Toward a New Understanding of Multicellularity

Marina Antonio, Dirk Schulze-Makuch


Multicellularity is a widespread development of life on Earth and so is the use of the term. The term multicellularity is currently used to characterize a broad spectrum of cellular manifestations, from unicellular symbiotic arrangements, to colonial gatherings and organisms that undergo cell specialization. These manifestations are remarkably distinct and therefore should have different designations. Here we divide multicellularity into facultative and obligate life cycles, reflecting the divergence between organisms that adopt multicellularity if environmentally triggered and organisms that are multicellular from conception and cannot complete their life cycle without undergoing a multicellular phase. We then compare multicellularity throughout the three domains of life and identify the circumstances involving the emergence of obligate multicellularity. It is here hypothesized that obligate multicellularity results from extended cooperation between different life entities adopted as a strategy to survive prolonged low-fitness periods.


multicellular; evolution; totipotency; Eukarya; Bacteria; Archaea


B.E. Schirrmeister, A. Antonelli, H.C. Bagheri, The Origin Of Multicellularity In Cyanobacteria, BMC Evolutionary Biology. 11 (2011) 45.

K. Stucken, U. John, A. Cembella, A.A. Murillo, K. Soto-Liebe, J.J. Fuentes-Valdés, M. Friedel, A.M. Plominsky, M. Vásquez, G. Glöckner, The Smallest Known Genomes Of Multicellular And Toxic Cyanobacteria: Comparison, Minimal Gene Sets For Linked Traits And The Evolutionary Implications, PLoS ONE. 5 (2010) 1-15.

C. Acquisti, J. Kleffe, S. Collins, Oxygen Content Of Transmembrane Proteins Over Macroevolutionary Time Scales, Nature. 445 (2007) 47-52.

P.C.J. Donoghue, J.B. Antcliffe, Origins Of Multicellularity, Nature. 466 (2010) 41-42.

R.K. Grosberg, R.R. Strathmann, The Evolution Of Multicellularity: A Minor Major Transition? Annual Review Ecology Evolution Systematics. 38 (2007) 621-54.

S.E. Prochnik, J. Umen, A.M. Nedelcu, et al., Genomic Analysis Of Organismal Complexity In The Multicellular Green Alga Volvox carteri, Science. 329 (2010) 223-226.

P. Baudouin-Cornu, Y. Surdin-Kerjan, P. Marlière, D. Thomas, Molecular Evolution Of Protein Atomic Composition, Science. 293 (2001) 297-300.

J.J. Elser, W.F. Fagan, S. Subramanian, S. Kumar, Signatures Of Ecological Resource Availability In The Animal And Plant Proteomes, Molecular Biology Evolution. 23 (2006) 1946-1951.

J.T. Bonner, First Signals: The Evolution Of Multicellular Development, Princeton University Press, New Jersey, 2000.

J.L. Payne, A.G. Boyer, J.H. Brown, S. Finnegan, M. Kowalewski, R.A. Krause Jr, S.K. Lyons, C.R. McClain, D.W. McShea, P.M. Novack-Gottshall, F.A. Smith, J.A. Stempien, S.C. Wang, Two-Phase Increase In The Maximum Size Of Life Over 3.5 Billion Years Reflects Biological Innovation And Environmental Opportunity, Proceedings National Academy of Sciences. 106 (2009) 24-27.

J.M. Smith, E. Szathmáry, The Major Transitions In Evolution, Oxford University Press, Great Britain, 1997.

G.M. Dunny, S.C. Winans, Cell-Cell Signaling In Bacteria, ASM Press, Washington, DC, 1999.

J.S. Webb, M. Givskov, S. Kjelleberg, Bacterial Biofilms: Prokaryotic Adventures In Multicellularity, Current Opinion In Microbiology. 6 (2003) 578-585.

K.J. Niklas, The Cell Walls That Bind The Tree Of Life, Bioscience. 54 (2004) 831-841.

N.J. Butterfield, Modes Of Pre-Ediacaran Multicellularity, Precambrian Research. 173 (2009) 201-211.

