Evolution of Multicellularity

Abstract

Multicellularity has evolved multiple times, independently, in lineages from all three domains of life. The transition from a unicellular to a multicellular life‐style entails the integration of previously independent individuals into a new kind of individual. The emergence of individuality at the higher level requires the evolution of cooperative and altruistic behaviours, division of labour (including the separation of reproductive and somatic activities among cells), the reorganisation of basic life properties (such as immortality and totipotency), and the reorganisation of fitness (with cells specialising in one or the other fitness components – survival or reproduction). At a more mechanistic level, a new genotype–phenotype map has to be created to reflect the emergence of a new kind of individual. Notably, many traits associated with multicellularity appear to have involved the co‐option of genes and pathways already present in unicellular lineages. The evolution of multicellularity has been driven by a combination of selective pressures, developmental constraints and life history trade‐offs specific to each lineage.

Key Concepts:

  • The transition from a unicellular to a multicellular life‐style constitutes a transition in individuality, a process whereby a group of previously independent individuals become stably integrated into a new functional, physiological and reproductively autonomous and indivisible evolutionary unit – that is, a new individual.

  • The successful integration of previously independent individuals into a new kind of individual requires the evolution of cooperative and altruistic behaviours, division of labour, the reorganisation of basic life properties, and the reorganisation of fitness.

  • Multicellularity has evolved independently in at least 25 lineages from all three domains of life.

  • The evolution of multicellularity has been driven by a combination of selective pressures, developmental constraints and life history trade‐offs specific to each lineage.

  • Many traits associated with multicellularity involved the co‐option of genes and pathways already present in unicellular lineages.

Keywords: evolution; multicellularity; soma; altruism; cooperation; life history trade‐offs; gene co‐option; volvocine algae; Volvox

References

Abedin M and King N (2010) Diverse evolutionary paths to cell adhesion. Trends in Cell Biology 20: 734–742.

Aguirre J, Rios‐Momberg M, Hewitt D and Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends in Microbiology 13: 111–118.

Bell G (1985) The origin and early evolution of germ cells as illustrated by the Volvocales. In: Halvorson HO and Monroy A (eds) The Origin and Evolution of Sex, pp. 221–256. New York: Alan R. Liss, Inc.

Blackstone NW (2000) Redox control and the evolution of multicellularity. BioEssays 22: 947–953.

Bode HR (1996) The interstitial cell lineage of Hydra: a stem cell system that arose early in evolution. Journal of Cell Science 109: 1155–1164.

Bonner JT (2003) Evolution of development in the cellular slime molds. Evolution & Development 5: 305–313.

Boraas ME, Seale DB and Boxhorn JE (1998) Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evolutionary Ecology 12: 153–164.

Buss LW (1987) The Evolution of Individuality. Princeton, NJ: Princeton University Press.

Carr M, Leadbeater BSC, Hassan R, Nelson M and Baldauf SL (2008) Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proceedings of the National Academy of Sciences of the USA 105: 16641–16646.

Dayel MJ, Alegado RA, Fairclough SR et al. (2011) Cell differentiation and morphogenesis in the colony‐forming choanoflagellate Salpingoeca rosetta. Developmental Biology 357: 73–82.

Degnan BM, Vervoort M, Larroux C and Richards GS (2009) Early evolution of metazoan transcription factors. Current Opinion in Genetics & Development 19: 591–599.

Duncan L, Nishii I, Harryman A et al. (2007) The VARL gene family and the evolutionary origins of the master cell‐type regulatory gene, regA, in Volvox carteri. Journal of Molecular Evolution 65: 1–11.

Gavrilets S (2010) Rapid transition towards the division of labor via evolution of developmental plasticity. PLoS Computational Biology 6: e100805.

Grosberg RK and Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annual Review of Ecology, Evolution, and Systematics 38: 621–654.

Herron MD and Michod RE (2008) Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye. Evolution 62: 436–451.

Kaiser D (2001) Building a multicellular organism. Annual Reviews Genetics 35: 103–123.

King N, Hittinger CT and Carroll SB (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361–363.

Kirk DL (1995) Asymmetric division, cell size and germ‐soma specification in Volvox. Seminars in Developmental Biology 6: 369–379.

Kirk DL (1998) Volvox: Molecular Genetic Origins of Multicellularity and Cellular Differentiation. New York: Cambridge University Press.

Kirk DL, Baran GJ, Harper JF et al. (1987) Stage‐specific hypermutability of the reg A locus of Volvox, a gene regulating the germ‐soma dichotomy. Cell 18: 11–24.

Kirk M, Ransick A, McRae SE and Kirk DL (1993) The relationship between cell size and cell fate in Volvox carteri. Journal of Cell Biology 123: 191–208.

Kirk M, Stark K, Miller S et al. (1999) regA, a Volvox gene that plays a central role in germ soma differentiation, encodes a novel regulatory protein. Development 126: 639–647.

Koufopanou V (1994) The evolution of soma in the Volvocales. American Naturalist 143: 907–931.

Larson A, Kirk M and Kirk DL (1992) Molecular phylogeny of the volvocine flagellates. Molecular Biology and Evolution 9: 85–105.

Lurling M and Van Donk E (2000) Grazer‐induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88: 111–118.

Lynch M and Conery JS (2003) The origins of genome complexity. Science 302: 1401–1404.

Margulis L (1981) Symbiosis in Cell Evolution. Freeman: San Francisco.

Maynard Smith J and Szathmáry E (1997) The Major Transitions in Evolution. Oxford: Oxford University Press.

