Cambrian Explosion

Xavier Fernàndez‐Busquets, Institute for Bioengineering of Catalonia, Barcelona, Spain

Published online: September 2010

DOI: 10.1002/9780470015902.a0022875

The Cambrian explosion of life was a relatively short period c. 540 Mya when a sudden acceleration in evolution led to the rise of multicellular animals, but the cause of this key biological event remains elusive. Diverse environmental, developmental and ecological causes have been put forward as potential triggering events, but none of them has so far succeeded in obtaining widespread acceptance. Probably the correct answer has to be sought in a unifying theory capable of taking into account several of the most likely candidate factors and using adequate physiological experimental models such as marine sponges, the oldest extant Precambrian metazoan phylum. The Cambrian explosion might have been unleashed by the coincidence in time of primitive metazoans endowed with self-/non-self-recognition and of a surge in sea water calcium that increased the binding forces between their calcium-dependent cell adhesion molecules.

Key Concepts:

  • The Cambrian explosion is widely regarded as one of the most relevant episodes in the history of life on Earth, when about half of living animal phyla first appear in the fossil record.
  • The proposals to explain the occurrence of the Cambrian explosion in terms of why and when it happened have been various and usually fall within environmental, developmental and ecological reasons.
  • The triggering event of the Cambrian explosion likely has not only environmental, developmental or ecological causes, but a mixture of them all.
  • The development of self-/nonself-recognition in primitive metazoans was a necessary innovation for the consolidation of multicellularity.
  • The molecular basis of the Cambrian explosion should be understood based on mechanisms which could generate organismal diversity by utilising pre-existing genes but not by creating new genes with novel function.
  • Marine sponges are an ideal candidate model to provide answers dealing with molecular, cellular, organismal and populational aspects of the Cambrian explosion.
  • Calcium-based cell adhesion is essential for the integrity of marine sponges.
  • There was a well-referenced substantial increase in sea water calcium levels around the beginning of the Cambrian period.
  • The calcium increase in Cambrian oceans coincided with the existence of primitive sessile metazoans, endowed with allogeneic recognition and carrying cell adhesion molecules which had significantly longer dissociation times at the new calcium concentrations.
  • The Cambrian explosion might have been triggered by the coincidence in time of primitive animals endowed with self-/nonself-recognition and of a surge in sea water calcium that increased the binding forces between their calcium-dependent cell adhesion molecules.

Keywords: biogeochemistry; Cambrian explosion; carbohydrates; cell adhesion; multicellularity; ocean calcium content; origin of Metazoa; Porifera (sponges); proteoglycans; self-/nonself-recognition

