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Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution

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Abstract

Holobionts, consisting of a host and diverse microbial symbionts, function as distinct biological entities anatomically, metabolically, immunologically, and developmentally. Symbionts can be transmitted from parent to offspring by a variety of vertical and horizontal methods. Holobionts can be considered levels of selection in evolution because they are well-defined interactors, replicators/reproducers, and manifestors of adaptation. An initial mathematical model is presented to help understand how holobionts evolve. The model offered combines the processes of horizontal symbiont transfer, within-host symbiont proliferation, vertical symbiont transmission, and holobiont selection. The model offers equations for the population dynamics and evolution of holobionts whose hologenomes differ in gene copy number, not in allelic or loci identity. The model may readily be extended to include variation among holobionts in the gene identities of both symbionts and host.

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References

  • Addis M, Tanca A, Uzzau S et al (2016) The bovine milk microbiota: insights and perspectives from -omics studies. Mol Biosyst 19:2359–2372

    Article  Google Scholar 

  • Babcock RC, Bull GD, Harrison PL et al (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Marine Biol 90:379—394

    Article  Google Scholar 

  • Bailey JH, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett 9:78–85

    Google Scholar 

  • Baldo L, Riera JL, Tooming-Klunderud A et al (2015) Gut microbiota dynamics during dietary shift in eastern African cichlid fishes. PLoS ONE 10(5):e0127462. doi:10.1371/journal.pone.0127462

    Article  Google Scholar 

  • Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Evol Syst 36:621–642

    Article  Google Scholar 

  • Bascompte J, Jordano P (2006) The structure of plant-animal mutualistic networks. In: Pascual M, Dunne J (eds) Ecological networks. Oxford University Press, Oxford, pp 143–159

    Google Scholar 

  • Bastolla U, Fortuna MA, Pascual-García A et al (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018—1021

    Article  Google Scholar 

  • Bates JM, Mittge E, Kuhlman J et al (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297:374–386

    Article  Google Scholar 

  • Baumann P, Lai CY, Roubakhsh D et al (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera—intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94

    Article  Google Scholar 

  • Belkaid Y, Hand TW (2014) Role of microbiota in immunity and inflammation. Cell 157:121–141

    Article  Google Scholar 

  • Beltran-Garcia MJ, White JF Jr, Prado FM et al (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep. doi:10.1038/srep06938

    Google Scholar 

  • Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148

    Article  Google Scholar 

  • Birky CW Jr, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513–527

    Google Scholar 

  • Blum JE, Fischer CN, Miles J, Handelsman J (2013) Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio 4:e00860–e00813

    Article  Google Scholar 

  • Booth A (2014) Symbiosis, selection, and individuality. Biol Philos 29:657–673

    Article  Google Scholar 

  • Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226

    Article  Google Scholar 

  • Brandvain Y, Wade MJ (2009) The functional transfer of genes from the mitochondria to the nucleus: the effects of selection, mutation, population size and rate of self-fertilization. Genetics 182:1129–1139

    Article  Google Scholar 

  • Brandvain Y, Barker MS, Wade MJ (2007) Gene co-inheritance and gene transfer. Science 315:1685

    Article  Google Scholar 

  • Bronstein JL (2015) Mutualism. Oxford University Press, New York

    Book  Google Scholar 

  • Brown JS, Vincent TL (1987) Coevolution as an evolutionary game. Evol Int J Org Evol 41:66–79

    Article  Google Scholar 

  • Browne H, Forster SC, Anonye BO et al (2016) Culturing of “unculturable” human microbiota reveals novel taxa and extensive sporulation. Nature 533:543–546

    Article  Google Scholar 

  • Brucker RM, Bordenstein SR (2012) Speciation by symbiosis. Trends Ecol Evol 27:442–451

    Article  Google Scholar 

  • Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341(6146):667–669

    Article  Google Scholar 

  • Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166

    Article  Google Scholar 

  • Bull JJ, Molineux IJ, Rice WR (1991) Selection of benevolence in a host–parasite system. Evol Int J Org Evol 45:875–882

    Article  Google Scholar 

  • Camp JG, Frank CL, Lickwar CR et al (2014) Microbiota modulate transcription in the intestinal epithelium without remodeling the accessible chromatin landscape. Genome Res 24:1504–15016

    Article  Google Scholar 

  • Caporael L, Wimsatt W, Griesemer JR (eds) (2014) Developing scaffolds in evolution, culture, and cognition. MIT Press, Cambridge

