Biological Theory

, Volume 13, Issue 1, pp 44–65 | Cite as

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

  • Joan Roughgarden
  • Scott F. Gilbert
  • Eugene Rosenberg
  • Ilana Zilber-Rosenberg
  • Elisabeth A. Lloyd
Original Article


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.


Holobiont Holobiont model Hologenome Level of selection Microbiome Microbiota Symbiont 



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.

Supplementary material

13752_2017_287_MOESM1_ESM.pdf (448 kb)
Supplementary material 1 (PDF 448 KB)


  1. Addis M, Tanca A, Uzzau S et al (2016) The bovine milk microbiota: insights and perspectives from -omics studies. Mol Biosyst 19:2359–2372CrossRefGoogle Scholar
  2. 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—394CrossRefGoogle Scholar
  3. 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 9:78–85Google Scholar
  4. 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 CrossRefGoogle Scholar
  5. Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Evol Syst 36:621–642CrossRefGoogle Scholar
  6. 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 143–159Google Scholar
  7. Bastolla U, Fortuna MA, Pascual-García A et al (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018—1021CrossRefGoogle Scholar
  8. Bates JM, Mittge E, Kuhlman J et al (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297:374–386CrossRefGoogle Scholar
  9. 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 49:55–94CrossRefGoogle Scholar
  10. Belkaid Y, Hand TW (2014) Role of microbiota in immunity and inflammation. Cell 157:121–141CrossRefGoogle Scholar
  11. 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
  12. Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148CrossRefGoogle Scholar
  13. 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 103:513–527Google Scholar
  14. Blum JE, Fischer CN, Miles J, Handelsman J (2013) Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio 4:e00860–e00813CrossRefGoogle Scholar
  15. Booth A (2014) Symbiosis, selection, and individuality. Biol Philos 29:657–673CrossRefGoogle Scholar
  16. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226CrossRefGoogle Scholar
  17. 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 182:1129–1139CrossRefGoogle Scholar
  18. Brandvain Y, Barker MS, Wade MJ (2007) Gene co-inheritance and gene transfer. Science 315:1685CrossRefGoogle Scholar
  19. Bronstein JL (2015) Mutualism. Oxford University Press, New YorkCrossRefGoogle Scholar
  20. Brown JS, Vincent TL (1987) Coevolution as an evolutionary game. Evol Int J Org Evol 41:66–79CrossRefGoogle Scholar
  21. Browne H, Forster SC, Anonye BO et al (2016) Culturing of “unculturable” human microbiota reveals novel taxa and extensive sporulation. Nature 533:543–546CrossRefGoogle Scholar
  22. Brucker RM, Bordenstein SR (2012) Speciation by symbiosis. Trends Ecol Evol 27:442–451CrossRefGoogle Scholar
  23. Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341(6146):667–669CrossRefGoogle Scholar
  24. Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166CrossRefGoogle Scholar
  25. Bull JJ, Molineux IJ, Rice WR (1991) Selection of benevolence in a host–parasite system. Evol Int J Org Evol 45:875–882CrossRefGoogle Scholar
  26. Camp JG, Frank CL, Lickwar CR et al (2014) Microbiota modulate transcription in the intestinal epithelium without remodeling the accessible chromatin landscape. Genome Res 24:1504–15016CrossRefGoogle Scholar
  27. Caporael L, Wimsatt W, Griesemer JR (eds) (2014) Developing scaffolds in evolution, culture, and cognition. MIT Press, CambridgeGoogle Scholar
  28. Carmona D, Fitzpatrick CR, Johnson MT (2015) Fifty years of co-evolution and beyond: integrating co-evolution from molecules to species. Mol Ecol 24:5315–5329CrossRefGoogle Scholar