Figure 1. Animal diversity across the Proterozoic–Cambrian transition. The green curve at the bottom of the graph represents the carbon isotopic record for terminal Proterozoic and Cambrian carbonates. Reproduced from Knoll and Carroll (1999), with permission from the American Association for the Advancement of Science.
Figure 2. Self-/nonself-recognition in an evolutionary context. (a) Scheme representing the fate of encounters between multicellular aggregates in the absence of self-/nonself-recognition. (b) Scheme representing how self-/nonself-recognition could speed up metazoan evolution. Reproduced from Fernàndez-Busquets et al. (2009), with permission from Oxford University Press.
Figure 3. Specificity of sponge cell recognition. (a) The marine sponges Microciona prolifera (orange) and Halichondria panicea (brownish) in the wild. (b) Reaggregation of a mixture of mechanically dissociated cells from M. prolifera (orange) and H. panicea (green) after ~30 min of gentle stirring. (c) Atomic force microscope images of M. prolifera aggregation factors (MAF), the extracellular proteoglycan molecules responsible for species-specific sponge cell adhesion. (d) In its native form, MAF has the structure of a sunburst where the ring is formed by ~20 units of the MAFp3 protein (empty circles), each noncovalently linked to a unit of the MAFp4 protein (a MAF ‘arm’). If the ring of MAF were open, the resulting structure is analogous to a classical proteoglycan, with MAFp3 and MAFp4 in place of link protein and proteoglycan monomer respectively. (e) Model of the MAF interactions responsible for species-specificity of cell adhesion: carbohydrates on MAFp4 bind receptors on the cell membrane whereas the g200 glycan on MAFp3 self-interacts in a calcium-dependent manner. For clarity, both MAF molecules are represented linearised. (f) Set up of an allogeneic graft. Note the lightly coloured zone of contact (arrowhead) due to grey cell migration towards this region. (g) Low magnification image of an allograft section stained for grey cells. Note the intensity of the signal in the zone of contact (arrowhead) and the path of the needle that held the graft together (arrow). (a) and (b) Reproduced from Fernàndez-Busquets and Burger (2003) with permission from Springer. (c)–(e) Reproduced from Fernàndez-Busquets et al. (2009) with permission from Oxford University Press. (f) and (g) Reproduced with permission from Sabella et al. (2007), Copyright 2007, The American Association of Immunologists, Inc.
Figure 4. Proposal for a sponge self-recognition-based histocompatibility system. In this model, the recognition of cell-bound nonvariant receptors would elicit an immune response (a) unless the simultaneous binding of membrane-bound or soluble self-markers acts as an inhibitory signal (b). The rejection mechanism would involve cytotoxic processes and a reduction in cell motility triggered by increased expression of cell adhesion molecules. This scenario can have its molecular basis in the existence of a highly polymorphic family of pairs of cell adhesion coevolved ligand-receptors (a1b1, a2b2, etc.), such that the probability of any given combination (e.g. 1+2 if each individual had two loci coding for polymorphic receptors) is sufficiently low to explain the very high percentage of tissue histoincompatibility that is found in sponges. Reproduced with permission from Sabella et al. (2007), Copyright 2007, The American Association of Immunologists, Inc.
Figure 5. A unifying hypothesis for the Cambrian explosion trigger. (a) Plots of dissolved calcium and sulfate in seawater from Phanerozoic time based on modelling data from Berner (2004). (b) Cartoon summarising the effect of high and low calcium concentrations on the integrity of primitive sessile metazoans having calcium-dependent cell adhesion molecules. Early metazoans capable of self-/nonself-discrimination could have developed cell adhesion that at the low calcium content of Precambrian seas was too short-lived to keep cells together for a time long enough to permit the stable persistence of multicellular individuals. (a) Reproduced with permission from Berner (2004). (b) Reproduced from Fernàndez-Busquets et al. (2009) with permission from Oxford University Press.
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 References
    Averof M and Patel NH (1997) Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388: 682–686.
