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The Evolution of Holobionts

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The Hologenome Concept: Human, Animal and Plant Microbiota

Abstract

In the previous chapters, we have presented published experimental data in support of the principles upon which the hologenome concept are based. We also pointed out special aspects of the concept, such as the additional modes of genetic variation within the holobiont. In this chapter, we will discuss the hologenome concept of evolution and how the concept relates to other ideas in evolutionary biology. The key point that we would like to stress is that microorganisms were fundamental in the formation and evolution of complexity in animals and plants.

So, like it or not, microbiology is going to be in the center of evolutionary study in the future—and vice versa.

—Carl R. Woese

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References

  • Alexy, K. J., Gassett, J. W., Osborn, D. A., & Miller, K. V. (2003). Bacterial fauna of the tarsal tufts of white-tailed deer (Odocoileus virginianus). American Midland Naturalist, 149, 237–240.

    Google Scholar 

  • Anderson, M. T., & Seifert, H. S. (2011). Opportunity and means: horizontal gene transfer from the human host to a bacterial pathogen. MBio, 2, e00005–e00011.

    PubMed Central  PubMed  Google Scholar 

  • Andersson, S. G. E., Zomorodipour, A., Andesson, J. O., et al. (1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature, 396, 133–140.

    CAS  PubMed  Google Scholar 

  • Archie, E. A., & Theis, K. R. (2011). Animal behaviour meets microbial ecology. Animal Behaviour, 82, 425–436.

    Google Scholar 

  • Austin, C., & Ellis, J. (2003). Microbial pathways leading to steroidal malodour in the axilla. Journal of Steroid Biochemistry and Molecular Biology, 87, 105–110.

    CAS  PubMed  Google Scholar 

  • Axelrod, R. (1984). The evolution of cooperation. New York: Basic Books Inc.

    Google Scholar 

  • Axelrod, R., & Hamilton, W. D. (1981). The evolution of cooperation. Science, 211, 1390–1396.

    CAS  PubMed  Google Scholar 

  • Bäckhed, F., Ley, R. E., Sonneburg, J. L., et al. (2005). Host-bacterial mutualism in the human intestine. Science, 307, 1915–1919.

    PubMed  Google Scholar 

  • BaluÅ¡ka, F., & Mancuso, S. (2013). Microorganism and filamentous fungi drive evolution of plant synapses. Frontiers in Cellular and Infection Microbiology, 3, 44. doi:10.3389/fcimb.2013.00044

    PubMed Central  PubMed  Google Scholar 

  • Belshaw, R., Pereira, V., Katzourakis, A., et al. (2004). Long-term reinfection of the human genome by endogenous retroviruses. Proceedings of the National Academy of Sciences of the United States of America, 101, 4894–4899.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ben-Dov, E., Kramarsky-Winter, E., & Kushmaro, A. (2009). An in situ method for cultivating microorganisms using a double encapsulation technique. FEMS Microbiology Ecology, 68, 363–371.

    CAS  PubMed  Google Scholar 

  • Benkler, Y. (2011). The penguin and the levaiathan: how cooperation triumphs over self-interest. New York: Crown business.

    Google Scholar 

  • Bidartondo, M. I., Read, D. J., Trappe, J. M., et al. (2011). The dawn of symbiosis between plants and fungi. Biology letters, 7, 574–577.

    PubMed Central  PubMed  Google Scholar 

  • Bijma, P., Muir, W. M., & Van Arendonk, J. A. M. (2007). Multilevel selection: quantitative genetics of inheritance and response to selection. Genetics, 175, 277–288.

    PubMed  Google Scholar 

  • Breznak, J. A., & Pankratz, H. S. (1977). In situ morphology of the gut microbiota of wood-eating termites (Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki). Applied and Environmental Microbiology, 33, 406–426.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brucker, R. M., & Bordenstein, S. R. (2012). Speciation by symbiosis. Trends in Ecology and Evolution, 27, 443–451.

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bugaut, M. (1987). Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comparative Biochemistry, 86, 439–472.

    CAS  PubMed  Google Scholar 

  • Collinson, M. E., & Hooker, J. J. (1991). Fossil evidence of interactions between plants and plant-eating mammals. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 333, 197–200.

    CAS  PubMed  Google Scholar 

  • Coyne, J. A. (1992). Genetics and speciation. Nature, 355, 511–515.

