Cambrian Explosion

Abstract

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 , 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., 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 with permission from Springer. (c)–(e) Reproduced from Fernàndez‐Busquets et al. with permission from Oxford University Press. (f) and (g) Reproduced with permission from Sabella et al., 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., 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 . (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 . (b) Reproduced from Fernàndez‐Busquets et al. with permission from Oxford University Press.

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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]