Abstract
Symbiosis plays a fundamental role in contemporary biology, as well as in recent thinking in philosophy of biology. The discovery of the importance and universality of symbiotic associations has brought new light to old debates in the field, including issues about the concept of biological individuality. An important aspect of these debates has been the formulation of the hologenome concept of evolution, the notion that holobionts are units of natural selection in evolution. This review examines the philosophical assumptions that underlie recent proposal of the hologenome concept of evolution, and traces those debates back in time to their historical origins, to the moment when the connection between the topics of symbiosis and biological individuality first caught the attention of biologists. The review is divided in two parts. The first part explores the historical origins of the connection between the notion of symbiosis and the concept of biological individuality, and emphasizes the role of A. de Bary, R. Pound, A. Schneider and C. Merezhkowsky in framing the debate. The second part examines the hologenome concept of evolution and explores four parallelisms between contemporary debates and the debates presented in the first part of the essay, arguing that the different debates raised by the hologenome concept were already present in the literature. I suggest that the novelty of the hologenome concept of evolution lies in the wider appreciation of the importance of symbiosis for maintaining life on Earth as we know it. Finally, I conclude by suggesting the importance of exploring the connections among contemporary biology, philosophy of biology and history of biology in order to gain a better understanding of contemporary biology.
Similar content being viewed by others
Notes
The review is not about the problem of biological individuality and how different biologists and philosophers have conceived the topic; rather, this review is about the relation between symbiosis and certain dimensions of the problem of biological individuality –the boundaries and composition of the biological individual and the units of selection. However, the reader must at least take into account that three different notions of biological individual will be considered, especially in part 2: biological individuals as functionally integrated units, biological individuals as units of selection and biological individuals as bounded units (with clear physical boundaries, such as a membrane). Readers interested in the philosophical problem of biological individuality might refer to Wilson and Barker (2013), Bouchard and Huneman (2013), Pradeu (2016a), DiFrisco (2017) and Lidgard & Nyhart (2017: 17-63).
There are alternative ways to spell his name (e.g. Merezhkovski, Mérejkovski, Mereschkovsky). I use the spelling that appears in Sapp et al. (2002).
My historical focus is selective and not exhaustive, since I aim to compare four parallelisms between the historical development of the concept of symbiosis and the recent developments of the concept of holobiosis. The reconstructed history I will present will reflect this interest. For the readers who are interested in seeing different historical reconstructions see Sapp (1994), Paracer & Ahmadjian (2000: 231-238), Wilkinson (2001), Peacock (2011), Martin and Schwab (2012), Egerton (2015), Carrapiço (2015), Gontier (2015, 2016a), Zook (2015).
Frank N. Egerton, however, in his review paper on the history of symbiosis studies dedicates the first section to studies of symbiotic phenomena that appeared before the concept of “symbiosis” was introduced (2015: 81–90). He goes as far as to Herodotus, Aristotle and Theophrastus. Despite the interest of their research, as far as this review is about the philosophical implications of the concept and its relation to other philosophical concepts, I have chosen to begin with de Bary’s account.
Parasitism was known while before van Beneden, but parasites (including those that we might call nowadays microorganisms, Pasteur’s germs) were basically considered as pursuing their own interests, thus necessarily damaging the other in a context of struggle for life (e.g. Spencer 1899; cf. Sapp 1994: 25–28). Precisely, what is innovative about van Beneden’s work was that he was the first in: (1) identifying the existence of an important number of associations among organisms that are not parasitic, a discovery that of course had historical precedents; (2) classifying the different types of biological associations in virtue of their effects in a systematic way, which is also conceptually different from previous views on the economy of nature (Egerton 2015: 84).
