Biology & Philosophy

, Volume 31, Issue 6, pp 875–892 | Cite as

Holobionts and the ecology of organisms: Multi-species communities or integrated individuals?

Article

Abstract

It is now widely accepted that microorganisms play many important roles in the lives of plants and animals. Every macroorganism has been shaped in some way by microorganisms. The recognition of the ubiquity and importance of microorganisms has led some to argue for a revolution in how we understand biological individuality and the primary units of natural selection. The term “holobiont” was introduced as a name for the biological unit made up by a host and all of its associated microorganisms, and much of this new debate about biological individuality has focused on whether holobionts are integrated individuals or communities. In this paper, I show how parts of the holobiont can span both characterizations. I argue that most holobionts share more affinities with communities than they do with organisms, and that, except for maybe in rare cases, holobionts do not meet the criteria for being organisms, evolutionary individuals, or units of selection.

Keywords

Holobiont Symbiosis Individuality Organism Bacteria Microbe 

References

  1. Apprill A, Marlow HQ, Martindale MQ, Rappe MS (2009) The onset of microbial associations in the coral Pocillopora meandrina. ISME J 3:685–699CrossRefGoogle Scholar
  2. Aristotle (1984) Categories. In: Barnes J (ed) The complete works of Aristotle, vol 1. Princeton University Press, PrincetonGoogle Scholar
  3. Berg RD (1996) The indigenous gastrointestinal microflora. Trends Microbiol 4:430–435CrossRefGoogle Scholar
  4. Bocci V (1992) The neglected organ: bacterial flora has a crucial immunostimulatory role. Perspect Biol Med 35(2):251–260CrossRefGoogle Scholar
  5. Booth A (2014) Symbiosis, selection and individuality. Biol Philos 29:657–673CrossRefGoogle Scholar
  6. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226CrossRefGoogle Scholar
  7. Bosch TCG, McFall-Ngai MJ (2011) Metaorganisms as the new frontier. Zoology 114:185–190CrossRefGoogle Scholar
  8. Bouchard F (2013) What is a symbiotic superindividual and how do you measure its fitness? In: Bouchard F, Huneman P (eds) From groups to individuals: evolution and emerging individuality. MIT Press, Cambridge, pp 243–264Google Scholar
  9. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8(3):218–230CrossRefGoogle Scholar
  10. Brucker RM, Bordenstein SR (2014) Response to comment on “The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia”. Science 345:1011CrossRefGoogle Scholar
  11. Buss L (1987) The evolution of individuality. Princeton University Press, PrincetonGoogle Scholar
  12. Clarke E (2011) The problem of biological individuality. Biol Theory 5(4):312–325CrossRefGoogle Scholar
  13. Clarke E (2016) Levels of selection in biofilms: multispecies biofilms are not evolutionary individuals. Biol Philos 31:191–212CrossRefGoogle Scholar
  14. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  15. Douglas AE, Werren JH (2016) Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7(2):e02099-15CrossRefGoogle Scholar
  16. Dupré J (2012) The polygenomic organism. In: Dupré J (ed) Processes of life: essays in the philosophy of biology. Oxford University Press, Oxford, pp 116–127CrossRefGoogle Scholar
  17. Dupré J, O’Malley MA (2009) Varieties of living things: life at the intersection of lineage and metabolism. Philos Theory Biol 1Google Scholar
  18. Ereshefsky M, Pedroso M (2013) Biological individuality: the case of biofilms. Biol Philos 28(2):331–349CrossRefGoogle Scholar
  19. Ereshefsky M, Pedroso M (2015) Rethinking evolutionary individuality. PNAS 112:10126–10132CrossRefGoogle Scholar
  20. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543CrossRefGoogle Scholar
  21. Garcia JR, Gerardo NM (2014) The symbiont side of symbiosis: do microbes really benefit? Front Microbiol 5(510):1–6Google Scholar
  22. Gilbert SF (2014) Symbiosis as the way of eukaryotic life: the dependent co-origination of the body. J Biosci 39:201–209CrossRefGoogle Scholar
  23. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87(4):325–341CrossRefGoogle Scholar
  24. Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, OxfordCrossRefGoogle Scholar
  25. Godfrey-Smith P (2011) Agents and acacias: replies to Dennett, Sterelny, and Queller. Biol Philos 26(4):501–515CrossRefGoogle Scholar
  26. Godfrey-Smith P (2013) Darwinian individuals. In: Bouchard F, Huneman P (eds) From groups to individuals: evolution and emerging individuality. MIT Press, Cambridge, pp 17–36Google Scholar
  27. Godfrey-Smith P (2015) Reproduction, symbiosis, and the eukaryotic cell. PNAS 112(33):10120–10125CrossRefGoogle Scholar
  28. Golubic S, Radtke G, Le Campion-Alsumard T (2005) Endolithic fungi in marine ecosystems. Trends Microbiol 13:229–235CrossRefGoogle Scholar
  29. Gordon J, Knowlton N, Relman DA, Rohwer F, Youle M (2013) Superorganisms and holobionts. Microbe 8(4):152–153Google Scholar
  30. Griesemer J (2000) Development, culture and the units of inheritance. Philos Sci 67:S348–S368CrossRefGoogle Scholar
  31. Griesemer J (2014) Reproduction and scaffolded developmental processes: an integrated evolutionary perspective. In: Minelli A, Pradeu T (eds) Towards a theory of development. Oxford University Press, New York, pp 183–202CrossRefGoogle Scholar
  32. Griesemer J (forthcoming) Reproduction in complex life cycles: toward a developmental reaction norms perspective. Philos Sci (online first)Google Scholar
