Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion

Journal article : Review

Evolving multicellularity is easy, especially in phototrophs and osmotrophs whose multicells feed like unicells. Evolving animals was much harder and unique; probably only one pathway via benthic ‘zoophytes’ with pelagic ciliated larvae allowed trophic continuity from phagocytic protozoa to gut-endowed animals. Choanoflagellate protozoa produced sponges. Converting sponge flask cells mediating larval settling to synaptically controlled nematocysts arguably made Cnidaria. I replace Haeckel's gastraea theory by a sponge/coelenterate/bilaterian pathway: Placozoa, hydrozoan diploblasty and ctenophores were secondary; stem anthozoan developmental mutations arguably independently generated coelomate bilateria and ctenophores. I emphasize animal origin's conceptual aspects (selective, developmental) related to feeding modes, cell structure, phylogeny of related protozoa, sequence evidence, ecology and palaeontology. Epithelia and connective tissue could evolve only by compensating for dramatically lower feeding efficiency that differentiation into non-choanocytes entails. Consequentially, larger bodies enabled filtering more water for bacterial food and harbouring photosynthetic bacteria, together adding more food than cell differentiation sacrificed. A hypothetical presponge of sessile triploblastic sheets (connective tissue sandwiched between two choanocyte epithelia) evolved oogamy through selection for larger dispersive ciliated larvae to accelerate benthic trophic competence and overgrowing protozoan competitors. Extinct Vendozoa might be elaborations of this organismal grade with choanocyte-bearing epithelia, before poriferan water channels and cnidarian gut/nematocysts/synapses evolved. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

Authors: Cavalier-Smith, T

• Publication status: Published
• Peer review status: Peer reviewed
• Publisher: The Royal Society
• Journal: Philosophical Transactions of the Royal Society B: Biological Sciences
• Volume: 372
• Issue: 1713
• Pages: 20150476
• Article number: 20150476
• Publication date: 2017-02-05
• Acceptance date: 2016-09-05
• DOI: 10.1098/rstb.2015.0476
• EISSN: 1471-2970
• ISSN: 0962-8436
• Language: English
• Keywords: nematocyst; origin of bilateria; vendozoa; epithelial origin; selective advantages of cell differentiation; placozoa
• Subtype: Review