It is important to note that lichenologists originally rejected Schwendener’s dual hypothesis (e.g. Crombie 1886), denying in some cases the evidence, among other reasons because its acknowledgment would threaten “the hard-won autonomy of lichenists themselves” (Sapp 1994: 4), in so far as lichens would stop being an independent biological individual. Interestingly, lichenologists did not lose their autonomy and it was precisely the study of lichens as dual individuals that began challenging traditional ways of understanding biological individuals more generally. This is the first moment, to my knowledge, that the problem of symbiosis and the philosophical problem of biological individuality get engaged in a way that questions the traditional conception of what counts as a biological individual.
One of the reasons why symbiosis became identified with mutualism during this period is related to the influence of the political ideas of the time, especially the anarchist ideas of Kropoptkin (1902). Readers interested in the influence of political ideas on symbiosis thinking can refer to Sapp (1994: 18-25) and Gontier (2016a).
Although he did not call them Rhizobium, but “tubercles,” stating “For all that I have read and seen, I am satisfied that the parasites [in Leguminosae] are bacteria, and I see no reason for separating them from the rest of Schizomycetes as Schneider does. I even doubt the necessity of creating a separate genus for them, as Frank did in 1890, under the name of ‘Rhizobium’” (Pound 1893: 517).
See Oldroyd (2013) to realize that some of Frank’s observations were indeed true and Pound, while having a fair point about the lack of proper evidence for some of Frank’s statements, could have not been more mistaken.
Pound’s seems to assume a concept of biological individuality similar to what Queller and Strassmann have recently called the “cooperation/conflict conception” of the biological individual (2009, 2016). For Pound, as it happens for the authors, symbiotic assemblages cannot be considered individuals in the proper sense, as the entities that engage in the symbiosis are in constant struggle with each other.
It must be noted, although in passing, that Schneider does not require that the two organisms that engage in symbiosis belong to different species: he only requires that they are morphologically different. That’s why, from his perspective, the mother and the embryo/foetus, the sexual cells that merge to form a zygote or even tumours or cysts would count as cases of symbiosis. This is, I think, different from de Bary’s original purpose –probably that’s why Schneider says that he uses symbiosis “in its broader meaning, not in the sense of De Bary” (1897: 923, fn. 1)–, who seemed to understand symbiosis requiring different species.
Schneider acknowledges the problems of this position, which can be criticized on the same basis as Pound had criticized Frank’s account of mycorrhiza –“[t]hat every tree has its root system covered with mycelia, proves nothing” (Pound 1893: 516). However, he justifies his decision by claiming “[f]rom a priori reasoning one is, however, forced to conclude that the first symbiotic activities began with the first contact of organisms” (1897: 933).
See part II of the paper for seeing how these sorts of claims are presently unsustainable.
Of course, extinction of the symbiotic association, but not necessarily of the partners that interact symbiotically. Remember that Schneider’s paper aims to study exclusively the phylogenetic evolution of symbiotic associations without reference to the organisms that interact.
Those readers who are not familiar with the different types of biological individuals (physiological, anatomical, developmental, evolutionary, etc.) can check Gilbert et al. (2012), Godfrey-Smith (2013), Pradeu (2016a, b), DiFrisco (2017). In brief, however, it is important that she notes that not all criteria for classifying biological individuals necessarily led to coincidental classifications and sometimes different criteria overlap. For the overlapping nature of biological classification see Clarke (2010).
It is widely acknowledged that chloroplasts are responsible for the green colour of plants.
Maynard-Smith does not use “units of selection”, but “units of evolution”, where a unit of selection is whatever entity exhibit phenotypic variation that led to multiplication of the entity within the population (thus being selected for or against), and a unit of evolution is a unit of selection that, furthermore, exhibits heredity (Maynard-Smith 1987). In contrast with Maynard-Smith, I will use “unit of selection” as it is conventionally used, i.e. requiring heredity, variance and fitness/multiplication, and thus meaning what Maynard-Smith means by “unit of evolution” (see Lloyd 2017a, c: 293–297; Gontier 2010, for an analysis of the concept of “unit of selection”)
Originally, they referred to it as the hologenome theory of evolution. Later on, they started calling it the hologenome concept of evolution (cf. Gissis et al. 2017: 303–384).