  29. Chiu L, Gilbert SF (2015) The birth of the holobiont: multi-species birthing through mutual scaffolding and niche construction. Biosemiotics 8:191–210CrossRefGoogle Scholar
  30. Choo JM, Leong LEX, Rogers GB (2015) Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep. doi: 10.1038/srep16350 Google Scholar
  31. Chu H, Mazmanian SK (2013) Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nature Immunol 14:668–675CrossRefGoogle Scholar
  32. 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
  33. Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255—1262CrossRefGoogle Scholar
  34. Coyne JA, Orr HA (2004) Speciation. Sinauer, SunderlandGoogle Scholar
  35. Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350:663—666CrossRefGoogle Scholar
  36. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  37. Diaz Heijtz RD, Wang S, Anuar F et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108:3047–3052CrossRefGoogle Scholar
  38. Dieckmann U, Law R (1996) The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol 34:579–612CrossRefGoogle Scholar
  39. Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160(3):1087–1094Google Scholar
  40. Dominguez-Bello MG, Blaser MJ (2011) The human microbiota as a marker for migrations of individuals and populations. Annu Rev Anthropol 40:451–474CrossRefGoogle Scholar
  41. Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nature Rev Microbiol 14:20–32CrossRefGoogle Scholar
  42. Doolittle WF, Booth A (2017) It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos 32(1):5–24CrossRefGoogle Scholar
  43. Douglas AE (2010) The symbiotic habit. Princeton University Press, PrincetonGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Drake J (1991) Community-assembly mechanics and the structure of an experimental species ensemble. Am Nat 137:1–26CrossRefGoogle Scholar
  46. Drown DM, Wade MJ (2014) Runaway coevolution: adaptation to heritable and non-heritable environments. Evol Int J Org Evol 68:3039–3046CrossRefGoogle Scholar
  47. Drown DM, Zee PC, Brandvain Y, Wade MJ (2013) Evolution of transmission mode in obligate symbionts. Evol Ecol Res 15:43–59Google Scholar
  48. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740CrossRefGoogle Scholar
  49. Dunbar HE, Wilson ACC, Ferguson NR, Moran NA (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5:e96CrossRefGoogle Scholar
  50. Dupre J (2010) The polygenomic organism. Sociol Rev 58(Supplement 1):19–31CrossRefGoogle Scholar
  51. Dupre J (2012) Post genomic Darwinism. In: Dupre J (ed) Processes of life: essays in the philosophy of biology. Oxford University Press, Oxford, pp 143–160CrossRefGoogle Scholar
  52. 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 311–344Google Scholar
  53. Dupressoir A, Lavialle C, Heidmann T (2012) From ancestral infectious retroviruses to bona fide cellular genes: role of the syncytins in placentation. Placenta 33:663–671CrossRefGoogle Scholar
  54. Eberl G (2010) A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol 3:450–460CrossRefGoogle Scholar
  55. Ebert D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst 44:623–643CrossRefGoogle Scholar
  56. Eisen J 2015. What does the term microbiome mean? And where did it come from? A bit of a surprise. Accessed 5 April 2016
  57. Ewald PW (1987) Transmission modes and evolution of the parasitism–mutualism continuum. Ann NY Acad Sci 503:295–306CrossRefGoogle Scholar
  58. Fell PE (1993) Reproductive biology of invertebrates. Asexual propagation and reproductive strategies. In: Adyodi KG, Adyodi RG (eds) Porifera. Wiley, Chichester, pp 1–44Google Scholar
  59. Fenn K, Blaxter M (2006) Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol 22(2):60–65CrossRefGoogle Scholar
  60. Fernández L, Langa S, Martína V et al (2013) The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 69:1–10CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA 104:13146–13151CrossRefGoogle Scholar
