. Once established within hosts, symbionts can also influence various aspects of host phenotype, such as resource acquisition, protection from predation by acquisition of toxicity, as well as behaviour. Once symbiosis is established, its fidelity between generations must be ensured. Hosts evolve various mechanisms to screen unwanted symbionts and to facilitate faithful transmission of mutualistic partners between generations. Microbes are the most important symbionts that have influenced plant and animal phenotypes; multicellular organisms engage in developmental symbioses with microbes at many stages in ontogeny. The co-construction of niches may result in composite organisms that are physically nested within each other. While it has been advocated that these composite organisms need new evolutionary theories and perspectives to describe their properties and evolutionary trajectories, it appears that standard evolutionary theories are adequate to explore selection pressures on their composite or individual traits. Recent advances in our understanding of composite organisms open up many important questions regarding the stability and transmission of these units.

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References

  • Alegado R. A., Brown L. W., Cao S., Dermenjian R. K., Zuzow R. and Fairclough S. R. 2012 A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1, e00013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett G. M. and Moran N. A. 2015 Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole. Proc. Natl. Acad. Sci.USA 112, 10169–10176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bercik P., Denou E., Collins J., Jackson W., Lu J., Jury J. et al. 2011 The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141, 599–609.

    Article  CAS  PubMed  Google Scholar 

  • Blüthgen N. and Wesenberg J. 2001 Ants induce domatia in a rain forest tree (Vochysia vismiaefolia). Biotropica 33, 637–642.

    Article  Google Scholar 

  • Borges R. M. 2015a How mutualisms between plants and insects are stabilized. Curr. Sci. 108, 1862–1868.

    Google Scholar 

  • Borges R.M. 2015b How to be a fig wasp parasite on the fig–fig wasp mutualism. Curr. Opin. Insect Sci. 8, 34–40.

    Article  Google Scholar 

  • Borges R. M. 2016 On the air: broadcasting and reception of volatile messages in brood-site pollination mutualisms. In Deciphering chemical language of plant communication (ed. J. D. Blande and R. Glinwood), pp. 227–255. Springer International Publishing, Switzerland.

    Chapter  Google Scholar 

  • Brucker R. M. and Bordenstein S. R. 2013 The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341, 667–669.

    Article  CAS  PubMed  Google Scholar 

  • Chau R., Kalaitzis J. A. and Neilan B. A. 2011 On the origins and biosynthesis of tetrodotoxin. Aquat. Toxicol. 104, 61–72.

    Article  CAS  PubMed  Google Scholar 

  • Chiu L. and Gilbert S. F. 2015 The birth of the holobiont: multi-species birthing through mutual scaffolding and niche construction. Biosemiotics 8, 191–210.

    Article  Google Scholar 

  • Coon K. L., Vogel K. J., Brown M. R. and Strand M. R. 2014 Mosquitoes rely on their gut microbiota for development. Mol. Ecol. 23, 2727–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cryan J. F. and Dinan T. G. 2012 Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712.

    Article  CAS  PubMed  Google Scholar 

  • Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M. E. and Boulétreau M. 2001 Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acad. Sci. USA 98, 6247–6252.

  • Dinan T. G., Stilling R. M., Stanton C. and Cryan J. F. 2015 Collective unconscious: how gut microbes shape human behavior. J. Psychiatr. Res. 63, 1–9.

    Article  PubMed  Google Scholar 

  • Doino J. A. and McFall-Ngai M. J. 1995 A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol. Bull. 189, 347–355.

    Article  Google Scholar 

  • Doolittle W. F. and Booth A. 2016 It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol. Philos. 32, 5–24.

    Article  Google Scholar 

  • Douglas A. E. and Werren J. H. 2016 Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7, e02099-15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebert D. 2013 The epidemiology and evolution of symbionts with mixed-mode transmission. Annu. Rev. Ecol. Syst. 44, 623–643.

    Article  Google Scholar 

  • Eisthen H. L. and Theis K. R. 2015 Animal – microbe interactions and the evolution of nervous systems. Phil. Trans. R. Soc. B 371, 20150052.

    Article  Google Scholar 

  • Ezenwa V. O. and Williams A. E. 2014 Microbes and animal olfactory communication: Where do we go from here? BioEssays 36, 847–854.

    Article  PubMed  Google Scholar 

  • Ferreira B. G., Álvarez R., Avritzer S. C. and Isaias R. M. S. 2016 Revisiting the histological patterns of storage tissues: beyond the limits of gall-inducing taxa. Botany 95, 173–184.

    Article  Google Scholar 

  • Forsythe P. and Kunze W. A. 2013 Voices from within: gut microbes and the CNS. Cell. Mol. Life Sci. 70, 55–69.

    Article  CAS  PubMed  Google Scholar 

  • Fraune S. and Bosch T. C. G. 2010 Why bacteria matter in animal development and evolution. BioEssays 32, 571–580.