    Google Scholar 

  • Carmona D, Fitzpatrick CR, Johnson MT (2015) Fifty years of co-evolution and beyond: integrating co-evolution from molecules to species. Mol Ecol 24:5315–5329

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Choo JM, Leong LEX, Rogers GB (2015) Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep. doi:10.1038/srep16350

    Google Scholar 

  • Chu H, Mazmanian SK (2013) Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nature Immunol 14:668–675

    Article  Google Scholar 

  • Colombo BM, Scalvenzi T, Benlamara S, Pollet N (2015) Microbiota and mucosal immunity in amphibians. Front Immunol. doi:10.3389/fimmu.2015.00111

    Google Scholar 

  • Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255—1262

    Article  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

    Google Scholar 

  • Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663—666

    Article  Google Scholar 

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  • Diaz Heijtz RD, Wang S, Anuar F et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052

    Article  Google Scholar 

  • Dieckmann U, Law R (1996) The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol 34:579–612

    Article  Google Scholar 

  • Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160(3):1087–1094

    Google Scholar 

  • Dominguez-Bello MG, Blaser MJ (2011) The human microbiota as a marker for migrations of individuals and populations. Annu Rev Anthropol 40:451–474

    Article  Google Scholar 

  • Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nature Rev Microbiol 14:20–32

    Article  Google Scholar 

  • Doolittle WF, Booth A (2017) It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos 32(1):5–24

    Article  Google Scholar 

  • Douglas AE (2010) The symbiotic habit. Princeton University Press, Princeton

    Google Scholar 

  • Douglas AE, Werren JH (2016) Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio 7(2):e02099-15. doi:10.1128/mBio.02099-15

    Article  Google Scholar 

  • Drake J (1991) Community-assembly mechanics and the structure of an experimental species ensemble. Am Nat 137:1–26

    Article  Google Scholar 

  • Drown DM, Wade MJ (2014) Runaway coevolution: adaptation to heritable and non-heritable environments. Evol Int J Org Evol 68:3039–3046

    Article  Google Scholar 

  • Drown DM, Zee PC, Brandvain Y, Wade MJ (2013) Evolution of transmission mode in obligate symbionts. Evol Ecol Res 15:43–59

    Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740

    Article  Google Scholar 

  • Dunbar HE, Wilson ACC, Ferguson NR, Moran NA (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5:e96

    Article  Google Scholar 

  • Dupre J (2010) The polygenomic organism. Sociol Rev 58(Supplement 1):19–31

    Article  Google Scholar 

  • Dupre J (2012) Post genomic Darwinism. In: Dupre J (ed) Processes of life: essays in the philosophy of biology. Oxford University Press, Oxford, pp 143–160

    Chapter  Google Scholar 

  • Dupre J, O’Malley M (2013) Variation of living things: life at the intersection of lineage and metabolism. In: Norman S, Wolfe CT (eds) Vitalism and the scientific age in post-enlightenment life science, 1800–2010. Springer, Dordrecht, pp 311–344

    Google Scholar 

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

    Article  Google Scholar 

  • Eberl G (2010) A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol 3:450–460

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Eisen J 2015. What does the term microbiome mean? And where did it come from? A bit of a surprise. http://microbe.net/2015/04/08. Accessed 5 April 2016

  • Ewald PW (1987) Transmission modes and evolution of the parasitism–mutualism continuum. Ann NY Acad Sci 503:295–306

    Article  Google Scholar 

  • Fell PE (1993) Reproductive biology of invertebrates. Asexual propagation and reproductive strategies. In: Adyodi KG, Adyodi RG (eds) Porifera. Wiley, Chichester, pp 1–44

    Google Scholar 

  • Fenn K, Blaxter M (2006) Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol 22(2):60–65

    Article  Google Scholar 

  • Fernández L, Langa S, Martína V et al (2013) The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 69:1–10

    Article  Google Scholar 

  • Fisher CK, Mehta P (2014) Identifying keystone species in the human gut microbiome from metagenomic timeseries using sparse linear regression. PLoS ONE 9(7):e102451. doi:10.1371/journal.pone.0102451

    Article  Google Scholar 

  • Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA 104:13146–13151

    Article  Google Scholar 

  • Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. Bioessays 32:571–580

    Article  Google Scholar 

  • Fukami T, Nakajima M (2011) Community assembly: alternative stable states or alternative transient states? Ecol Lett 14:973—984