  63. Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. Bioessays 32:571–580CrossRefGoogle Scholar
  64. Fukami T, Nakajima M (2011) Community assembly: alternative stable states or alternative transient states? Ecol Lett 14:973—984CrossRefGoogle Scholar
  65. 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
  66. Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11(8):e1001631CrossRefGoogle Scholar
  67. Fussmann GF, Loreau M, Abrams PA (2007) Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21(3):465–477CrossRefGoogle Scholar
  68. Galtier Ni (2007) A model of horizontal gene transfer and the bacterial phylogeny problem. Syst Biol 56(4):633–642CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. Gause GF ([1934]1964) The struggle for existence. Hafner Press, New YorkCrossRefGoogle Scholar
  71. Gilbert SF (2003) The genome in its ecological context: philosophical perspectives on interspecies epigenesis. Ann N Y Acad Sci 981:202–218CrossRefGoogle Scholar
  72. Gilbert SF (2014) A holobiont birth narrative: the epigenetic transmission of the human microbiome. Front Genet 5:282. doi: 10.3389/fgene.2014.00282 CrossRefGoogle Scholar
  73. Gilbert SF, Epel D (2015) Ecological developmental biology: the developmental integration of evolution, development, and medicine. Sinauer, SunderlandGoogle Scholar
  74. 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):671–678CrossRefGoogle Scholar
  75. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341CrossRefGoogle Scholar
  76. 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, CambridgeGoogle Scholar
  77. Gill SR, Pop M, Deboy RT et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359CrossRefGoogle Scholar
  78. Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, OxfordCrossRefGoogle Scholar
  79. Godfrey-Smith P (2011) Agents and acacias: replies to Dennett, Sterelny, and Queller. Biol Philos. doi: 10.1007/s10539=011=9246-6 Google Scholar
  80. Goodnight CJ (1990a) Experimental studies of community evolution I: the response to selection at the community level. Evol Int J Org Evol 44:1614–1624CrossRefGoogle Scholar
  81. Goodnight CJ (1990b) Experimental studies of community evolution II: The ecological basis of the response to community selection. Evol Int J Org Evol 44:1625–1636CrossRefGoogle Scholar
  82. Goodnight CJ (2005) Multilevel selection: the evolution of cooperation in non-kin groups. Popul Ecol 47(1):3–12CrossRefGoogle Scholar
  83. Goodnight CJ (2013a) On multilevel selection and kin selection: contextual analysis meets direct fitness. Evolution 67:1539–1548CrossRefGoogle Scholar
  84. Goodnight, CJ (2013b) Defining the individual. In: Bouchard F, Huneman P (eds) From groups to individuals. MIT Press, Cambridge, pp 37–54Google Scholar
  85. 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 140:743–761CrossRefGoogle Scholar
  86. Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253CrossRefGoogle Scholar
  87. Griesemer J (2000a) Development, culture and the units of inheritance. Philos Sci 67:S348–S368CrossRefGoogle Scholar
  88. Griesemer J (2000b) The units of evolutionary transition. Selection 1:67–80CrossRefGoogle Scholar
  89. 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 59–115CrossRefGoogle Scholar
  90. 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 23–55Google Scholar
  91. 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 183–202CrossRefGoogle Scholar
  92. Griesemer JR (2016) Reproduction in complex life cycles: toward a developmental reaction norms perspective. Philos Sci 83.5:803–815CrossRefGoogle Scholar
  93. Hart MW (2002) Life history evolution and comparative developmental biology of echinoderms. Evol Dev 4:62–71CrossRefGoogle Scholar
  94. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702–702CrossRefGoogle Scholar
  95. Hehemann JH, Correc G, Barbeyron T et al (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–914CrossRefGoogle Scholar