A clear antecedent to the hologenome concept is found in Sapp (2003: 234-251, 2004), when he coins the concept of “symbiome”. He defines the symbiome as the entity “comprising chromosomal genes, organellar genes, viral genes, as well as other microbial symbionts, sometimes inside cells and always outside them, functioning across a continuum from parasitism to mutualism, depending on their nature and context (…). Since every plant and animal consists of complex ecological communities of microbes, the symbiome must function as a unit of selection.” (2004: 1047). Nonetheless, Sapp first presents the concept in a section dedicated to developmental symbiosis (Sapp 2003: 235–236), and there is no reason to believe that a developmental organism should be delineated by the same boundaries than a unit of selection (e.g. DiFrisco 2017). The concept of “symbiome”, however, is not as frequent in current literature as the concept of “holobiont” and it has been recently used with two different meanings: first, to refer to the whole set of symbionts that associate with a host, without including the host (e.g. Boucias et al. 2013; Rosas-Pérez et al. 2017); second, to refer exclusively to “the colocalized and coevolving taxa in a given consortium” (Tripp et al. 2017: 552). If we define the concept according to the second formulation, then one might argue either that symbiome = hologenome (if the hologenome is proven to evolve as a single unit) or that the symbiome corresponds to the part of the hologenome that actually evolves as a single unit (e.g. the set of vertically transmitted symbionts). This warrants further discussion, which is, however, outside the scope of this paper. For my present purposes I will restrict the discussion to the concept of the holobiont sui generis.
“Such that replication is differential” does not specify which are the entities whose differential replication might be affected by belonging to an interactor. It is conceptually possible that the holobiont is an interactor that promotes a more efficient replication of the different individuals that compose the holobiont (host, microbes of the microbiome), but not of the hologenome.
This position is taken to the extreme in Doolittle (2017).
References
Booth A (2014) Symbiosis, selection and individuality. Bio Philos 29:657–673
Bordenstein SR, Theis KR (2015) Host biology in the light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. https://doi.org/10.1371/journal.pbio.1002226
Bouchard F, Huneman P (2013) From groups to individuals. Evolution and emerging individuality. The MIT Press, London
Boucher P (1965) Endosymbiosis of animals with plants microorganisms. Interscience Publishers, New York
Boucias DG, Kariithi HM, Bourtzis K, Schneider DI, Kelley K, Miller WJ, Parker AG, Abd-Alla AMM (2013) Transgenerational transmission of the Glossina pallidipes Hytrosavirus depends on the presence of a functional Symbiome. PLoS One 8(4):e61150
Brandt K (1881) Über das Zusammenleben von Algen und Tieren. Biologisches Centallblatt 1:524–527
Brucker RM, Bordenstein SR (2012) Speciation by Symbiosis. Trends Ecol Evol 27(8):443–451
Brucker RM, Bordenstein SR (2013) The capacious hologenome. Zoology 116:260–261
Carrapiço F (2015) Can we understand evolution without Symbiogenesis? In: Gontier N (ed) Reticulate evolution: Symbiogenesis, lateral gene transfer, hybridization and infectious heredity. Springer, London, pp 81–106
Chiu L, Eberl G (2016) Microorganisms as scaffolds of biological individuality: an eco-immunity account of the holobiont. Biol Philos 31:819–837
Clarke E (2010) The problem of biological individuality. Biological Theory 5(4):312–325
Crombie JM (1886) On the algo-lichen hypothesis. Journal of Linnaean Society 21:259–282