    Article  Google Scholar 

  • Fullmer MS, Soucy SM, Gogarten JP. 2015. The pan-genome as a shared genomic resource: mutual cheating, cooperation and the black queen hypothesis. Front Microbiol. doi:10.3389/fmicb.2015.00728

    Google Scholar 

  • Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11(8):e1001631

    Article  Google Scholar 

  • Fussmann GF, Loreau M, Abrams PA (2007) Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21(3):465–477

    Article  Google Scholar 

  • Galtier Ni (2007) A model of horizontal gene transfer and the bacterial phylogeny problem. Syst Biol 56(4):633–642

    Article  Google Scholar 

  • Garrido D, Ruiz-Moyano S, Kirmiz N et al (2016) A novel gene cluster allows preferential utilization of fucosylated milk oligosaccharides in Bifidobacterium longum subsp. longum SC596. Sci Rep 6:35045. doi:10.1038/srep35045

    Article  Google Scholar 

  • Gause GF ([1934]1964) The struggle for existence. Hafner Press, New York

    Book  Google Scholar 

  • Gilbert SF (2003) The genome in its ecological context: philosophical perspectives on interspecies epigenesis. Ann N Y Acad Sci 981:202–218

    Article  Google Scholar 

  • Gilbert SF (2014) A holobiont birth narrative: the epigenetic transmission of the human microbiome. Front Genet 5:282. doi:10.3389/fgene.2014.00282

    Article  Google Scholar 

  • Gilbert SF, Epel D (2015) Ecological developmental biology: the developmental integration of evolution, development, and medicine. Sinauer, Sunderland

    Google Scholar 

  • Gilbert SF, McDonald E, Boyle N et al (2010) Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos Trans R Soc Lond B 365(1540):671–678

    Article  Google Scholar 

  • Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341

    Article  Google Scholar 

  • Gilbert SF, Rosenberg E, Zilber-Rosenberg I (2018) The holobiont with its hologenome is a level of selection in evolution. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. Vienna series in theoretical biology. MIT Press, Cambridge

    Google Scholar 

  • Gill SR, Pop M, Deboy RT et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359

    Article  Google Scholar 

  • Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, Oxford

    Book  Google Scholar 

  • Godfrey-Smith P (2011) Agents and acacias: replies to Dennett, Sterelny, and Queller. Biol Philos. doi:10.1007/s10539=011=9246-6

    Google Scholar 

  • Goodnight CJ (1990a) Experimental studies of community evolution I: the response to selection at the community level. Evol Int J Org Evol 44:1614–1624

    Article  Google Scholar 

  • Goodnight CJ (1990b) Experimental studies of community evolution II: The ecological basis of the response to community selection. Evol Int J Org Evol 44:1625–1636

    Article  Google Scholar 

  • Goodnight CJ (2005) Multilevel selection: the evolution of cooperation in non-kin groups. Popul Ecol 47(1):3–12

    Article  Google Scholar 

  • Goodnight CJ (2013a) On multilevel selection and kin selection: contextual analysis meets direct fitness. Evolution 67:1539–1548

    Article  Google Scholar 

  • Goodnight, CJ (2013b) Defining the individual. In: Bouchard F, Huneman P (eds) From groups to individuals. MIT Press, Cambridge, pp 37–54

    Google Scholar 

  • Goodnight CJ, Schwartz JM, Stevens L (1992) Contextual analysis of models of group selection, soft selection, hard selection and the evolution of altruism. Am Nat 140:743–761

    Article  Google Scholar 

  • Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253

    Article  Google Scholar 

  • Griesemer J (2000a) Development, culture and the units of inheritance. Philos Sci 67:S348–S368

    Article  Google Scholar 

  • Griesemer J (2000b) The units of evolutionary transition. Selection 1:67–80

    Article  Google Scholar 

  • Griesemer JR (2005) The informational gene and the substantial body: on the generalization of evolutionary theory by abstraction. In: Jones MR, Cartwright N (eds) Idealization XII: correcting the model. Idealization and abstraction in the sciences. Pozna! studies in the philosophy of the science and the humanities, vol 86. Rodopi, Amsterdam/New York, pp 59–115

    Chapter  Google Scholar 

  • Griesemer J (2014a) Reproduction and the scaffolded development of hybrids. In: Caporael LR, Griesemer JR, Wimsatt WC (eds) Developing scaffolds in evolution, culture, and cognition. MIT Press, Cambridge, pp 23–55

    Google Scholar 

  • Griesemer J (2014b) Reproduction and scaffolded developmental processes: an integrated evolutionary perspective. In: Minelli A, Pradeu T (eds) Towards a theory of development. Oxford University Press, Oxford, pp 183–202