  96. 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 109:19786–19791CrossRefGoogle Scholar
  97. Heisler IL, Damuth J (1987) A method for analyzing selection in hierarchically structured populations. Am Nat 130(4):582–602CrossRefGoogle Scholar
  98. 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
  99. Hill JH, Franzosa EA, Huttenhower C, Guillemin K (2016) A conserved bacterial protein induces pancreatic beta cell expansion during zebrafish development. eLife 5:e20145CrossRefGoogle Scholar
  100. 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 23:873–881CrossRefGoogle Scholar
  101. Hodgson S, Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4:1199–1208CrossRefGoogle Scholar
  102. Hooper LV, Wong MH, Thelin A et al (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884CrossRefGoogle Scholar
  103. Hubbell S (2001) The unified neutral theory of biodiversity and biogeography. Monographs in population biology 32. Princeton University Press, PrincetonGoogle Scholar
  104. Hull DL (1980) Individuality and selection. Annu Rev Ecol Syst 11:311–332CrossRefGoogle Scholar
  105. 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:e21313CrossRefGoogle Scholar
  106. Huxley TH (1852) Upon animal individuality. Edinb New Philos J 53:172–177Google Scholar
  107. Inoue R, Ushida K (2003) Vertical and horizontal transmission of intestinal commensal bacteria in the rat model. FEMS Microbiol Ecol 46:213–219CrossRefGoogle Scholar
  108. 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 40:52–58CrossRefGoogle Scholar
  109. 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):1270–1284CrossRefGoogle Scholar
  110. 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 14:1–10Google Scholar
  111. Kikuchi Y, Hayatsu M, Hosikawa T et al (2012) Symbiont-mediated insecticide resistance. Proc Nat Acad Sci USA 109:8618–8622CrossRefGoogle Scholar
  112. Klein J (1982) Immunology: the science of self-nonself discrimination. Wiley, New YorkGoogle Scholar
  113. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62CrossRefGoogle Scholar
  114. Koren O, Goodrich JK, Cullender TC et al (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150:470–480CrossRefGoogle Scholar
  115. Kort R, Caspers M, van de Graaf A et al (2014) Shaping the oral microbiota through intimate kissing. Microbiome 2:41CrossRefGoogle Scholar
  116. 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 46:205–210CrossRefGoogle Scholar
  117. Laland KN, Odling-Smee J, Gilbert SF (2008) Evo-Devo and niche construction: building bridges. J Exp Zool 310:549–566CrossRefGoogle Scholar
  118. Laland K, Odling-Smee J, Turner S (2014) The role of internal and external constructive processes in evolution. J Physiol 592(11):2413–2422CrossRefGoogle Scholar
  119. 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):e3096CrossRefGoogle Scholar
  120. Lanning DK, Rhee KJ, Knight KL (2005) Intestinal bacteria and development of the B-lymphocyte repertoire. Trends Immunology 26:419–425CrossRefGoogle Scholar
  121. 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 113:15036–15041CrossRefGoogle Scholar
  122. Lederberg J, McCray AT (2001) ‘Ome sweet ‘omics—a genealogical treasury of words. The Scientist 15:8Google Scholar
  123. Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768–1773CrossRefGoogle Scholar
  124. 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 75:6147–6156CrossRefGoogle Scholar
  125. Lewontin RC (1978) Adaptation. Sci Am 239:156–169CrossRefGoogle Scholar
  126. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell: 124:837–848CrossRefGoogle Scholar
  127. Ley RE, Lozupone CA, Hamady M et al (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788CrossRefGoogle Scholar
  128. 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 96:761–771CrossRefGoogle Scholar