    CAS  PubMed  Google Scholar 

  • Coyne, J. A., Orr, H. A. (2004). Speciation (pp. xiii, pp. 545). Sunderland: Sinauer.

    Google Scholar 

  • Darwin, C. (1859). Origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. www.talkorigins.org/faqs/origin.html

  • Dawkins, R. (1976). The Selfish Gene. Oxford: Oxford University Press.

    Google Scholar 

  • De Clerck, O., Bogaert, K. A., & Leliaert, F. (2012). Diversity and evolution of algae. Advances in Botanical Research, 64, 55–86.

    Google Scholar 

  • Denison, R. F., & Kiers, E. T. (2011). Life histories of symbiotic rhizobia and mycorrhizal fungi. Current Biology, 21, R775–R785.

    CAS  PubMed  Google Scholar 

  • Dethlefsen, L., McFall-Ngai, M., & Relman, D. A. (2007). An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature, 449, 811–818.

    CAS  PubMed  Google Scholar 

  • Dobzhansky, T. (1936). Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobsmra hybrids. Genetics, 21, 113–135.

    CAS  PubMed  Google Scholar 

  • Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.

    Google Scholar 

  • Dodd, D. M. B. (1989). Reproductive isolation as a consequence of adaptive divergence in Drosophila-pseudoobscura. Evolution, 43, 1308–1311.

    Google Scholar 

  • Dolan, L. (2009). Body building on land—morphological evolution of land plants. Current Opinion in Plant Biology, 12, 4–8.

    CAS  PubMed  Google Scholar 

  • Domazet-Loso, T., & Tautz, D. (2008). An ancient evolutionary origin of genes associated with human genetic diseases. Molecular Biology and Evolution, 25, 2699–2707.

    CAS  PubMed  Google Scholar 

  • Douglas, A. E. (2008). Conflict, cheats and the persistence of symbioses. New Phytologist, 177, 849–858.

    PubMed  Google Scholar 

  • Dunning-Hotopp, J. C., Clark, M. E., Oliveira, D. C., et al. (2007). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science, 317, 1753–1756.

    CAS  PubMed  Google Scholar 

  • Dupressoir, A., Lavialle, C., & Heidmann, T. (2012). From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta, 33, 663–671.

    CAS  PubMed  Google Scholar 

  • Dupressoir, A., Vernochet, C., Bawa, O., et al. (2009). Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proceedings of the National Academy of Sciences of the United States of America, 106, 12127–12132.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ejima, A., & Griffith, L. C. (2007). Measurement of courtship behavior in Drosophila melanogaster. Cold Spring Harbor Protocols,. doi:10.1101/pdb.prot4847

    PubMed  Google Scholar 

  • Faith, J. J., Guruge, J. L., Charbonneau, M., et al. (2013). The long-term stability of the human gut microbiota. Science, 341(6141), 1237439.

    PubMed Central  PubMed  Google Scholar 

  • Frank, S. A. (1998). Foundations of social evolution. Princeton: Princeton University Press.

    Google Scholar 

  • Gerdes, S., El Yacoubi, B., Bailly, M., et al. (2011). Synergistic use of plant-prokaryote comparative genomics for functional annotations. BMC Genomics, 12(1), S2.

    PubMed Central  PubMed  Google Scholar 

  • Gilbert, S. F., Sapp, J., & Tauber, A. I. (2012). Asymbiotic view of life: we have never been individuals. The Quarterly Review of Biolog, 87, 325–341.

    Google Scholar 

  • Gill, S. R., Pop, M., DeBoy, R. T., et al. (2006). Metagenomic analysis of the human distal gut microbiome. Science, 312, 1355–1359.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goodnight, C. J., & Stevens, L. (1997). Experimental studies of group selection: What do they tell us about group selection in nature? The American Naturalist, 150, S59–S79.

    PubMed  Google Scholar 

  • Gordon, J., Knowlton, N., Relman, D. A., et al. (2013). Superorganisms and holobionts. Microb.

    Google Scholar 

  • Gorman, M. L., Nedwell, D. B., & Smith, R. M. et al. (1974). Analysis of contents of anal scent pockets of Herpestes auropunctatus (Carnivora-Viverridae). Journal of Zoology, 172, 389–399.

    Google Scholar 

  • Gray, M. W. (2012). Mitochondrial evolution. Cold Spring Harbor Perspectives in Biology,. doi:10.1101/cshperspect.a011403

    PubMed  Google Scholar 

  • Harari, Y. N. (2012). From animals into Gods: a brief history of humankind. Israel: Kinneret, Zamora-Bitan, Dvir—Publishing House Ltd.