    Chapter  Google Scholar 

  • Griesemer JR (2016) Reproduction in complex life cycles: toward a developmental reaction norms perspective. Philos Sci 83.5:803–815

    Article  Google Scholar 

  • Hart MW (2002) Life history evolution and comparative developmental biology of echinoderms. Evol Dev 4:62–71

    Article  Google Scholar 

  • Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702–702

    Article  Google Scholar 

  • Hehemann JH, Correc G, Barbeyron T et al (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–914

    Article  Google Scholar 

  • Hehemann JH, Kelly AG, Pudlo NA et al (2012) Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci USA 109:19786–19791

    Article  Google Scholar 

  • Heisler IL, Damuth J (1987) A method for analyzing selection in hierarchically structured populations. Am Nat 130(4):582–602

    Article  Google Scholar 

  • Hester ER, Barott KL, Nulton J et al (2016) Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. doi:10.1038/ismej.2015.190

    Google Scholar 

  • Hill JH, Franzosa EA, Huttenhower C, Guillemin K (2016) A conserved bacterial protein induces pancreatic beta cell expansion during zebrafish development. eLife 5:e20145

    Article  Google Scholar 

  • Hirose M, Hidaka M (2006) Early development of zooxanthella-containing eggs of the corals, Porites cylindirica and Montipora digitata: The endodermal localization of zooxanthellae. Zool Sci 23:873–881

    Article  Google Scholar 

  • Hodgson S, Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208

    Article  Google Scholar 

  • Hooper LV, Wong MH, Thelin A et al (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884

    Article  Google Scholar 

  • Hubbell S (2001) The unified neutral theory of biodiversity and biogeography. Monographs in population biology 32. Princeton University Press, Princeton

    Google Scholar 

  • Hull DL (1980) Individuality and selection. Annu Rev Ecol Syst 11:311–332

    Article  Google Scholar 

  • Hunt KM, Foster JA, Forney LJ et al (2011) Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 6:e21313

    Article  Google Scholar 

  • Huxley TH (1852) Upon animal individuality. Edinb New Philos J 53:172–177

    Google Scholar 

  • Inoue R, Ushida K (2003) Vertical and horizontal transmission of intestinal commensal bacteria in the rat model. FEMS Microbiol Ecol 46:213–219

    Article  Google Scholar 

  • Jin L, Hinde K, Tao L (2011) Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta). J Med Primatol 40:52–58

    Article  Google Scholar 

  • Jones EI, Afkhami ME, Akçay E et al (2015) Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism. Ecol Lett 18(11):1270–1284

    Article  Google Scholar 

  • Jost T, Lacroix C, Braesier C, Chassard C (2013) Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr 14:1–10

    Google Scholar 

  • Kikuchi Y, Hayatsu M, Hosikawa T et al (2012) Symbiont-mediated insecticide resistance. Proc Nat Acad Sci USA 109:8618–8622

    Article  Google Scholar 

  • Klein J (1982) Immunology: the science of self-nonself discrimination. Wiley, New York

    Google Scholar 

  • Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62

    Article  Google Scholar 

  • Koren O, Goodrich JK, Cullender TC et al (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150:470–480

    Article  Google Scholar 

  • Kort R, Caspers M, van de Graaf A et al (2014) Shaping the oral microbiota through intimate kissing. Microbiome 2:41

    Article  Google Scholar 

  • Kovacs M, Szendro Z, Milisits G et al (2006) Effect of nursing methods and feces consumption on the development of bacteroides, lactobacillus and coliform flora in the caecum of the newborn rabbits. Reprod Nutr Dev 46:205–210

    Article  Google Scholar 

  • Laland KN, Odling-Smee J, Gilbert SF (2008) Evo-Devo and niche construction: building bridges. J Exp Zool 310:549–566

    Article  Google Scholar 

  • Laland K, Odling-Smee J, Turner S (2014) The role of internal and external constructive processes in evolution. J Physiol 592(11):2413–2422

    Article  Google Scholar 

  • Landmann F, Foster JM, Michalski ML (2014) Co-evolution between a nematode and its nematode host: Wolbachia asymmetric localization and A-P polarity establishment. PLoS Negl Dis 8(8):e3096

    Article  Google Scholar 

  • Lanning DK, Rhee KJ, Knight KL (2005) Intestinal bacteria and development of the B-lymphocyte repertoire. Trends Immunology 26:419–425