  129. Lloyd EA (1992) Unit of selection. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, CambridgeGoogle Scholar
  130. 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 267–291Google Scholar
  131. Lloyd EA (2017) Units and levels of selection. In: Zalta EN (ed) Stanford encyclopedia of philosophy.
  132. 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, CambridgeGoogle Scholar
  133. Lloyd E, Lewontin RC, Feldman MW (2008) The generational cycle of state spaces and adequate genetical representation. Philos Sci 75(2):140–156CrossRefGoogle Scholar
  134. Lozupone CA, Stombaugh JI, Gordon JI et al (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230CrossRefGoogle Scholar
  135. MacDonald SJ, Thomas GH, Douglas AE (2011) Genetic and metabolic determinants of nutritional phenotype in an insect-bacterial symbiosis. Mol Ecol 20:2073–2084CrossRefGoogle Scholar
  136. Macke E, Tasiemski A, Massol F et al (2017) Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos 126:508–531CrossRefGoogle Scholar
  137. Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S-1045SGoogle Scholar
  138. Margulis L, Sagan D (2001) The beast with five genomes. Nat Hist 110:3Google Scholar
  139. Matsuura Y, Kikuchi Y, Miura T, Fukatsu T (2015) Ultrabithorax is essential for bacteriocyte development. Proc Natl Acad Sci USA 112:9376–9381CrossRefGoogle Scholar
  140. 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, CambridgeGoogle Scholar
  141. McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21:1366–1372CrossRefGoogle Scholar
  142. 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 110:3229–3236CrossRefGoogle Scholar
  143. McInerney JO, Pisani D, Bapteste E, O’Connell MJ (2011) The public goods hypothesis for the evolution of life on earth. Biol Direct 6:41CrossRefGoogle Scholar
  144. Meiklejohn CD, Montooth KL, Rand DM (2007) Positive and negative selection on the mitochondrial genome. Trends Genet 23:259–263CrossRefGoogle Scholar
  145. Milani C, Mancabelli L, Lugli GA et al (2015) Exploring vertical transmission of Bifidobacteria from mother to child. Appl Environ Microbiol 81:7078–7087CrossRefGoogle Scholar
  146. Moeller AH, Caro-Quintero A, Mjungu D et al (2016) Co-speciation of gut microbiota with hominids. Science 353:380–382CrossRefGoogle Scholar
  147. Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13(12):e1002311CrossRefGoogle Scholar
  148. Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci USA 112:2093–2096CrossRefGoogle Scholar
  149. Mounier J, Monnet C, Vallaeys T et al (2008) Microbial interactions within a cheese microbial community. Appl Environ Microbiol 74:172–181CrossRefGoogle Scholar
  150. Mueller NT, Bakacs E, Combellick J et al (2014) The infant microbiome development: mom matters. Trends Mol Med 21:109–117CrossRefGoogle Scholar
  151. 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 222:181–202CrossRefGoogle Scholar
  152. 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 26:1612–1625CrossRefGoogle Scholar
  153. Nicholson JK, Holmes E, Kinross J et al (2012) Host-gut microbiota metabolic interactions. Science 336:1262–1267CrossRefGoogle Scholar
  154. 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 18:272–280CrossRefGoogle Scholar
  155. Nikoh N, Hosokawa T, Moriyama M et al (2014) Evolutionary origin of insect–Wolbachia nutritional mutualism. Proc Natl Acad Sci USA 111(28):10257–10262CrossRefGoogle Scholar
  156. Nuriel-Ohayon M, Neuman H, Koren O (2016) Microbial changes during pregnancy, birth, and infancy. Front Microbiol 7:1031CrossRefGoogle Scholar
  157. Nyholm SV, Stewart JJ, Ruby EG et al (2008) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11:483–493CrossRefGoogle Scholar
  158. 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 CrossRefGoogle Scholar
  159. Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution (No. 37). Princeton University Press, PrincetonGoogle Scholar
  160. Ohnmacht C, Park JH, Cording S et al (2015) The microbiota regulates type 2 immunity through RORγt+ T cells. Science 349(6251):989–993CrossRefGoogle Scholar
  161. Okasha S (2006) Evolution and the levels of selection. Oxford University Press, OxfordCrossRefGoogle Scholar
  162. Oldroyd GE, D. JD, Murray PS, Poole, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Gen 45:119–144CrossRefGoogle Scholar
  163. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994CrossRefGoogle Scholar
  164. 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 41:611–620CrossRefGoogle Scholar
  165. Osmanovic D, Kessler DA, Rabin Y, Soen Y (2017) Darwinian selection induces lamarckian adaptation in a holobiont model. arXiv preprint arXiv:1612.03567
  166. Pannebakker BA, Loppin B, Elemans CP. H. et al (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci USA 104:213–215CrossRefGoogle Scholar