  33. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53CrossRefGoogle Scholar
  34. Hull D (1978) A matter of individuality. Philos Sci 45(3):335–360CrossRefGoogle Scholar
  35. Hull D (1980) Individuality and selection. Annu Rev Ecol Syst 11:311–332CrossRefGoogle Scholar
  36. Hull D (1992) Individual. In: Fox-Keller E, Lloyd E (eds) Keywords in evolutionary biology. Harvard University Press, Cambridge, pp 181–187Google Scholar
  37. Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. PNAS 113(16):4416–4421CrossRefGoogle Scholar
  38. Huss J (2014) Methodology and ontology in microbiome research. Biol Theory 9:392–400CrossRefGoogle Scholar
  39. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62CrossRefGoogle Scholar
  40. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000CrossRefGoogle Scholar
  41. Lesser MP, Stat M, Gates RD (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:603–611CrossRefGoogle Scholar
  42. Lewontin RC (1970) The units of selection. Annu Rev Ecol Syst 1(1):1–18CrossRefGoogle Scholar
  43. Lloyd E (2012) Units and levels of selection. In: Zalta EN (ed) The stanford encyclopedia of philosophy. Winter 2012. http://plato.stanford.edu/archives/win2012/entries/selection-units/
  44. Margulis L (1991) Symbiogenesis and symbionticism. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Cambridge, pp 1–14Google Scholar
  45. Maynard Smith J, Szathmary E (1995) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  46. McFall-Ngai M (2016) Introduction to the hologenome special series. mBio 7(2):e00371-16CrossRefGoogle Scholar
  47. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236CrossRefGoogle Scholar
  48. Michod RE (1999) Darwinian dynamics. Evolutionary transitions in fitness and individuality. Princeton University Press, PrincetonGoogle Scholar
  49. Moran NA (2006) Symbiosis. Curr Biol 16(October):R866–R871CrossRefGoogle Scholar
  50. Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13(12):e1002311CrossRefGoogle Scholar
  51. Morris JJ, Lenski RE, Zinser ER (2012) The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3(2):e00036-12CrossRefGoogle Scholar
  52. Mushegian AA, Ebert D (2016) Rethinking “mutualism” in diverse host-symbiont communities. BioEssays 38:100–108CrossRefGoogle Scholar
  53. O’Malley MA (forthcoming) Reproduction expanded: multigenerational and multilineal units of evolution. Philos Sci (online first)Google Scholar
  54. Pradeu T (2010) What is an organism? An immunological answer. Hist Philos Life Sci 32(2–3):247–267Google Scholar
  55. Pradeu T (2012) The limits of the self: immunology and biological identity. Oxford University Press, USA, Translated by Elizabeth VitanzaGoogle Scholar
  56. Queller DC, Strassmann JE (2009) Beyond society: the evolution of organismality. Philos Trans R Soc B 364:3143–3155CrossRefGoogle Scholar
  57. Queller DC, Strassmann JE (this issue) Problems of multi-species organisms: endosymbionts to holobionts. Biol Philos. doi:10.1007/s10539-016-9547-x
  58. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  59. Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5(422):1–22Google Scholar
  60. Sachs JL, Hollowell AC (2012) The origins of cooperative bacterial communities. mBio 3(3):e00099-12CrossRefGoogle Scholar
  61. Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202–209CrossRefGoogle Scholar
  62. Singh Y, Ahmad J, Musarrat J, Ehtesham NZ, Hasnain SE (2013) Emerging importance of holobionts in evolution and in probiotics. Gut Pathog 5:12CrossRefGoogle Scholar
  63. Sober E, Wilson DS (1998) Unto others: the evolution and psychology of unselfish behaviour. Harvard University Press, Cambridge, MAGoogle Scholar
  64. Stat M, Baker AC, Bourne DG, Correa AMS, Forsman Z, Huggett MJ, Pochon X, Skillings D, Toonen RJ, van Oppen MJH, Gates RD (2012) Molecular delineation of species in the coral holobiont. In: Lesser M (ed) Advances in marine biology, vol 63. Academic Press, Amsterdam, pp 1–65Google Scholar
  65. Sterelny K (2001) Niche construction, developmental systems, and the extended replicator. In: Oyama S, Griffiths PE, Gray RD (eds) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge, pp 333–349Google Scholar
  66. Sterelny K (2004) Symbiosis, evolvability and modularity. In: Schlosser G, Wagner G (eds) Modularity in development and evolution. University of Chicago Press, ChicagoGoogle Scholar
  67. Sterelny K (2006) Local ecological communities. Philos Sci 73:215–231CrossRefGoogle Scholar
  68. Sterelny K (2011) Darwinian spaces: Peter Godfrey-Smith on selection and evolution. Biol Philos 26:489–500CrossRefGoogle Scholar
  69. Theis KR, Dhelly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein SR (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1(2):e00028-16CrossRefGoogle Scholar
  70. Thompson JR, Rivera HE, Closek CJ, Medina M (2015) Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol 4(176):1–20. doi:10.3389/fcimb.2014.00176 Google Scholar
  71. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9(11):2707–2719CrossRefGoogle Scholar
  72. Wooldridge SA (2010) Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? BioEssays 32:615–625CrossRefGoogle Scholar
  73. Xu J, Gordon JI (2003) Honor thy symbionts. Proc Natl Acad Sci USA 100:10452–10459CrossRefGoogle Scholar
  74. 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

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Philosophy ProgramThe Graduate Center, CUNYNew YorkUSA
  2. 2.University of Bordeaux/CNRSUMR5164BordeauxFrance

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