    Google Scholar 

  • Hardison, R. C. (1996). A brief history of hemoglobins: plant, animal, protist, and bacteria. Proceedings of the National Academy of Sciences of the United States of America, 93, 5675–5679.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hehemann, J. H., Correc, G., Barbeyron, T., et al. (2010). Transfer of carbohydrate active enzymes from marine bacteria to Japanese gut microbiota. Nature, 464, 908–912.

    Google Scholar 

  • Hölldobler, B., & Wilson, E. O. (2008). The superorganism: the beauty, elegance, and strangeness of insect societies. New York: W. W. Norton.

    Google Scholar 

  • Horie, M., Honda, T., Suzuki, Y., et al. (2010). Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature, 463, 84–87.

    CAS  PubMed Central  PubMed  Google Scholar 

  • International Human Genome Sequencing Consortium. (2004). Finishing the euchromatic sequence of the human genome. Nature, 431, 931–945.

    Google Scholar 

  • Jami, E., & Mizrahi, I. (2012). Composition and similarity of bovine rumen microbiota across individual animals. PLoS One, 7(3), e33306.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Janda, J. M., & Abbott, S. L. (2007). 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. Journal of Clinical Microbiology, 45, 2761–2764.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jansa, J., Bukovská, P., & Gryndler, M. (2013). Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts—or just soil free-riders? Frontiers in Plant Science, 4, 134–142.

    PubMed Central  PubMed  Google Scholar 

  • Johnson, N. A. (2000). Gene interaction and the origin of species. Epistasis and the Evolutionary Process (pp. 197–212). New York: Oxford University.

    Google Scholar 

  • Keeling, P. J., & Palmer, J. D. (2008). Horizontal gene transfer in eukaryotic evolution. Nature Reviews Genetics, 9, 605–618.

    CAS  PubMed  Google Scholar 

  • Kerr, B., & Godfrey-Smith, P. (2002). Individualist and multi-level perspectives on selection in structured populations. Biology and Philosophy, 17, 477–517.

    Google Scholar 

  • Kikuchi, Y., Hayatsu, M., Hasokawa, T., et al. (2012). Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences, 109, 8618–8622.

    CAS  Google Scholar 

  • Kim, Y. K., Phillips, D. R., Chao, T., & Ehrman, L. (2004). Developmental isolation and subsequent adult behavior of Drosophila paulistorum. VI. Quantitative variation in cuticular hydrocarbons. Behavior Genetics, 34, 385–394.

    PubMed  Google Scholar 

  • Kyriacou, C. P., & Hall, J. C. (1980). Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male’s courtship song. Proceedings of the National Academy of Sciences of the United States of America, 77, 6729–6733.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu, M. Y., Fan, L., Zhong, L., et al. (2012). Metaproteogenomic analysis of a community of sponge symbionts. The ISME Journal, 6, 1515–1525.

    CAS  PubMed  Google Scholar 

  • Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., et al. (2012). Diversity, stability and resilience of the human gut microbiota. Nature, 489, 220–230.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mackie, R. I. (2002). Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integrative and Comparative Biology, 42, 319–326.

    PubMed  Google Scholar 

  • Mahowald, M. A., Rey, F. E., Seedorf, H., et al. (2009). Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proceedings of the National Academy of Sciences of the United States of America, 106, 5859–5864.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martin, W., Rujan, T., Richlyet, E., et al. (2002). Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 99, 12246–12251.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.

    Google Scholar 

  • Mayr, E. (1996). What is a species, and what is not? Philosophy of Science, 63, 262–277.

    Google Scholar 

  • Mazhar, S., Cohen, J. D., & Hasnain, S. (2013). Auxin producing non-heterocystous cyanobacteria and their impact on the growth and endogenous auxin homeostasis of wheat. Journal of Basic Microbiology, 37, 634–663.

    Google Scholar 

  • McKinnon, J. S., Mori, S., Blackman, B. K., et al. (2004). Evidence for ecology’s role in speciation. Nature, 429, 294–298.

    CAS  PubMed  Google Scholar 

  • Mizrahi, I. (2011). Role of the rumen microbiota in determining the feed efficiency of dairy cows. In E. Rosenberg & U. Gophna (Eds.), Beneficial microorganisms in multicellular life forms. Heidelberg: Springer.