  167. 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 290:12630–12649CrossRefGoogle Scholar
  168. Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29(3):170–175CrossRefGoogle Scholar
  169. Pradeu T (2012) The limits of the self: immunology and biological identity. Oxford University Press, New YorkCrossRefGoogle Scholar
  170. Rand DM, Hane RA, Fry AJ (2004) Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 19:645–653CrossRefGoogle Scholar
  171. Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101:4596–4601CrossRefGoogle Scholar
  172. Relman DA (2012) The human microbiome: ecosystem resilience and health. Nutr Rev 70:S2–S9CrossRefGoogle Scholar
  173. Rezende EL, Lavabre JE, Guimares PR (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature: 448:925–928CrossRefGoogle Scholar
  174. 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 172:1118–1124CrossRefGoogle Scholar
  175. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  176. Rosenberg E, Zilber-Rosenberg I (2011) Symbiosis and development: the hologenome concept. Birth Defects Res C 93:56–66CrossRefGoogle Scholar
  177. 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 CrossRefGoogle Scholar
  178. Rosenberg E, Koren O, Reshef L et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362CrossRefGoogle Scholar
  179. Rosner JL (2014) Ten times more microbial cells than body cells in humans? Microbe 9:47Google Scholar
  180. Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422. doi: 10.3389/fmicb.2014.00422 CrossRefGoogle Scholar
  181. Roughgarden J (1983) The theory of coevolution. In: Futuyma DJ, Slatkin M (eds) Coevolution. Sinauer, Sunderland, pp 33–64Google Scholar
  182. Roughgarden J (1998) Primer of ecological theory. Prentice Hall, Upper Saddle RiverGoogle Scholar
  183. 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, CambridgeGoogle Scholar
  184. 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, CambridgeGoogle Scholar
  185. 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 332:974–977CrossRefGoogle Scholar
  186. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2010) The making of a photosynthetic animal. J Exp Biol 214:303–311CrossRefGoogle Scholar
  187. Russell JB, Muck RE, Weimer PJ (2009) Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen. FEMS Microbiol Ecol 67:183–197CrossRefGoogle Scholar
  188. Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79(2):135–160CrossRefGoogle Scholar
  189. Sachs JL, Skophammer RG, Bansal N, Stajich JE (2014). Evolutionary origins and diversification of proteobacterial mutualists. Proc R Soc B 281(1775):20132146CrossRefGoogle Scholar
  190. 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 CrossRefGoogle Scholar
  191. Sanders JG, Powell S, Kronauer DJ et al (2014) Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 23:1268–1283CrossRefGoogle Scholar
  192. Schluter J, Foster KR (2012) The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol 10(11):e1001424Google Scholar
  193. Sefik E, Geva-Zatorsky N, Oh S et al (2015) Individual intestinal symbionts induce a distinct population of RORγ+ regulatory T cells. Science 349:993–997CrossRefGoogle Scholar
  194. Sekirov I, Russell SL, Antunes CM et al (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904CrossRefGoogle Scholar
  195. Sela DA, Li Y, Lerno L et al (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem 286:11909–11918CrossRefGoogle Scholar
  196. Sender R, Fuchs S, Milo R (2016) Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–340CrossRefGoogle Scholar
  197. 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 107:20051–20056CrossRefGoogle Scholar
  198. 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 60:991–1003CrossRefGoogle Scholar
  199. 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 10:3807–3821CrossRefGoogle Scholar
  200. Smith J (2007) A gene’s-eye view of symbiont transmission. Am Nat 170:542–550 CrossRefGoogle Scholar
  201. Soen Y (2014) Environmental disruption of host-microbe co-adaptation as a potential driving force in evolution. Front Genet 5:168CrossRefGoogle Scholar
  202. 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 370:20140303CrossRefGoogle Scholar
  203. Song SJ, Lauber C, Costello EK et al (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458Google Scholar
  204. 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 CrossRefGoogle Scholar
  205. 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 CrossRefGoogle Scholar
  206. Sterelny K (2011) Darwinian spaces: Peter Godfrey-Smith on selection and evolution. Biol Philos 26:489–500CrossRefGoogle Scholar
  207. Tadych M, Bergen MS, White JF (2014) Epichloë spp. associated with grasses: new insights on life cycles, dissemination and evolution. Mycologia 106:181–201CrossRefGoogle Scholar
  208. 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 24:3766–3778CrossRefGoogle Scholar