Cullen TW, Schofield WB, Barry NA, Putnam EE, Rundell EA, Trent MS, Degnan PH, Booth CJ, Yu H, Goodman AL (2015) Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347(6218):170–175
Dawkins R (1976) The Selfish Gene. Oxford, Oxford University Press
De Bary A (1879) Die Erscheinung der Symbiose. Verlag von Karl J, Trübner
Díaz, JS (2015) El mecanismo evolutivo de Margulis y los niveles de selección. Contrastes: Revista internacional de filosofía 20(1):7–24
DiFrisco J (2017) Kinds of biological individuals: Sortals, projectability, and selection. Br J Philos Sci
Doolittle WF (2017) Darwinizing Gaia. J Theor Biol 434:11–19
Doolittle WF, Booth A (2017) It’s the song not the singer: an exploration of holobiosis and evolutionary theory. Biol Philos 32:5–24. https://doi.org/10.1007/s10539-016-9542-2
Douglas AE (2010) The symbiotic habit. Princeton University Press, Oxford
Douglas AE, Werren JH (2016) Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio 7(2):e02099–e02015
Dupré J (2010) The polygenomic organism. Sociol Rev 58(s1):19–30
Dupré J (2012) Processes of life: essays in the philosophy of biology. Oxford University Press, Oxford
Dupré J, O’Malley MA (2009) Varieties of living things: life at the intersection of lineage and metabolism. Philosophy & Theory in Biology 1(December). https://doi.org/10.3998/ptb.6959004.0001.003
Egerton FN (2015) History of ecological sciences, part 52: Symbiosis studies. Bulletin of Ecological Society of America 96(1):80–139
Frank R (1877) Über die biologischen Verthältnisse des Thallus eineger Krustenflecten. Beitrage zur Biologie der Pflanzen 2:123–200
Frank R (1885) Über die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Berichte der Deutschen Botanischen Gesellschaf 3:128–145
Frank R (2005) On the nutritional dependence of certain trees on root symbiosis with belowground fungi (an English translation of a.B. Frank’s classic paper of 1885). Mycorrhiza 15:267–275
Geddes P (1882) Further researchers on animals containing chlorophyll. Nature 25:303–304
Gilbert SF, Epel D (2009) Ecological Developmental Biology. Sinauer Associates
Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87(4):325–341
Gilbert SF, Rosenberg E, Zilber-Rosenberg I (2017) 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. The MIT Press, London, pp 305–324
Gissis SB, Lamm E, Shavit A (eds) (2017) Landscapes of collectivity in the life sciences. The MIT Press, Cambridge
Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, Oxford
Godfrey-Smith P (2015) Reproduction, symbiosis, and the eukaryotic cell. PNAS 112(33):10120–10125
Gontier N (2015) Reticulate evolution: Symbiogenesis, lateral gene transfer, hybridization and infectious heredity. Springer, London
Gontier N (2016a) Symbiosis. In: Kliman RM (ed) The Encyclopaedia of evolutionary biology, vol 4. Academic Press, Oxford, pp 272–281
Gontier N (2016b) Symbiogenesis. In: Kliman RM (ed) The Encyclopaedia of evolutionary biology, vol 4. Academic Press, Oxford, pp 261–271
Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O et al (2014) Human genetics shapes the gut microbiome. Cell 159:789–799
Goodrich JK, Davenport ER, Beaumont M, Clark AG, Ley RE (2017) The relationship between the human genome and microbiome comes into view. Annu Rev Genet 51:413–433
Griesemer J (2016) Reproduction in complex life cycles: a developmental reaction norms perspective. Philos Sci 83:803–815
Griesemer J (2017) Landscapes of developmental collectivity. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. The MIT Press, London, pp 25–48
Guerrero R, Margulis L, Berlanga M (2013) Symbiogenesis: the holobiont as a unit of evolution. Int Microbiol 16:133–143
Hester ER, Barott KL, Nulton J, Vermeij MJA, Rohwer FL (2016) Stable and sporadic symbiotic communities of coral and algal holobionts. The ISME Journal 10:1157–1169