    Article  Google Scholar 

  • Leclercq S, Thézé J, Chebbi MA et al (2016) Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proc Natl Acad Sci USA 113:15036–15041

    Article  Google Scholar 

  • Lederberg J, McCray AT (2001) ‘Ome sweet ‘omics—a genealogical treasury of words. The Scientist 15:8

    Google Scholar 

  • Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768–1773

    Article  Google Scholar 

  • Lee OO, Chui PY, Wong YH et al (2009) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microbiol 75:6147–6156

    Article  Google Scholar 

  • Lewontin RC (1978) Adaptation. Sci Am 239:156–169

    Article  Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell: 124:837–848

    Article  Google Scholar 

  • Ley RE, Lozupone CA, Hamady M et al (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788

    Article  Google Scholar 

  • Linaje R, Coloma MD, Perez-Martınez G et al (2004) Characterization of faecal enterococci from rabbits for the selection of probiotic strains. J Appl Microbiol 96:761–771

    Article  Google Scholar 

  • Lloyd EA (1992) Unit of selection. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, Cambridge

    Google Scholar 

  • Lloyd EA (2001) Units and levels of selection: an anatomy of the units of selection debates. In: Singh R, Krimbas C, Paul D, Beatty J (eds) Thinking about evolution: historical, philosophical and political perspectives. Cambridge University Press, Cambridge, pp 267–291

    Google Scholar 

  • Lloyd EA (2017) Units and levels of selection. In: Zalta EN (ed) Stanford encyclopedia of philosophy. http://www.plato.stanford.edu/entries/selection-units

  • Lloyd EA (2018) Holobionts as units of selection: holobionts as interactors, reproducers, and manifestors of adaptation. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. Vienna series in theoretical biology. MIT Press, Cambridge

    Google Scholar 

  • Lloyd E, Lewontin RC, Feldman MW (2008) The generational cycle of state spaces and adequate genetical representation. Philos Sci 75(2):140–156

    Article  Google Scholar 

  • Lozupone CA, Stombaugh JI, Gordon JI et al (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230

    Article  Google Scholar 

  • MacDonald SJ, Thomas GH, Douglas AE (2011) Genetic and metabolic determinants of nutritional phenotype in an insect-bacterial symbiosis. Mol Ecol 20:2073–2084

    Article  Google Scholar 

  • Macke E, Tasiemski A, Massol F et al (2017) Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos 126:508–531

    Article  Google Scholar 

  • Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S-1045S

    Google Scholar 

  • Margulis L, Sagan D (2001) The beast with five genomes. Nat Hist 110:3

    Google Scholar 

  • Matsuura Y, Kikuchi Y, Miura T, Fukatsu T (2015) Ultrabithorax is essential for bacteriocyte development. Proc Natl Acad Sci USA 112:9376–9381

    Article  Google Scholar 

  • Maynard Smith J (1987) Evolutionary progress and levels of selection. In: Dupre J (ed) The latest on the best: essays on evolution and optimality. MIT Press, Cambridge

    Google Scholar 

  • McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372

    Article  Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TC et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236

    Article  Google Scholar 

  • McInerney JO, Pisani D, Bapteste E, O’Connell MJ (2011) The public goods hypothesis for the evolution of life on earth. Biol Direct 6:41

    Article  Google Scholar 

  • Meiklejohn CD, Montooth KL, Rand DM (2007) Positive and negative selection on the mitochondrial genome. Trends Genet 23:259–263

    Article  Google Scholar 

  • Milani C, Mancabelli L, Lugli GA et al (2015) Exploring vertical transmission of Bifidobacteria from mother to child. Appl Environ Microbiol 81:7078–7087

    Article  Google Scholar 

  • Moeller AH, Caro-Quintero A, Mjungu D et al (2016) Co-speciation of gut microbiota with hominids. Science 353:380–382

    Article  Google Scholar 

  • Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13(12):e1002311

    Article  Google Scholar 

  • Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci USA 112:2093–2096

    Article  Google Scholar 

  • Mounier J, Monnet C, Vallaeys T et al (2008) Microbial interactions within a cheese microbial community. Appl Environ Microbiol 74:172–181

    Article  Google Scholar 

  • Mueller NT, Bakacs E, Combellick J et al (2014) The infant microbiome development: mom matters. Trends Mol Med 21:109–117

    Article  Google Scholar 

  • Muscatine L, Falkowski PG, Porter W, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222:181–202