    Article  CAS  PubMed  Google Scholar 

  • Fraune S., Augustin R., Anton-Erxleben F., Wittlieb J., Gelhaus C. and Klimovich V. B. 2010 In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proc. Natl. Acad. Sci. USA 107, 18067–18072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frederickson M. E. 2013 Rethinking mutualism stability: cheaters and the evolution of sanctions. Q. Rev. Biol. 88, 269–295.

    Article  PubMed  Google Scholar 

  • Fullmer M. S., Soucy S. M. and Gogarten J. P. 2015 The pan-genome as a shared genomic resource: mutual cheating, cooperation and the black queen hypothesis. Front. Microbiol. 6, 728.

  • Gilbert S. F. and Tauber A. I. 2016 Rethinking individuality: the dialectics of the holobiont. Biol. Philos. 31, 839–853.

    Article  Google Scholar 

  • Gilbert S. F., Sapp J. and Tauber A. I. 2012 A symbiotic view of life: we have never been individuals. Q. Rev. Biol. 87, 325–341.

    Article  PubMed  Google Scholar 

  • Gilbert S. F., Bosch T. C. G. and Ledón-Rettig C. 2015 Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat. Rev. Genet. 16, 611–622.

    Article  CAS  PubMed  Google Scholar 

  • Ghara M., Ranganathan Y., Krishnan A., Gowda V. and Borges R. M. 2014 Divvying up an incubator: how parasitic and mutualistic fig wasps use space within their nursery microcosm. Arthropod-Plant Interac. 8, 191–203.

    Article  Google Scholar 

  • Gorman M. L., Nedwell D. B. and Smith R. M. 1974 An analysis of the contents of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J. Zool. 172, 389–399.

    Article  Google Scholar 

  • Hehemann J.-H., Correc G., Barbeyron T., Helbert W., Czjzek M. and Michel G. 2010 Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908–912.

    Article  CAS  PubMed  Google Scholar 

  • Hembry D. H. and Althoff D. M. 2016 Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity. Am. J. Bot. 103, 1783–1792.

    Article  PubMed  Google Scholar 

  • Hom E. F. Y. and Murray A. W. 2014 Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345, 94–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosokawa T., Hironaka M., Inadomi K., Mukai H., Nikoh N. and Fukatsu T. 2013 Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. PLoS One 8, e65081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon K. W. 1983 Integration of bacterial endosymbionts in amoebae. Int. Rev. Cytol. Suppl. 14, 29–47.

    Google Scholar 

  • Jeon T. J. and Jeon K. W. 2003 Characterization of sams genes of Amoeba proteus and the endosymbiotic X-bacteria. J. Eukaryot. Microbiol. 50, 61–69.

    Article  CAS  PubMed  Google Scholar 

  • Johnston P. R. and Rolff J. 2015 Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog. 11, e1005246.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jost M. C., Hillis D. M., Lu Y., Kyle J. W., Fozzard H. A. and Zakon H. H. 2008 Toxin-resistant sodium channels: parallel adaptive evolution across a complete gene family. Mol. Biol. Evol. 25, 1016–1024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Junker R. R. and Tholl D. 2013 Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 39, 810–825.

    Article  CAS  PubMed  Google Scholar 

  • Junker R. R., Loewel C., Gross R., Dötterl S., Keller A. and Blüthgen N. 2011 Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol. 13, 918–924.

    Article  CAS  PubMed  Google Scholar 

  • Kaltenpoth M., Roeser-Mueller K., Koehler S., Peterson A., Nechitaylo T. Y., Stubblefield J. W. et al. 2014 Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis. Proc. Natl. Acad. Sci. USA  111, 6359–6364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khakhina L. N., Margulis L. and McMenamin M. A. 1992 Concepts of symbiogenesis: a historical and critical study of the research of Russian botanists. Yale University Press, New Haven, USA.

  • Krishnan A. and Borges R. M. 2014 Parasites exert conflicting selection pressures to affect reproductive asynchrony of their host plant in an obligate pollination mutualism. J. Ecol. 102, 1329–1340.

    Article  Google Scholar 

  • Kwong W. K. and Moran N. A. 2015 Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 6, 214–220.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwong W. K., Engel P., Koch H. and Moran N. A. 2014 Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl. Acad. Sci. USA 111, 11509–11514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanan M. C., Rodrigues P. A. P., Agellon A., Jansma P. and Wheeler D. E. 2016 A bacterial filter protects and structures the gut microbiome of an insect. ISME J.  10, 1866–1876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laland K. N. and Sterelny K. 2006 Perspective: seven reasons (not) to neglect niche construction. Evolution 60, 1751–1762.

    Article  PubMed  Google Scholar 

  • Lewontin R. C. 1983 Genes, organisms and environment. In Evolution from molecules to men (ed. D. S. Bendall), pp. 273–285. Cambridge University Press, Cambridge, UK.

  • Margulis L. 1991 Symbiogenesis and symbionticism. In Symbiosis as a source of evolutionary innovation: speciation and morphogenesis (ed. L. Margulis and R. Fester), pp. 1–14. MIT Press, Cambridge, Massachusetts, USA.

    Google Scholar 

  • Mayer V. E., Frederickson M. E., McKey D. and Blatrix R. 2014 Current issues in the evolutionary ecology of ant–plant symbioses. New Phytol. 202, 749–764.