Honegger R (2000) Simon Schwendener (1829–1919) and the dual hypothesis of lichens. Bryologist 103(2):307–313. https://doi.org/10.1639/0007-2745(2000)103[0307:SSATDH]2.0.CO;2
Hull DL (1980) Individuality and selection. Annu Rev Ecol Syst 11:311–332. https://doi.org/10.1146/annurev.es.11.110180.001523
Hurst GDD (2017) Extended genomes: symbiosis and evolution. Interface Focus 7:20170001. https://doi.org/10.1098/rsfs.2017.0001
Huttenhower C, Gevers D, Knight R, Creas HH et al (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214
Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215
Khakhina LN (1992) Concepts of Symbiogenesis: a historical and critical study of the research of Russian botanists. Yale University Press, New Haven
Kozo-Polyanski M (1924 [2010]) Symbiogenesis. A new principle in evolution. Edited by V Fett & L Margulis. Cambridge, Harvard University Press
Kropoptkin P (1902) Mutual aid. A factor of evolution. William Heinemann, London
Lamm E (2017) Cultural group selection and Holobiont evolution: a comparison of structures of evolution. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. The MIT Press, London, pp 369–384
Lemanceau P, Blouin M, Muller D, Moënne-Loccoz Y (2017) Let the core microbiota be functional. TRENDS in Plant Science 22 (7): 583–595
Lewontin RC (1970) The units of selection. Annu Rev Ecol Syst 1:1–18
Lidgard S, Nyhart LK (2017) The work of biological individuality. Concepts and contexts. In: Lidgard S, Nyharts LK (eds) Biological individuality. Integrating scientific, philosophical and historical perspectives. The University of Chicago Press, London, pp 17–62
Lipnicki LL (2015) The role of symbiosis in the transmission of some eukaryotes from aquatic to terrestrial environments. Symbiosis 65:39–53
Lloyd E (2017a) Units and Levels of selection. In EN Zalta (ed.) Stanford Encyclopaedia of Philosophy. https://plato.stanford.edu/entries/selection-units/
Lloyd E (2017b) 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. The MIT Press, London, pp 351–367
Lloyd E (2017c) A glimpse of philosophy of biology and collectivities today. In: Gissis SB, Lamm E, Shavit A (eds) Landscapes of collectivity in the life sciences. The MIT Press, London, pp 291–301
Margulis L (1970) The origin of eukaryotic cells. Yale University Press
Margulis L (1990) Words as battle cries – symbiogenesis and the new field of endocytobiology. Bio Sci 40(9):673–677
Margulis L (1991) Symbiogenesis and symbioticism. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge, pp 1–14
Margulis L (1993) Symbiosis in cell evolution: microbial communities in the Archean and Proterozoic eons. WH Freeman and Co., New York
Margulis L (1998) Symbiotic planet. A new look at evolution. Basic Books, New York
Margulis L (2010) Symbiogenesis. A new principle in evolution. Paleontol J 44(12):1525–1539
Margulis L, Fester R (eds) (1991) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge
Margulis L, Sagan D (2002) Acquiring genomes. A theory of the origin of species. Basic Books, New York
Martin W, Kowallik K (1999) Annotated English translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der Chromatophoren im Pflanzanreiche”. Eur J Phycol 34(3):287–295
Martin BD, Schwab E (2012) Symbiosis: “living together” in chaos. Studies in the History of Biology 4(4):7–25
Martin BD, Schwab E (2013) Current usage of symbiosis and associated terminology. International Journal of Biology 5:32–45
Maynard-Smith J (1987) Evolutionary progress and levels of selection. In: Dupré J (ed) The latest on the best: essays on evolution and optimality. MIT Press, Cambridge, pp 119–131
Maynard-Smith J (1991) A Darwinian view of symbiosis. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge, pp 26–39