    Bengtson S (2002) Origins and early evolution of predation. Paleontological Society Papers 8: 289–317.
    Berner RA (2004) A model for calcium, magnesium and sulfate in seawater over Phanerozoic time. American Journal of Science 304: 438–453.
    Brennan ST, Lowenstein TK and Horita J (2004) Seawater chemistry and the advent of biocalcification. Geology 32: 473–476.
    Bucior I, Scheuring S, Engel A and Burger MM (2004) Carbohydrate-carbohydrate interaction provides adhesion force and specificity for cellular recognition. Journal of Cell Biology 165: 529–537.
    Budd GE (2008) The earliest fossil record of the animals and its significance. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363: 1425–1434.
    Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proceedings of the National Academy of Sciences of the USA 79: 5337–5341.
    book Butterfield NJ (2001) "Ecology and evolution of Cambrian plankton". In: Zhuravlev AY and Riding R (eds) The Ecology of the Cambrian Radiation, pp. 200–216. New York: Columbia University Press.
    book Carroll SB, Grenier JK and Weatherbee SD (2001) From DNA to Diversity. Oxford: Blackwell Science.
    Cauldwell CB, Henkart P and Humphreys T (1973) Physical properties of sponge aggregation factor. A unique proteoglycan complex. Biochemistry 12: 3051–3055.
    Chadwick-Furman NE and Weissman IL (1995) Life history plasticity in chimaeras of the colonial ascidian Botryllus schlosseri. Proceedings of the Royal Society of London. Series B 262: 157–162.
    Conway Morris S (2006) Darwin's dilemma: the realities of the Cambrian ‘explosion’. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 361: 1069–1083.
    Dammer U, Popescu O, Wagner P et al. (1995) Binding strength between cell adhesion proteoglycans measured by atomic force microscopy. Science 267: 1173–1175.
    Dunn CW, Hejnol A, Matus DQ et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745–749.
    Elkinton JR (1957) The relationship of water and salt. Proceedings of the Nutrition Society 16: 113–118.
    Fernàndez-Busquets X and Burger MM (1997) The main protein of the aggregation factor responsible for species-specific cell adhesion in the marine sponge Microciona prolifera is highly polymorphic. Journal of Biological Chemistry 272: 27839–27847.
    Fernàndez-Busquets X and Burger MM (2003) Circular proteoglycans from sponges: first members of the spongican family. Cellular and Molecular Life Sciences 60: 88–112.
    Fernàndez-Busquets X, Körnig A, Bucior I, Burger MM and Anselmetti D (2009) Self-recognition and Ca2+-dependent carbohydrate-carbohydrate cell adhesion provide clues to the Cambrian explosion. Molecular Biology and Evolution 26: 2551–2561.
    Fernàndez-Busquets X, Kuhns WJ, Simpson TL et al. (2002) Cell adhesion-related proteins as specific markers of sponge cell types involved in allogeneic recognition. Developmental and Comparative Immunology 26: 313–323.
    Finnerty JR, Pang K, Burton P, Paulson D and Martindale MQ (2004) Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304: 1335–1337.
    Gauthier M and Degnan BM (2008) Partitioning of genetically distinct cell populations in chimeric juveniles of the sponge Amphimedon queenslandica. Developmental and Comparative Immunology 32: 1270–1280.
    Hoffman PF, Kaufman AJ, Halverson GP and Schrag DP (1998) A Neoproterozoic snowball Earth. Science 281: 1342–1346.
    Jarchow J, Fritz J, Anselmetti D et al. (2000) Supramolecular structure of a new family of circular proteoglycans mediating cell adhesion in sponges. Journal of Structural Biology 132: 95–105.
    Kerr RA (2002) Paleoceanography. Inconstant ancient seas and life's path. Science 298: 1165–1166.
    King N, Hittinger CT and Carroll SB (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301: 361–363.
    book Kirschvink JL (1992) "Late Proterozoic low-latitude global glaciation: the snowball Earth". In: Schopf JW and Klein C (eds) The Proterozoic Biosphere: A Multidisciplinary Study, pp. 51–58. Cambridge, UK: Cambridge University Press.
    Kirschvink JL and Raub TD (2003) A methane fuse for the Cambrian explosion: carbon cycles and true polar wander. Comptes Rendus Geosciences 335: 65–78.
    Kirschvink JL, Ripperdan RL and Evans DA (1997) Evidence for a large-scale reorganization of early Cambrian continental masses by inertial interchange true polar wander. Science 277: 541–545.
    Knauth LP (2005) Temperature and salinity history of the Precambrian ocean: implications for the course of microbial evolution. Palaeogeography, Palaeoclimatology, Palaeoecology 219: 53–59.