    Google Scholar 

  • Monahan-Giovanelli, H., Pinedo, C. A., & Gage, D. J. (2006). Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiology, 104, 661–670.

    Google Scholar 

  • Moriguchi, K., Maeda, Y., Satou, M., et al. (2001). The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae. Journal of Molecular Biology, 307, 771–784.

    CAS  PubMed  Google Scholar 

  • Moran, N. A., & Jarvik, T. (2010). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science, 328, 624–627.

    CAS  PubMed  Google Scholar 

  • Muir, W. M., Bijma, P., & Schinckel, A. (2013). Multilevel selection with kin and non-kin groups. Experimental results with Japanese quail (Coturnix japonica). Evolution, 67, 1598–1606.

    PubMed Central  PubMed  Google Scholar 

  • Nalepa, C. A., Bignell, D. E., & Bandi, C. (2001). Detritivory, coprophagy, and the evolution of digestive mutualisms. Insectes Sociaux, 48, 194–201.

    Google Scholar 

  • Nowak, M. A. (2006). Five rules for the evolution of cooperation. Science, 314, 1560–1563.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nyholm, S. V., & McFall-Ngai, M. (2004). The winnowing: establishing the squid vibrio symbiosis. Nature Reviews Microbiology, 2, 632–642.

    CAS  PubMed  Google Scholar 

  • Ochman, H., Worobey, M., Kuo, C., et al. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8, e1000546.

    PubMed Central  PubMed  Google Scholar 

  • Okasha, S. (2006). The levels of selection debate: philosophical issues. Philosophy Compass, 1, 1–12.

    Google Scholar 

  • Ott, T., Sullivan, J., James, E. K., et al. (2009). Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Molecular Plant-Microbe Interactions, 22, 800–808.

    CAS  PubMed  Google Scholar 

  • Parfreya, L. W., Lahra, D. J. G., Knoll, A. H., & Katza, L. A. (2011). Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proceedings of the National Academy of Sciences of the United States of America, 108, 13624–13629.

    Google Scholar 

  • Pérez-Brocal, V., Gil, R., Ramos, S., et al. (2006). A small microbial genome: the end of a long symbiotic relationship? Science, 314, 312–313.

    PubMed  Google Scholar 

  • Price, D. C., Chan, C. X., Yoon, H. S., et al. (2012). D. Cyanophora paradoxa Genome elucidates origin of photosynthesis in algae and plants. Science, 335, 843–847.

    CAS  PubMed  Google Scholar 

  • Qin, J., Lil, R., Raes, J., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59–65.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Redecker, D., Kodner, R., & Graham, L. E. (2002). Palaeoglonius grayi from the Ordovician. Mycotaxon, 84, 33–37.

    Google Scholar 

  • Rice, W. R., & Hostert, E. E. (1993). Laboratory experiments on speciation: what have we learned in 40 years? Evolution, 47, 1637–1653.

    Google Scholar 

  • Ridley, M. (2004). Evolution (3rd ed.). Oxford: Blackwell Publishing Co.

    Google Scholar 

  • Rosenberg, E., Keller, K. H., & Dworkin, M. (1977). Cell density dependent growth of Myxococcus xanthus on casein. Journal of Bacteriology, 129, 770–777.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruse, M. (1980). Charles Darwin and group selection. Annals of Science, 37, 615–630.

    CAS  PubMed  Google Scholar 

  • Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323, 737–741.

    CAS  PubMed  Google Scholar 

  • Sharon, G., Segal, D., Ringo, J. M., et al. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 107, 20051–20056.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sharon, G., Segal, D., Zilber-Rosenberg, I., et al. (2011). Symbiotic bacteria are responsible for diet-induced mating preference in Drosophila melanogaster, providing support for the hologenome concept of evolution. Gut Microbes, 2, 190–192.

    PubMed  Google Scholar 

  • Singh, P. B., Herbert, J., Arnott, L., et al. (1990). Rearing rats in a germ-free environment eliminates their odors of individuality. Journal of Chemical Ecology, 16, 1667–1682.

    CAS  PubMed  Google Scholar 

  • Sorenson, M. D., & Fleischer, R. C. (1996). Multiple independent transpositions of mitochondrial DNA control region sequences to the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 93, 15239–15243.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Turnbaugh, P. J., Hamady, M., Yatsunenko T., et al. (2009). A core gut microbiome in obese and lean twins. Nature, 457, 80–484.