    Article  PubMed  Google Scholar 

  • McFall-Ngai M. J. 2002 Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242, 1–14.

    Article  CAS  PubMed  Google Scholar 

  • McFall-Ngai M., Hadfield M. G., Bosch T. C., Carey H. V., Domazet-Lošo T., Douglas A. E. et al. 2013 Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110, 3229–3236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moczek, A. P. 2015 Re-evaluating the environment in developmental evolution. Front. Ecol. Evol. 3, 7.

    Article  Google Scholar 

  • Montgomery M. K. and McFall-Ngai M. 1994 Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120, 1719–1729.

    CAS  PubMed  Google Scholar 

  • Moran N. A. and Sloan D. B. 2015 The hologenome concept: helpful or hollow? PLoS Biol. 13, e1002311.

    Article  PubMed  PubMed Central  Google Scholar 

  • Morris J. J. 2015 Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet. 31, 475–482.

  • Morris J. J., Lenski R. E. and Zinser E. R. 2012 The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036-12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mushegian A. A. and Ebert D. 2015 Rethinking “mutualism” in diverse host-symbiont communities. BioEssays 38, 100–108.

    Article  PubMed  Google Scholar 

  • Ohbayashi T. et al. 2015 Insect’s intestinal organ for symbiont sorting. Proc. Natl. Acad. Sci. USA 112, E5179–E5188.

  • Oliveira D. C., Isaias R. M. S., Fernandes G. W., Ferreira B. G., Carneiro R. G. S. and Fuzaro L. 2016 Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J. Insect Physiol. 84, 103–113.

  • Oono R., Anderson C. G. and Denison R. F. 2011 Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc. R. Soc. London, Ser. B 278, 2698–2703.

    Article  Google Scholar 

  • Peñuelas J., Farré-Armengol G., Llusia J., Gargallo-Garriga A., Rico L., Sardans J., Terradas J. and Filella I. 2014 Removal of floral microbiota reduces floral terpene emissions. Sci. Rep. 4, 6727.

  • Rawls J. F., Samuel B. S. and Gordon J. I. 2004 Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 101, 4596–4601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Root-Bernstein R. 2016 Autoimmunity and the microbiome: T-cell receptor mimicry of “self” and microbial antigens mediates self tolerance in holobionts. BioEssays 38, 1068–1083.

  • Salem H., Florez L., Gerardo N. and Kaltenpoth M. 2015 An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. London, Ser. B 282, 20142957.

  • Sapp J. 1994 Evolution by association: a history of symbiosis. Oxford University Press, New York, USA.

    Google Scholar 

  • Schwartzman J. A. and Ruby E. G. 2016 A conserved chemical dialog of mutualism: lessons from squid and vibrio. Microbes Infect. 18, 1–10.

    Article  PubMed  Google Scholar 

  • Schwartzman J. A., Koch E., Heath-Heckman E. A. C., Zhou L., Kremer N., McFall-Ngai M. J. and Ruby E. G. 2015 The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation. Proc. Natl. Acad. Sci. USA 112, 566–571.

    Article  CAS  PubMed  Google Scholar 

  • Shapira M. 2016 Gut microbiotas and host evolution: scaling up symbiosis. Trends Ecol. Evol. 31, 539–549.

    Article  PubMed  Google Scholar 

  • Shropshire J. D. and Bordenstein S. R. 2016 Speciation by symbiosis: the microbiome and behavior. mBio 7, e01785-15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stappenbeck T. S., Hooper L. V. and Gordon J. I. 2002 Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99, 15451–15455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Valen L. 1973 A new evolutionary law. Evol. Theory 1, 1–30.

    Google Scholar 

  • Wang D., Yang S., Tang F., and Zhu H. 2012 Symbiosis specificity in the legume–rhizobial mutualism. Cell. Microbiol. 14, 334–342.

    Article  PubMed  Google Scholar 

  • Werren J. H., Baldo L. and Clark M. E. 2008 Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751.

    Article  CAS  PubMed  Google Scholar 

  • Wong A. C. N., Holmes A., Ponton F., Lihoreau M., Wilson K., Raubenheimer D. and Simpson S. J. 2015 Behavioral microbiomics: a multi-dimensional approach to microbial influence on behavior. Front. Microbiol. 6, 1359.

    PubMed  PubMed Central  Google Scholar 

  • Wray G. A., Hoekstra H. E., Futuyma D. J., Lenski R. E., Mackay F. C., Schulter D. and Strassmann J. E. 2014 Does evolutionary theory need a rethink? No, all is well. Nature 514, 161–164.

    Article  PubMed  Google Scholar 

  • Zilber-Rosenberg I. and Rosenberg. 2008 Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735.

    Article  CAS  PubMed  Google Scholar 

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  1. Centre for Ecological Sciences, Indian Institute of Science, Bengaluru, 560 012, India

    Renee M. Borges

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Borges, R.M. Co-niche construction between hosts and symbionts: ideas and evidence. J Genet 96, 483–489 (2017). https://doi.org/10.1007/s12041-017-0792-9

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