A. El Abani, S. Bengtson, D.E. Canfield, et al., Large Colonial Organisms With Coordinated Growth In Oxygenated Environments 2.1 Gyr Ago, Nature. 466 (2010) 100-104.

N. King, The Unicellular Ancestry Of Animal Development, Developmental Cell. 7 (2004) 313-325.

G. Bell, A.O. Mooers, Size And Complexity Among Multicellular Organisms, Biological Journal Of The Linnean Society. 60 (1997) 345-363.

A. Smith, An Inquiry Into The Nature And Causes Of The Wealth Of Nations. 1937, Reprint, New York, 1776.

C. Limoges, Milne-Edwards, Darwin, Durkheim And The Division Of Labor: A Case Study In The Reciprocal Conceptual Exchanges Between The Social And The Natural Sciences, in: I.B. Cohen (Eds.), The Natural Sciences And The Social Sciences, MIT Press, Cambridge, MA, 1994.

J.T. Bonner, Perspective: The Size-Complexity Rule, Evolution. 58 (2004) 1883-1890.

W. Dawid, Biology And Global Distribution Of Myxobacteria In Soils, FEMS Microbiology Reviews. 24 (2000) 403-427.

J. Pérez, A. Castañeda-García, H. Jenke-Kodama, R. Müller, J. Muñoz-Dorado, Eukaryotic-like Protein Kinases In The Prokaryotes And The Myxobacterial Kinome, Proceedings of the National Academy of Sciences. 41 (2008) 15950-15955.

F. Fiegna, Y.-T.N. Yu, S.V. Kadam, G.J. Velicer, Evolution Of An Obligate Social Cheater To A Superior Cooperator, Nature. 441 (2006) 310-314.

S. Fröls, M. Ajon, M. Wagner, D. Teichmann, B. Zolghadr, M. Folea, E.J. Boekema, A.J.M. Driessen, C. Schleper, S.-V. Albers, UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation, Molecular Microbiology. 70 (2008) 938-952.

A. Boetius, K. Rovenschlag, C.J. Schubert, D. Rickert, F. Widdel, A. Gieseke, R. Amann, B.B. Jøgensen, U. Witte, O. Pfannkuche, A marine microbial consortium apparently mediating anaerobic oxidation of methane, Nature. 407 (2000) 623-626.

C. LaPaglia, P.L. Hartzell, Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus, Applied Environmental Microbiology. 63 (1997) 3158-3163.

L.E. Mayerhofer, A.J.L. Macario, E.C. De Macario, Lamina, a Novel Multicellular Form of Methanosarcina mazei S-6, Journal of Bacteriology. 174 (1992) 309-314.

I. Ruiz-Trillo, A.J. Roger, G. Burger, M.W. Gray, B.F. Lang, A Phylogenomic Investigation Into The Origin Of Metazoa, Molecular Biology And Evolution. 25 (2008) 664-672.

C.S. Veerappan, Z. Avramova, E.N. Moriyama, Evolution Of SET-domain Protein Families In The Unicellular And Multicellular Ascomycota Fungi, BMC Evolutionary Biology. 8 (2008) 190.

S. Seiler, D. Justa-Schuch, Conserved Components, But Distinct Mechanisms For The Placement And Assembly Of The Cell Division Machinery In Unicellular And Filamentous Ascomycetes, Molecular Microbiology. (2010) doi: 10.1111/j.1365-2958.2010.07392.x.

B.N. Gantner, R.M. Simmons, D.M. Underhill, Dectin-1 Mediates Macrophage Recognition Of Candida albicans Yeast But Not Filaments, The EMBO Journal. 24 (2005) 1277-1286.

M. Whiteway, U. Oberholzer, Candida Morphogenesis And Host-pathogen Interactions, Current Opinion in Microbiology. 7 (2004) 350-357.

N. King, M.J. Westbrook, S.L. Young , et al., The Genome Of The Choanoflagellate Monosiga brevicollis And The Origin Of Metazoans, Nature. 451 (2008) 783-788.