    Article  Google Scholar 

  • Nayfach S, Rodriguez-Mueller B, Garud N, Pollard KS (2016) An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res 26:1612–1625

    Article  Google Scholar 

  • Nicholson JK, Holmes E, Kinross J et al (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267

    Article  Google Scholar 

  • Nikoh N, Tanaka K, Shibata F et al (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18:272–280

    Article  Google Scholar 

  • Nikoh N, Hosokawa T, Moriyama M et al (2014) Evolutionary origin of insect–Wolbachia nutritional mutualism. Proc Natl Acad Sci USA 111(28):10257–10262

    Article  Google Scholar 

  • Nuriel-Ohayon M, Neuman H, Koren O (2016) Microbial changes during pregnancy, birth, and infancy. Front Microbiol 7:1031

    Article  Google Scholar 

  • Nyholm SV, Stewart JJ, Ruby EG et al (2008) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11:483–493

    Article  Google Scholar 

  • Ochman H, Worobey M, Kuo CH et al (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8(11):e1000546. doi:10.1371/journal.pbio.1000546

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution (No. 37). Princeton University Press, Princeton

    Google Scholar 

  • Ohnmacht C, Park JH, Cording S et al (2015) The microbiota regulates type 2 immunity through RORγt+ T cells. Science 349(6251):989–993

    Article  Google Scholar 

  • Okasha S (2006) Evolution and the levels of selection. Oxford University Press, Oxford

    Book  Google Scholar 

  • Oldroyd GE, D. JD, Murray PS, Poole, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Gen 45:119–144

    Article  Google Scholar 

  • Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994

    Article  Google Scholar 

  • Osawa R, Blanshard WH, Ocallaghan PG (1993) Microbiological studies of the intestinal microflora of the koala, Phascolarctos cinereus. II. Pap, a special maternal feces consumed by juvenile koalas. Aust J Zool 41:611–620

    Article  Google Scholar 

  • Osmanovic D, Kessler DA, Rabin Y, Soen Y (2017) Darwinian selection induces lamarckian adaptation in a holobiont model. arXiv preprint arXiv:1612.03567

  • Pannebakker BA, Loppin B, Elemans CP. H. et al (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci USA 104:213–215

    Article  Google Scholar 

  • Peterson DA, Planer JD, Guruge JL et al (2015) Characterizing the interactions between a naturally primed immunoglobulin A and its conserved Bacteroides thetaiotaomicron species-specific epitope in gnotobiotic mice. J Biol Chem 290:12630–12649

    Article  Google Scholar 

  • Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29(3):170–175

    Article  Google Scholar 

  • Pradeu T (2012) The limits of the self: immunology and biological identity. Oxford University Press, New York

    Book  Google Scholar 

  • Rand DM, Hane RA, Fry AJ (2004) Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 19:645–653

    Article  Google Scholar 

  • Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101:4596–4601

    Article  Google Scholar 

  • Relman DA (2012) The human microbiome: ecosystem resilience and health. Nutr Rev 70:S2–S9

    Article  Google Scholar 

  • Rezende EL, Lavabre JE, Guimares PR (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature: 448:925–928

    Article  Google Scholar 

  • Rhee KJ, Sethupathi P, Driks A, Lanning DK, Knight KL (2004) Role of commensal bacteria in development of gut-associated lymphoid tissue and preimmune antibody repertoire. J Immunol 172:1118–1124

    Article  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Rosenberg E, Zilber-Rosenberg I (2011) Symbiosis and development: the hologenome concept. Birth Defects Res C 93:56–66

    Article  Google Scholar 

  • Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. MBio 7(2):e01395-15. doi:10.1128/mBio.01395-15

    Article  Google Scholar 

  • Rosenberg E, Koren O, Reshef L et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  Google Scholar 

  • Rosner JL (2014) Ten times more microbial cells than body cells in humans? Microbe 9:47

    Google Scholar 

  • Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422. doi:10.3389/fmicb.2014.00422

    Article  Google Scholar 

  • Roughgarden J (1983) The theory of coevolution. In: Futuyma DJ, Slatkin M (eds) Coevolution. Sinauer, Sunderland, pp 33–64

    Google Scholar 

  • Roughgarden J (1998) Primer of ecological theory. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Roughgarden J (2018a) Incentivizing biological cooperation: approaches from the economic theory of the firm. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. Vienna series in theoretical biology. MIT Press, Cambridge

    Google Scholar 

  • Roughgarden J (2018b) Model of holobiont population dynamics and evolution: a preliminary sketch. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. Vienna series in theoretical biology. MIT Press, Cambridge

