Abstract
That holobionts (microbial communities and their animal or plant hosts) are units of selection squares poorly with the observation that microbes are often recruited (horizontally acquired) from the environment, not passed down vertically from parent to offspring, as required for collective reproduction. The taxonomic makeup of a holobiont’s microbial community may vary over its lifetime and differ from that of conspecifics. In contrast, biochemical functions of the microbiota and contributions to host biology are more conserved, with taxonomically variable but functionally similar microbes recurring across generations and hosts. To save what is of interest in holobiont thinking, we propose casting metabolic and developmental interaction patterns, rather than the taxa responsible for them, as units of selection. Such units need not directly reproduce or form parent-offspring lineages: their prior existence has created the conditions under which taxa with the genes necessary to carry out their steps have evolved in large numbers. These taxa or genes will reconstruct the original interaction patterns when favorable conditions occur. Interaction patterns will vary (for instance by the alteration or addition of intermediates) in ways that affect the likelihood of and circumstances under which such reconstruction occurs. Thus, they vary in fitness, and evolution by natural selection will occur at this level. It is on the persistence, reconstruction, and spread of such interaction patterns that students of holobiosis should concentrate, we suggest. This model also addresses other multi-species collectively beneficial interactions, such as biofilms or biogeochemical cycles maintaining all life.
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References
Bateson P (1978) Review of The Selfish Gene. Anim Behav 26:316–318
Bateson P (2006) The nest’s tale. A reply to Richard Dawkins. Biol Philos 21(4):553–558
Bonner JT (1974) On development: the biology of form. Harvard University Press, Cambridge
Boon E, Meehan CJ, Whidden C, Wong DH-J, Langille MGI, Beiko RG (2014) Interactions in the microbiome: communities of organisms and communities of genes. FEMS Microbiol Rev 38:90–118
Booth A (2014) Symbiosis, selection and individuality. Biol Philos 29:657–673
Booth A, Doolittle WF (2015) Eukaryogenesis, how special really? Proc Natl Acad Sci USA 112(33):10278–10285
Booth A, Mariscal C, Doolittle WF (2016) The modern synthesis in the light of microbial genomics. Annu Rev Microbiol 70:279–297
Bordenstein SR (2013) The capacious hologenome. Zoology 116(5):260–261
Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226
Brown CT, Hug LA, Thomas BC, Sharon I, Castelle CJ, Singh A, Wilkins MJ, Wrighton KC, William KH, Banfield JF (2015) Unusual biology across a group comprising more than 15 % of domain Bacteria. Nature 523:206–211
Burke C, Steinberg P, Rusch D, Kjellberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108(34):14288–14293
Charbonneau MR, Blanton LV, DiGiulio DB, Relman DA, Lebrilla CB, Mills DA, Gordon JI (2016) A microbial perspective of human developmental biology. Nature 535:48–55
Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270
Clarke E (2016) Levels of selection in biofilms: multispecies biofilms are not evolutionary individuals. Biol Philos 32(2):191
Clemente JC, Ursell LK, Parfey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270
Datta MS, Sliwerska E, Gore J, Polz MF, Cordero OX (2016) Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat Commun 7:11965
De Monte S, Rainey PB (2014) Nascent multicellular life and the emergence of individuality. J Biosci 39:237–248
Doolittle WF (2013) Microbial neopleomorphism. Biol Philos 28(2):351–378
Doolittle WF (in press) Making the most of clade selection. Philos Sci 84
Doolittle WF, Brunet TDP (2016) What is the tree of life? PLoS Genet 12(4):e1005912
Douglas AR, Werren JH (2015) Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio 7(2):e02099-15
Ereshefsky M, Pedroso M (2015) Rethinking evolutionary individuality. Proc Natl Acad Sci USA 112(33):10126–10132
Falkowski P, Fenchel T, Delong EF (2008) The microbial engines that drive earth’s biogeochemical cycles. Science 320:1034–1039
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 6:728
Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Quart Rev Biol 87(4):325–341
Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, Oxford
Godfrey-Smith P (2013) Darwinian individuals. In: Bouchard F, Huneman P (eds) From groups to individuals: perspectives on biological associations and emerging individuality. MIT Press, Cambridge, pp 17–36
Godfrey-Smith P (2015a) Reproduction, symbioisis and the eukaryotic cell. Proc Natl Acad Sci USA 112(33):10120–10125
Godfrey-Smith P (2015b) Philosophy of biology. Prinecteon University Press, Princeton