Y. Segawa, H. Suga, N. Iwabe, C. Oneyama, T. Akagi, T. Miyata, M. Okada, Functional Development Of Src Tyrosine Kinases During Evolution From A Unicellular Ancestor To Multicellular Animals, Proceedings of the National Academy of Sciences. 103 (2006) 12021-12026.

J.D.I. Harper, J. Thuet, K.F. Lechtreck, A.R. Hardham, Proteins Related To Green Algal Striated Fiber Assemblin Are Present In Stramenopiles And Alveolates, Protoplasma. 236 (2009) 97-101.

K.-F. Lechtreck, M. Melkonian, SF-Assemblin, Striated Fibers, And Segmented Coiled Coil Proteins, Cell Motility and the Cytoskeleton. 41 (1998) 289-296.

D.K. Stoecker, A. Taniguchi, A.E. Michaels, Abundance Of Autotrophic, Mixotrophic And Heterotrophic Planktonic Ciliates In Shelf And Slope Waters, Marine Ecology Progress Series. 50 (1989) 241-254.

M. Putt, D.K. Stoecker, An Experimentally Determined Carbon: Volume Ratio For Marine “Oligotrichous” Ciliates From Estuarine And Coastal Waters, Limnology and Oceanography. 34 (1989 1097-1103.

J. Flegr, A Possible Role Of Intracellular Isoelectric Focusing In The Evolution Of Eukaryotic Cells And Multicellular Organisms, Journal Molecular Evolution. 69 (2009) 444-451.

M.B. Kok, S. Hak, W.J.M. Mulder, D.W.J. van der Schaft, G.J. Strijkers, K. Nicolay, Cellular Compartmentalization Of Internalized Paramagnetic Liposomes Strongly Influences Both T1 and T2 Relaxivity, Magnetic Resonance in Medicine. 61 (2009) 1022-1032.

E.M. Özbudak, O. Tassy, O. Pourquié, Spatiotemporal Compartmentalization Of Key Phisiological Processes During Muscle Precursor Differentiation, Proceedings of the National Academy of Sciences. 107 (2010) 4224-4229.

A. Annila, E. Annila, Why Did Life Emerge?, International Journal of Astrobiology. 7 (2008) 293-300.

C.H.M. Beck, Nature, Evolution, Culture, Free Will And Morals: A Thermodynamic Singularity. Library and Archives Canada. (2010) Retrieved from

V.R.I. Kaila, A. Annila, Natural Selection For Least Action, Proceedings of the Royal Society A. 464 (2008) 3055-3070.

T. Grönholm, A. Annila, Natural Distribution, Mathematical Biosciences. 210 (2007) 659-667.

V. Sharma, A. Annila, Natural Process – Natural Selection, Biophysical Chemistry. 127 (2007) 123-128.

J.M. Cock, L. Sterck, P. Rouzé, et al., The Ectocarpus Genome And The Independent Evolution Of Multicellularity In Brown Algae, Nature. 465 (2010) 617-621.

S.M. Dittami, D. Scornet, J.-L. Petit, B. Ségurens, C. Da Silva, E. Corre, M. Dondrup, K.-H. Glatting, R. König, L. Sterck, P. Rouzé, Y. Van de Peer, J.M. Cock, C. Boyen, T. Tonon, Global Expression Analysis Of The Brown Alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress, Genome Biology. 10 (2009) 66.1-66.20.

A. Le Bail, B. Billoud, N. Kowalczyk, M. Kowalczyk, M. Gicquel, S. Le Panse, S. Stewart, D. Scornet, J.M. Cock, K. Ljung, B. Charrier, Auxin Metabolism And Function In The Multicellular Bown Alga Ectocarpus siliculosus, Plant Physiology. 153 (2010) 128-144.

António, M.R.S. Cooperation: The Emergence and Maintenance of Biological Complexity. PhD Dissertation, Washington State University, Pullman, 2012.


  • There are currently no refbacks.