McFall-Ngai M (2015) Giving microbestheir due – animal life in amicrobially dominant world. J Exp Biol 218:1968–1973
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G et al (2013) Animals in the bacterial world, a new imperative for the life sciences. PNAS 110(9):3229–3236
Merezhkowsky C (1905) Über Natur und Ursprung der Chromatophoren imPflanzanreiche. Biologisches Centralblatt 25:593–604
Merezhkowsky C (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biologisches Centralblatt 30:278–303
Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV et al (2016) Cospeciation of gut microbiota with hominids. Science 353:380–382
Moran N, Sloan DB (2015) The Hologenome concept: helpful or hollow? PLoSBiol 13(12):e1002311
O’Malley MA (2017) From endosymbiosis to holobionts: evaluating a conceptual legacy. J Theor Biol 434:34–41. https://doi.org/10.1016/j.jtbi.2017.03.008
O’Malley MA, Dupré J (2007) Size doesn’t matter: towards a more inclusive philosophy of biology. Biol Philos 22:155–191
Ochman H, Worobey M, Kuo C-H, Ndjango N-BN, Peeters M et al (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8(11):e10000546
Okasha S (2006) Evolution and the levels of selection. Oxford University Press, Oxford
Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263
O'Malley MA (2014) Philosophy of microbiology. Cambridge University Press, Cambridge
Oulhen N, Schulz BJ, Carrier TJ (2016) English translation of Heinrich Anton de Bary’s 1878 speech, ‘die Erscheinung der Symbiose’(‘De la symbiose’). Symbiosis 69:131–139. https://doi.org/10.1007/s13199-016-0409-8
Paracer S, Ahmadjian V (2000) Symbiosis: an introduction to biological associations. Oxford University Press, Oxford
Peacock KA (2011) Symbiosis in ecology and evolution. In: Gabbay DM, Thagard P, Woods J (eds) Handbook of the philosophy of science: philosophy of ecology. North Holland, San Diego, pp 219–250
Portier P (1918) Les Symbiotes. Masson, Paris
Pound R (1893) Symbiosis and mutualism. Am Nat 27(318):509–520
Pradeu T (2016a) The many faces of biological individuality. Biol Philos 31:761–773
Pradeu T (2016b) Organisms or biological individuals? Combining physiological and evolutionary individuality. Biol Philos 31:797–817
Queller DC, Strassmann JE (2009) Beyond society: the evolution of organismality. Philos Trans R Soc B 364:3143–3155
Queller DC, Strassmann JE (2016) Problems of multispecies organisms: endosymbionts to holobionts. Biol Philos 31:855–873
Relman DA (2012) Microbiology: learning about who we are. Nature 486:194–195
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Rosas-Pérez T, Vera-Ponce de León A, Ramírez-Puebla ST, Rincón-Rosales R, Martínez-Romer J, Dunn MF, Kondorosi E & Martínez-Romero E (2017) The Symbiome of Llaveia Cochineals (Hemiptera: Coccoidea: Monophlebidae) Includes a Gammaproteobacterial Cosymbiont Sodalis TME1 and the Known Candidatus Walczuchella monophlebidarum. In VDC Shields (ed.): Insect Physiology and Ecology. DOI: https://doi.org/10.5772/66442. Available from: https://mts.intechopen.com/books/insect-physiology-and-ecology/the-symbiome-of-llaveia-cochineals-hemiptera-coccoidea-monophlebidae-includes-a-gammaproteobacterial
Rosenberg E, Zilber-Rosenberg I (2014) TheHologenome concept. Springer, London
Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. MBio 7(2):e01395–e01315
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362
Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2(4):500–506
Roughgarden J, Gilbert SF, Rosenberg E, Zilber-Rosenberg I & Lloyd EA (2017). Holobionts as units of selection and a model of their population dynamics and evolution. Biological Theory
Sagan L (1967) On the origin of mitosing cells. Journal of Theoretical Biology 14: 225–274