Gray MW, Lukes J, Archibald JM, Keeling PJ, Doolittle WF (2011) Cell biology: irremediable complexity. Science 330(6006):920–921
Griesemer J (2000) Development, culture and the units of inheritance. Philos Sci 67:S348–S368 (Proceedings)
Hull DL (1980) Individuality and selection. Annu Rev Ecol Syst 11:311–332
Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30:409–425
Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108:4578–4585
Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169(2):2–17
Lenton T, Watson A (2011) Revolutions that made the Earth. Oxford University Press, Oxford
Lewontin R (1970) The units of selection. Annu Rev Ecol Syst 11(1):1–18
Lloyd EA (Forthcoming) Holobionts as units of selection: holobionts as interactors, reproducers, and manifestors of adaptation
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 365:1272–1277
Mas A, Jamshidi S, Lagadeuc Y, Eveillard D, Vandenkoornhuyse P (2016) Beyond the black queen hypothesis. ISME J. doi:10.1038/ismej.2016.22
Maynard Smith L, Szathmáry E (1995) The major transitions in evolution. WH Freeman, San Francisco
Moran NA, Sloan DB (2015) The hologenome concept: Helpful or hollow? PLoS Biol 13(12):e1002311
Morowitz HJ, Smith E, Srinivasan V (2008) Selfish metabolism. Complexity 14(2):7–9
Noda S, Kitade O, Inoue T, Kawai M, Kanuka M, Hiroshima K, Hongoh Y, Constantino R, Uys V, Zhong J, Kudo T, Ohkuma M (2007) Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp), their hosts, and their bacterial endosymbionts. Mol Ecol 16(6):1257–1266
O’Malley M (Forthcoming) Causal claims about microbiota: implications for individuality. Biol Philos
Odling-Smee FJ, Laland KV, Feldman MW (1996) Niche construction. Am Nat 147:641–648
Omelchenko MV, Makarova KS, Wolf YI, Rogozin IB, Koonin EV (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4(9):R55
Queller DC (1997) Cooperators since life began. Quart Rev Biol 72:184–188
Rader BA, Nyholm SV (2012) Host/microbe interactions revealed through “omics” in the symbiosis between the Hawaiian bobtail squid Eurypymna scolopes and the bioluminescent bacterium Vibrio fischeri. Biol Bull 223:103–111
Rao K, Safdar N (2016) Fecal microbiota transplantation for the treatment of Clostridium difficile infection. J. Hosp Med 11:56–61
Rison SGG, Thornton JM (2002) Pathway evolution, structurally speaking. Curr Opin Struct Biol 12(3):374–382
Røder HL, Sørensen SJ, Burmølle M (2016) Studying bacterial multispecies biofilms: Where to start? Trends Microbiol 24(6):503–513
Schmidt S, Sunyaev S, Bork P, Dandekar T (2003) Metabolites: a helping hand for pathway evolution? Trends Biochem Sci 28(6):336–341
Sommer RJ (2008) Homology and the hierarchy of biological systems. BioEssays 30:653–658
Sonnenburg JL, Bäckhed F (2016) Diet-microbiota interactions as moderators of human metabolism. Nature 535:56–64
Sterelny K, Smith KC, Dickison M (1996) The extended replicator. Biol Philos 11(3):377–403
Taxis T, Wolff S, Gregg SJ, Minton NO, Zhang C, Dai J, Schnabel RD, Taylor JF, Kerley MS, Pires JC, Lamberson WR, Conant GC (2015) The players may change but the game remains: network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity. Nucl Acids Res 42(20):9600–9612
The Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214
Theis KR, Dheilly 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: and ecoevolutionary framework for hosts and their microbiomes. mSystems 1(2):e00028-16
Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-Garcia C, Olson JB, Erwin PM, López-Legenti S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870. doi:10.1038/ncomms11870
Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, Podar M, Short JM, Mathur EJ, Detter JC, Bork P, Hugenholtz P, Rubin ER (2005) Comparative metagenomics of microbial communities. Science 308(5721):554–557
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2007) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031
Wade WG (2013) The oral microbiome in health and disease. Pharmcol Res 69(1):137–143
Wagner GP (2007) The developmental genetics of homology. Nat Rev Genet 8:473–476
Wagner GP (2014) Homology, genes and evolutionary innovation. Princeton University Press, Princeton
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(5):725–735
Acknowledgments
We thank the Natural Sciences and Engineering Research Council of Canada (Grant GLDSU 447989) for support and Maureen O’Malley, Carlos Mariscal, Tyler Brunet, Letitia Meynell, and Andrew Fenton for comments on an earlier version.
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Doolittle, W.F., Booth, A. It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos 32, 5–24 (2017). https://doi.org/10.1007/s10539-016-9542-2
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DOI: https://doi.org/10.1007/s10539-016-9542-2