    Google Scholar 

  • Round JL, Lee SM, Li J et al (2011) The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974–977

    Article  Google Scholar 

  • Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2010) The making of a photosynthetic animal. J Exp Biol 214:303–311

    Article  Google Scholar 

  • Russell JB, Muck RE, Weimer PJ (2009) Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen. FEMS Microbiol Ecol 67:183–197

    Article  Google Scholar 

  • Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79(2):135–160

    Article  Google Scholar 

  • Sachs JL, Skophammer RG, Bansal N, Stajich JE (2014). Evolutionary origins and diversification of proteobacterial mutualists. Proc R Soc B 281(1775):20132146

    Article  Google Scholar 

  • Sakwinska O, Moine D, Delley M et al (2016) Microbiota in breast milk of Chinese lactating mothers. PLoS ONE 11(8):e0160856. doi:10.1371/journal.pone.0160856

    Article  Google Scholar 

  • Sanders JG, Powell S, Kronauer DJ et al (2014) Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 23:1268–1283

    Article  Google Scholar 

  • Schluter J, Foster KR (2012) The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol 10(11):e1001424

  • Sefik E, Geva-Zatorsky N, Oh S et al (2015) Individual intestinal symbionts induce a distinct population of RORγ+ regulatory T cells. Science 349:993–997

    Article  Google Scholar 

  • Sekirov I, Russell SL, Antunes CM et al (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  Google Scholar 

  • Sela DA, Li Y, Lerno L et al (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem 286:11909–11918

    Article  Google Scholar 

  • Sender R, Fuchs S, Milo R (2016) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–340

    Article  Google Scholar 

  • Sharon G, Segal D, Ringo JM et al (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107:20051–20056

    Article  Google Scholar 

  • Shuster SM, Lonsdorf EV, Wimp GM et al (2006) Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evol Int J Org Evol 60:991–1003

    Article  Google Scholar 

  • Sipkema D, de Caralt S, Morillo JA et al (2015) Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission. Environ Microbiol 10:3807–3821

    Article  Google Scholar 

  • Smith J (2007) A gene’s-eye view of symbiont transmission. Am Nat 170:542–550

    Article  Google Scholar 

  • Soen Y (2014) Environmental disruption of host-microbe co-adaptation as a potential driving force in evolution. Front Genet 5:168

    Article  Google Scholar 

  • Sofonea MT, Alizon S, Michalakis Y (2015) From within-host interactions to epidemiological competition: a general model for multiple infections. Philos Trans R Soc Lond Ser B Biol Sci 370:20140303

    Article  Google Scholar 

  • Song SJ, Lauber C, Costello EK et al (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458

    Google Scholar 

  • Stanley D, Geier MS, Chen H et al (2015) Comparison of fecal and cecal microbiotas reveals qualitative similarities but quantitative differences. BMC Microbiol 15:51. doi:10.1186/s12866-015-0388-6

    Article  Google Scholar 

  • Stein RR, Bucci V, Toussaint NC et al (2013) Ecological modeling from time-series inference: insight into dynamics and stability of intestinal microbiota. PLoS Comput Biol 9:e1003388. doi:10.1371/journal.pcbi.1003388

    Article  Google Scholar 

  • Sterelny K (2011) Darwinian spaces: Peter Godfrey-Smith on selection and evolution. Biol Philos 26:489–500

    Article  Google Scholar 

  • Tadych M, Bergen MS, White JF (2014) Epichloë spp. associated with grasses: new insights on life cycles, dissemination and evolution. Mycologia 106:181–201

    Article  Google Scholar 

  • Tago K, Kikuchi Y, Nakaoka S et al (2015) Insecticide applications to soil contribute the development of Burkholderia mediating insecticide resistance in stinkbugs. Mol Ecol 24:3766–3778

    Article  Google Scholar 

  • Tauber AI 2009. The biological notion of self and non-self. In: Zelta EN (ed) Stanford encyclopedia of philosophy. http://plato.stanford.edu/entries/biologyself/

  • Teixeira L, Ferreira Á., Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12):.e1000002

    Article  Google Scholar 

  • Theis KR, Dheilly NM, Klassen et al. (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems. doi:10.1128/mSystems.00028-16

    Google Scholar 

  • Trench RK (1993) Microalgal-invertebrate symbioses: a review. Endocytobiosis Cell Res 9:135–175

