The origin of the Metazoa in the light of the Proterozoic fossil record

Abstract

Origin of the eukaryotic organisms (including the multicellular animals or Metazoa) is commonly considered to be related to growing oxygen content in the atmosphere up to a level that allows aerobic metabolism. Here it is suggested that oxygenation of the biosphere was not a permissive condition but rather a forcing factor that drove evolution towards the formation of complex biological systems. Growing concentration of free oxygen in conjunction with other geohistorical trends acted to chemically impoverish the ocean and atmosphere and made many of the chemical elements immobile or unavailable for metabolic processes. Of particular importance in this connection was the decreasing concentration in sea water of the heavy metals that demonstrate high catalytic ability and make an active center in many enzymes. Increasing biological complexity and the eukaryotization of the biosphere (origin of the eukaryotic cell, growing role of heterotrophy, increasing biodiversity, rise of multicellular organisms, lengthening of trophic chains, acceleration of biological recycling of the chemical elements, etc.) can be considered as an evolutionary response to the geochemical deterioration of the environment. Recent discoveries of the oldest megascopic eukaryotes, such as spiral Grypania (1.9 Ga), the necklace-like colonial organism of tissue-grade organization Horodyskia (1.5 Ga), vermiform Parmia (about 1.0 Ga) and Sinosabellidites (800 Ma ago) are consistent with the "molecular clock" models on an early origin of animals; metazoans were, however, confined to relatively cold and well oxygenated basins beyond the carbonate belt of the ocean until the end of the Proterozoic. Large and diverse invertebrates of the Vendian Period are known mostly from siliciclastic marine basins. This fauna is characterized by high density of the benthic populations and well established clades both at the diploblastic (e.g., Phylum Trilobozoa) and triploblastic (e.g., Phylum Proarticulata) grades of organization as well as some taxa related to the Paleozoic phyla. An organic skeleton preceded the rise of the mineralized skeleton in some metazoan phyla. Low temperature of the habitats inhibited biomineralization. Almost simultaneous development of the phosphatic, carbonate and siliceous skeletons in different metazoan groups at the beginning of the Cambrian Period some 545 Ma ago could be related to the colonization of the warm carbonate basins by the metazoans. An additional factor for the rapid diversification of the biomineralized phyla could be the growing length of the trophic chains brought about by the rapidly increasing biodiversity and the need for detoxification at the top of the trophic pyramid. Being the byproduct of detoxification, sclerites and spicules, hard mineralized shells and carapaces immediately became an important factor of morphological evolution and growing biodiversity, as well as the object of intensive selection under the growing pressure of predators. Explosive growth of morphophysiological diversity in metazoans during the Vendian and Cambrian had an enormous impact on evolution of other groups of organisms and on the environment.