    Google Scholar 

  • Turnbaugh, P. J., Quince, C., Faith, J. J., et al. (2010). Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proceedings of the National Academy of Sciences of the United States of America, 107, 7503–7508.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Velagapudi, V. R., Hezaveh, R., Reigstad, C. S., et al. (2010). The gut microbiota modulates host energy and lipid metabolism in mice. Journal of Lipid Research, 51, 1101–1112.

    CAS  PubMed  Google Scholar 

  • Voigt, C. C., Caspers, B., & Speck, S. (2005). Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. Journal of Mammalogy, 86, 745–749.

    Google Scholar 

  • Wakano, J. Y., Nowak, M. A., & Hauert, C. (2009). Spatial dynamics of ecological public goods. Proceedings of the National Academy of Sciences of the United States of America, 106, 7910–7914.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Williams, G. C. (1966). Adaptation and natural selection. Princeton: Princeton University Press.

    Google Scholar 

  • West, S. A., Griffin, A. S., Gardner, A., & Diggle, S. P. (2006). Social evolution theory for microorganisms. Nature Reviews Microbiology, 4, 597–607.

    CAS  PubMed  Google Scholar 

  • West, S. A., Diggle, S. P., Buckling, A., et al. (2007). The social lives of microbes. Annual Review of Ecology, Evolution, and Systematics, 38, 53–77.

    Google Scholar 

  • Wheeler, W. M. (1928). The social insects, their origin and evolution. New York: Harcourt Brace.

    Google Scholar 

  • Wikoff, W. R., Anfora, A. T., Liu, J., et al. (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences of the United States of America, 106, 3698–3703.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilson, D. S. (1989). Levels of selection: an alternative to individualism in biology and the human sciences. Social Networks, 11, 257–272.

    Google Scholar 

  • Wilson, A. C. C., Ashton, P. D., Calevro, F., et al. (2010). Genomic insight into the amino acid relations of the pea aphid Acyrthosiphon pisum with its symbiotic bacterium Buchnera aphidicola. Insect Molecular Biology, 19, 249–258.

    CAS  PubMed  Google Scholar 

  • Wilson, D. S., & Sober, E. (1989). Reviving the superorganism. Journal of Theoretical Biology, 136, 337–356.

    CAS  PubMed  Google Scholar 

  • Woese, C. R. (1994). There must be a prokaryote somewhere: microbiology’s search for itself. Microbiological Reviews, 58, 1–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Woese, C., & Fox, G. (1977). Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences of the United States of America, 74, 5088–5090.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wolf, J. B., Brodie, E. D., & Moore, A. J. (1999). Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. The American Naturalist, 153, 254–266.

    Google Scholar 

  • Wood, T. G. (1976). The role of termites (Isoptera) in decomposition processes. In J. M. Anderson (Ed.), The role of terrestrial and aquatic organisms in decomposition processes (pp. 145–168). Oxford: Blackwell.

    Google Scholar 

  • Woods, R. (1999). Reef evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Wynne-Edwards, V. C. (1963). Animal dispersion in relation to social behavior. Edinburg: Oliver and Boyd.

    Google Scholar 

  • Yildirim, S., Yeoman, C. J., Sipos, M., et al. (2010). Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. Plos One, 5, e13963.

    PubMed Central  PubMed  Google Scholar 

  • Yue, J., Hu, X., Huang, J. (2013). Horizontal gene transfer in the innovation and adaptation of land plants. Plant Signaling and Behavior , 8, e24130.1–e24130.3.

    Google Scholar 

  • Yue, J., Hu, X., Sun, H., et al. (2012). Widespread impact of horizontal gene transfer on plant colonization of land. Nature Communications, 3, 1152.

    PubMed Central  PubMed  Google Scholar 

  • Zamioudis, C., Mastranesti, P., Dhonukshe, P., et al. (2013). Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiology, 162, 304–318.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong, B., Liu, L., Yan, Z., & Penny, D. (2013). Origin of land plants using the multispecies coalescent model. Trends in Plant Science, 18, 492–495.

    CAS  PubMed  Google Scholar 

  • Zilber-Rosenberg, I., & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews, 32, 723–735.

    CAS  PubMed  Google Scholar 

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Rosenberg, E., Zilber-Rosenberg, I. (2013). The Evolution of Holobionts. In: The Hologenome Concept: Human, Animal and Plant Microbiota. Springer, Cham. https://doi.org/10.1007/978-3-319-04241-1_8

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