    Google Scholar 

  • Tsuchida T, Koga R, Horikawa M et al (2010) Symbiotic bacterium modifies aphid body color. Science 330:1102–1104

    Article  Google Scholar 

  • van Opstal EJ, Bordenstein SR (2015) Rethinking heritability of the microbiome. Science 349:1172–1173

    Article  Google Scholar 

  • Vandermeer J (1969) The competitive structure of communities: an experimental approach with protozoa. Ecology 50:362–371

    Article  Google Scholar 

  • Vaughn D (2010) Why run and hide when you can divide? Evidence for larval cloning and reduced larval size as an adaptive inducible defense. Mar Biol 15:1301–1312

    Article  Google Scholar 

  • Veneti Z, Clark ME, Karr TL et al (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70:5366–5372

    Article  Google Scholar 

  • Wade MJ (2007) The co-evolutionary genetics of ecological communities. Nat Rev Genet 8:185–195

    Article  Google Scholar 

  • Wade MJ (2014) Paradox of mother’s curse and the maternally provisioned offspring microbiome. In: Rice WR, Gavrilets S (eds) Additional perspectives on sexual conflict. Cold Spring Harbor Perspectives in Biology, New York. doi:10.1101/cshperspect.a017541

    Google Scholar 

  • Wade MJ (2016) Adaptations in metapopulations. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Wade M, Drown DM (2016) Nuclear-mitochondrial epistasis: a gene’s view of genomic conflict. Ecol Evol 6:6460–6472

    Article  Google Scholar 

  • Wade MJ, Goodnight CJ (2006) Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species. Evol Int J Org Evol 60:643–659

    Article  Google Scholar 

  • Wagner GP, Kin K, Muglia L, Pavlicev M (2014) Evolution of mammalian pregnancy and the origin of the decidual stromal cell. Int J Dev Biol 58:117–126

    Article  Google Scholar 

  • Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632

    Article  Google Scholar 

  • Weeks AR, Turelli M, Harcombe WR et al (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5(5):.e114

    Article  Google Scholar 

  • Weiblen GD, Treiber EL (2015) Evolutionary origins and diversification of mutualism. Mutualism. Oxford University Press, Oxford, pp 37–56

    Google Scholar 

  • Wesemann DR, Portuguese AJ, Meyers RM et al (2013) Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 501:112–115

    Article  Google Scholar 

  • West-Eberhard M-J (1992) Adaptation: current uses. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, Cambridge

    Google Scholar 

  • Whipps JM, Lewis K, Cooke RC (1988) Mycoparasitism and plant disease control. In Burge NM (ed) Fungi in biological control systems. Manchester University Press, Manchester, pp 161–187

    Google Scholar 

  • Whitham TG, Bailey JK, Schweitze JA et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Gen 7:510–523

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Wilson DS (1980) The natural selection of populations and communities. Benjamin/Cummings Publishing, Menlo Park

    Google Scholar 

  • Yano JM, Yu K, Donaldson GP et al (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276

    Article  Google Scholar 

  • Yildirim S, Yeoman CJ, Sipos M et al (2010) Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS ONE 5:e13963

    Article  Google Scholar 

  • Ying H, Zeng D, Chi L et al (2015) The influence of age and gender on skin-associated microbial communities in urban and rural human populations. PLoS ONE 10(10):e0141842

    Article  Google Scholar 

  • Yoshida E, Sakurama H, Kiyohara M et al (2012) Bifidobacterium longum subsp.infantis uses two different β- type-2 human milk oligosaccharides. Glycobiology 22:361–368

    Article  Google Scholar 

  • Zeng Q, Sukumaran J, Wu S, Rodrigo A (2015) Neutral models of microbiome evolution. PLoS Comput Biol 11(7):e1004365. doi:10.1371/journal.pcbi.1004365

    Article  Google Scholar 

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

    Article  Google Scholar 

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Acknowledgements

We thank Snait Gissis, Ehud Lamm, and Ayelet Shavit for organizing a workshop that brought the authors of this manuscript together and for their encouragement and helpful comments on the manuscript. We also thank Michael Wade, John Dupre, James Griesemer, Oren Kolodny, Marcus Feldman, Tadashi Fukami, and three anonymous reviewers for helpful suggestions. SG is funded by NSF Grant IOS 145177. JR was funded by The John Templeton Foundation Grant 51473.

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Roughgarden, J., Gilbert, S.F., Rosenberg, E. et al. Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution. Biol Theory 13, 44–65 (2018). https://doi.org/10.1007/s13752-017-0287-1

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