    Knoll AH and Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284: 2129–2137.
    Love GD, Grosjean E, Stalvies C et al. (2009) Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457: 718–721.
    Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Annual Review of Earth and Planetary Sciences 34: 355–384.
    Müller WEG and Müller IM (2003) Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integrative and Comparative Biology 43: 281–292.
    Ohno S (1997) The reason for as well as the consequence of the Cambrian explosion in animal evolution. Journal of Molecular Evolution 44(suppl. 1): S23–S27.
    Ono K, Suga H, Iwabe N, Kuma K and Miyata T (1999) Multiple protein tyrosine phosphatases in sponges and explosive gene duplication in the early evolution of animals before the parazoan-eumetazoan split. Journal of Molecular Evolution 48: 654–662.
    Peterson KJ, Cotton JA, Gehling JG and Pisani D (2008) The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363: 1435–1443.
    Peterson KJ and Davidson EH (2000) Regulatory evolution and the origin of the bilaterians. Proceedings of the National Academy of Sciences of the USA 97: 4430–4433.
    Peterson KJ, McPeek MA and Evans DAD (2005) Tempo and mode of early animal evolution: inferences from rocks, Hox and molecular clocks. Paleobiology 31(suppl.): 36–55.
    Rinaudo M (2006) Non-covalent interactions in polysaccharide systems. Macromolecular Bioscience 6: 590–610.
    Ruiz-Trillo I, Roger AJ, Burger G, Gray MW and Lang BF (2008) A phylogenomic investigation into the origin of Metazoa. Molecular Biology and Evolution 25: 664–672.
    Sabella C, Faszewski E, Himic L et al. (2007) Cyclosporin A suspends transplantation reactions in the marine sponge Microciona prolifera. Journal of Immunology 179: 5927–5935.
    Shen B, Dong L, Xiao S and Kowalewski M (2008) The Avalon explosion: evolution of Ediacara morphospace. Science 319: 81–84.
    Simkiss K (1977) Biomineralization and detoxification. Calcified Tissue Research 24: 199–200.
    book Simpson TL (1984) The Cell Biology of Sponges. New York: Springer.
    Solé RV, Fernández P and Kauffman SA (2003) Adaptive walks in a gene network model of morphogenesis: insights into the Cambrian explosion. International Journal of Developmental Biology 47: 685–693.
    Stanley SM (1973) An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences of the USA 70: 1486–1489.
    Steinberg MS and Garrod DR (1975) Observations on the sorting-out of embryonic cells in monolayer culture. Journal of Cell Science 18: 385–403.
    Stoner DS and Weissman IL (1996) Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. Proceedings of the National Academy of Sciences of the USA 93: 15254–15259.
    book Valentine JW (1986) "Fossil record of the origin of Baupläne and its implications". In: Raup DM and Jablonski D (eds) Patterns and Processes in the History of Life, pp. 209–231. New York: Springer.
    Valentine JW (1995) Why no new phyla after the Cambrian? Genome and ecospace hypotheses revisited. Palaios 10: 190–194.
    Valentine JW and Jablonski D (2003) Morphological and developmental macroevolution: a paleontological perspective. International Journal of Developmental Biology 47: 517–522.
 Further Reading
    book Conway Morris S (1998) The Crucible of Creation. Oxford: Oxford University Press.
    book Davidson EH (2001) Genomic Regulatory Systems: Development and Evolution. San Diego: Academic.
    book Dawkins R (1976) The Selfish Gene. Oxford: Oxford University Press.
    book Gould SJ (2000) Wonderful Life. The Burgess Shale and the Nature of History. London: Vintage.
    Müller WE (2001) How was metazoan threshold crossed? The hypothetical Urmetazoa. Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology 129: 433–460.
    book Raff RA (1996) The Shape of Life. Chicago: University of Chicago Press.
    book Valentine JW (2004) On the Origin of Phyla. Chicago: University of Chicago Press.
    book Vermeij GJ (2004) Nature: An Economic History. Princeton, NJ: Princeton University Press.

Related Sub-Topics:

Diversification of Plants and Animals | Macroevolution | Evolution Rates
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Article Title: Cambrian Explosion
 
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Fernàndez‐Busquets, Xavier(Sep 2010) Cambrian Explosion. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022875]