Meissner M, Stark K, Cresnar B, Kirk DL and Schmitt R (1999) Volvox germline‐specific genes that are putative targets of RegA repression encode chloroplast proteins. Current Genetics 36: 363–370.

Merchant SS, Prochnik SE, Vallon O et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–251.

Michod RE and Nedelcu AM (2003) On the reorganization of fitness during evolutionary transitions in individuality. Integrative and Comparative Biology 43: 64–73.

Michod RE and Roze D (2001) Cooperation and conflict in the evolution of multicellularity. Heredity 86: 1–7.

Michod RE (2006) The group covariance effect and fitness trade‐offs during evolutionary transitions in individuality. Proceedings of the National Academy of Sciences of the USA 103: 9113–9117.

Michod RE, Viossat Y, Solari CA, Hurand M and Nedelcu AM (2006) Life‐history evolution and the origin of multicellularity. Journal of Theoretical Biology 239: 257–272.

Morgan NC, Backiel T, Bretschko G et al. (1980) Secondary production. In: Le Cren ED and Lowe‐McConell RH (eds) The Functioning of Freshwater Ecosystems, pp. 247–340. Cambridge: Cambridge University Press.

Nedelcu AM (2009a) Comparative genomics of phylogenetically diverse unicellular eukaryotes provide new insights into the genetic basis for the evolution of the programmed cell death machinery. Journal of Molecular Evolution 68: 256–268.

Nedelcu AM (2009b) Environmentally induced responses co‐opted for reproductive altruism. Biology Letters 5: 805–808.

Nedelcu AM, Borza T and Lee RW (2006) A land plant‐specific multigene family in the unicellular mesostigma argues for its close relationship to streptophyta. Molecular Biology and Evolution 23: 1111–1015.

Nedelcu AM, Driscoll WW, Durand PM, Herron MD and Rashidi A (2011) On the paradigm of altruistic suicide in the unicellular world. Evolution 65: 3–20.

Nedelcu AM and Michod RE (2004) Evolvability, modularity, and individuality during the transition to multicellularity in volvocalean green algae. In: Schlosser A and Wagner G (eds) Modularity in Development and Evolution, pp. 466–489. Chicago, USA: University of Chicago Press.

Nedelcu AM and Michod RE (2006) The evolutionary origin of an altruistic gene. Molecular Biology and Evolution 23: 1460–1464

Nedelcu AM and Michod RE (2011) Molecular mechanisms of life history trade‐offs and the evolution of multicellular complexity in volvocalean green algae. In: Flatt T and Heyland A (eds) Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade‐Offs, pp. 271–283. New York: Oxford University Press.

Otsuka J (2008) A theoretical approach to the large‐scale evolution of multicellularity and cell differentiation. Journal of Theoretical Biology 255: 129–136.

Pfannschmidt T, Brautigam K, Wagner R et al. (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Annals of Botany 103: 599–607.

Pfeiffer T and Bonhoeffer S (2003) An evolutionary scenario for the transition to undifferentiated multicellularity. Proceedings of the National Academy of Sciences of the USA 100: 1095–1098.

Prochnik SE, Umen J, Nedelcu AM et al. (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329: 223–226.

Schaap P (2011) Evolution of developmental cyclic adenosine monophosphate signaling in the Dictyostelia from an amoebozoan stress response. Development, Growth & Differentiation 53: 452–462.

Schlichting CD (2003) Origins of differentiation via phenotypic plasticity. Evolution & Development 5: 98–105.

Sebe‐Pedros A, Roger AJ, Lang FB, King N and Ruiz‐Trillo I (2010) Ancient origin of the integrin‐mediated adhesion and signaling machinery. Proceedings of the National Academy of Sciences of the USA 107: 10142–10147.

Solari CA, Ganguly S, Kessler JO, Michod RE and Goldstein RE (2006a) Multicellularity and the functional interdependence of motility and molecular transport. Proceedings of the National Academy of Sciences of the USA 103: 1353–1358.

Solari CA, Kessler JO and Michod RE (2006b) A hydrodynamics approach to the evolution of multicellularity: flagellar motility and germ‐soma differentiation in volvocalean green algae. American Naturalist 167: 537–554.

Stanley SM (1973) Ecological theory for sudden origin of multicellular life in late precambrian – (adaptive radiation‐cambrian‐evolution‐paleontology‐predation). Proceedings of the National Academy of Sciences of the USA 70: 1486–1489.

Velicer GJ and Vos M (2009) Sociobiology of the Myxobacteria. Annual Review of Microbiology 63: 599–623.

Wagner GP and Altenberg L (1996) Complex adaptations and the evolution of evolvability. Evolution 50: 967–976.

Further Reading

King N, Westbrook MJ, Young SL et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783–788.

Knoll AH (2011) The multiple origins of complex multicellularity. Annual Review of Earth and Planetary Sciences 39: 217–239.

Mikhailov KV, Konstantinova AV, Nikitin MA et al. (2009) The origin of Metazoa: a transition from temporal to spatial cell differentiation. BioEssays 31: 758–768.

Rokas A (2008a) The molecular origins of multicellular transitions. Current Opinion in Genetics & Development 18: 472–478.

Rokas A (2008b) The origins of multicellularity and the early history of the genetic toolkit for animal development. Annual Review of Genetics 42: 235–251.

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How to Cite close
Nedelcu, Aurora M(Mar 2012) Evolution of Multicellularity. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023665]