  209. Tauber AI 2009. The biological notion of self and non-self. In: Zelta EN (ed) Stanford encyclopedia of philosophy.
  210. Teixeira L, Ferreira Á., Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12):.e1000002CrossRefGoogle Scholar
  211. 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
  212. Trench RK (1993) Microalgal-invertebrate symbioses: a review. Endocytobiosis Cell Res 9:135–175Google Scholar
  213. Tsuchida T, Koga R, Horikawa M et al (2010) Symbiotic bacterium modifies aphid body color. Science 330:1102–1104CrossRefGoogle Scholar
  214. van Opstal EJ, Bordenstein SR (2015) Rethinking heritability of the microbiome. Science 349:1172–1173CrossRefGoogle Scholar
  215. Vandermeer J (1969) The competitive structure of communities: an experimental approach with protozoa. Ecology 50:362–371CrossRefGoogle Scholar
  216. 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 15:1301–1312CrossRefGoogle Scholar
  217. Veneti Z, Clark ME, Karr TL et al (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70:5366–5372CrossRefGoogle Scholar
  218. Wade MJ (2007) The co-evolutionary genetics of ecological communities. Nat Rev Genet 8:185–195CrossRefGoogle Scholar
  219. 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
  220. Wade MJ (2016) Adaptations in metapopulations. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  221. Wade M, Drown DM (2016) Nuclear-mitochondrial epistasis: a gene’s view of genomic conflict. Ecol Evol 6:6460–6472CrossRefGoogle Scholar
  222. Wade MJ, Goodnight CJ (2006) Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species. Evol Int J Org Evol 60:643–659CrossRefGoogle Scholar
  223. 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 58:117–126CrossRefGoogle Scholar
  224. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632CrossRefGoogle Scholar
  225. 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):.e114CrossRefGoogle Scholar
  226. Weiblen GD, Treiber EL (2015) Evolutionary origins and diversification of mutualism. Mutualism. Oxford University Press, Oxford, pp 37–56Google Scholar
  227. Wesemann DR, Portuguese AJ, Meyers RM et al (2013) Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 501:112–115CrossRefGoogle Scholar
  228. West-Eberhard M-J (1992) Adaptation: current uses. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard University Press, CambridgeGoogle Scholar
  229. 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 161–187Google Scholar
  230. Whitham TG, Bailey JK, Schweitze JA et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Gen 7:510–523CrossRefGoogle Scholar
  231. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  232. Wilson DS (1980) The natural selection of populations and communities. Benjamin/Cummings Publishing, Menlo ParkGoogle Scholar
  233. Yano JM, Yu K, Donaldson GP et al (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276CrossRefGoogle Scholar
  234. 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:e13963CrossRefGoogle Scholar
  235. 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):e0141842CrossRefGoogle Scholar
  236. Yoshida E, Sakurama H, Kiyohara M et al (2012) Bifidobacterium longum subsp.infantis uses two different β- type-2 human milk oligosaccharides. Glycobiology 22:361–368CrossRefGoogle Scholar
  237. 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 CrossRefGoogle Scholar
  238. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735CrossRefGoogle Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2017

Authors and Affiliations

  • Joan Roughgarden
    • 1
    • 6
  • Scott F. Gilbert
    • 2
  • Eugene Rosenberg
    • 3
  • Ilana Zilber-Rosenberg
    • 4
  • Elisabeth A. Lloyd
    • 5
  1. 1.Institute of Marine BiologyUniversity of HawaiiKaneoheUSA
  2. 2.Department of BiologySwarthmore CollegeSwarthmoreUSA
  3. 3.Department of Molecular MicrobiologyTel-Aviv UniversityTel AvivIsrael
  4. 4.Independent ScholarGivat ShmuelIsrael
  5. 5.History and Philosophy of Science and Medicine Department and Biology DepartmentIndiana UniversityBloomingtonUSA
  6. 6.Department of BiologyStanford UniversityStanfordUSA

Personalised recommendations