Sapp J (1994) Evolution by association. A history of symbiosis. Oxford University Press, New York
Sapp J (2002) Paul Buchner (1886-1978) and hereditary symbiosis in insects. Int Microbiol 5(3):145–150
Sapp J (2003) Genesis: the evolution of biology. Oxford University Press, New York
Sapp J (2004) The dynamics of symbiosis: an historical overview. Can J Bot 82:1046–1056
Sapp J (2010) Saltational symbiosis. Theory Biosciences 129:125–133
Sapp J, Carrapiço F, Zolotonosov M (2002) Symbiogenesis. The hidden face of Constantin Merezhkowky. History and Philosophy of the Life Sciences 24(3/4):413–440
Schneider A (1897) The phenomena of Symbiosis. Minnesota Botanical Studies 1(9):923–948
Schwendener S (1868) Über die Beziehungen zwischen Algen und Flechtengonidien. Botanische Zeitung [Berlin]: 289–292
Shropshire JD, Bordenstein SR (2016) Speciation by symbiosis: the microbiome and behavior. MBio 7(2):e01785–e01715
Skillings D (2016) Holobionts and the ecology of organisms: multi-species communities or integrated individuals? Bio Philos 31:875–892
Sommer F, Bäckhed F (2013) The gut microbiota – masters manipulator of host development and physiology. Nat Rev Microbiol 11(4):227–238
Spencer H (1899) The principles of biology. D. Appleton & Co., New York
Stahl E (1877) Beiträge zur Entwickelungsgeschichte der Flechten (vols. 1 & 2). Leipzig: A Felix
Stencel A (2016) The relativity of Darwinian populations and the ecology of endosymbiosis. BiolPhilos 31:619–637
Taxis TM, 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. Nucleic Acids Res 43(20):9600–9612
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: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1(2):e00028–e00016
Trappe JM (2005) A. B. Frank and mycorrhizae: the challenge to evolutionary and ecologic theory. Mycorrhiza 15(4):277–281
Tripp EA, Zhans N, Schneider H, Huang Y, Mueller GM, Hu Z, Häggblom M, Bhattacharya D (2017) Reshaping Darwin’s tree: impact of the symbiome. TRENDS in Ecology and Evolution 32(8):552–555
Turpin W, Espín-García O, Xu W, Silverberg MS, Kevans D, Smith MI, Guttman DS, Griffiths A et al (2016) Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet 48(11):1413–1417
Van Beneden P-J (1876) Animal parasites and messmates. Henry S. King, London
Wallin IE (1927) Symbioticism and the origin of species. Williams & Wilkins Co., Baltimore
Wilkinson DM (2001) At cross purposes. Nature 412:485
Wilson RA, Barker M (2013) The biological notion of individual. In EN Zalta (ed.) The Stanford Encyclopedia of Philosophy. https://plato.stanford.edu/archives/spr2017/entries/biology-individual/
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenometheoryof evolution. FEMS Microbiol Rev:723–735
Zook D (2015) Symbiosis: Evolution’s co-author. In: Gontier N (ed) Reticulate Evolution. Springer, London, pp 41–80
Acknowledgments
I would like to thank Staffan Müller-Wille, Sabina Leonelli, Caglar Karaca, John Dupré, José Díez, who read previous versions of this manuscript and made helpful comment. Benjamin Smart is especially acknowledged for all his help and detailed comments in the final version of the manuscript. Finally, I would like to thank two anonymous reviewers for their comments, which clearly helped in improving the content and structure of the paper. This work was economically supported by the Spanish Ministry of Education (FFU16/02570) and the Spanish Ministry of Economy and Competitiveness (FFI2016-76799-P).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Suárez, J. ‘The importance of symbiosis in philosophy of biology: an analysis of the current debate on biological individuality and its historical roots’. Symbiosis 76, 77–96 (2018). https://doi.org/10.1007/s13199-018-0556-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-018-0556-1