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

Abstract

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’.

Animal origins and the Tonian Earth system

“…In this sense, the transition to complex multicellularity directly from unicellular, heterotrophic phagotrophs lacking cell walls (i.e. the evolution of animal multicellularity) is an evolutionary singularity [19]. In contrast, fungi have obtained complex multicellularity at least two times from unicellular osmotrophs with cell walls [20], and algae have evolved complex multicellularity at least three times from unicellular phototrophs with cell walls [21].…”

“…Although the unicellular ancestors of multicellular animals were probably capable of osmotrophy -some choanoflagellates, for instance, can subsist off dissolved organics in culture [22] and in nature [23,24] -flagellates and other protozoa rely primarily on the phagocytosis of other cells for nutrition [25,26]. The earliest multicellular stem-group metazoans, like modern sponges, most probably retained and relied on this ancestral phagotrophic feeding mode before the advent of gut-bearing animals, which feed osmotrophically at the cellular level and utilize phagocytosis for non-trophic functions, such as programmed cell death and immune defense [6,18,19]. In contrast, multicellular basidiomycetes and ascomycetes, the only other complex multicellular heterotrophs (the other complex multicellular lineages are all phototrophs), evolved directly from obligate osmotrophs with chitinous cell walls [20].…”

“…In contrast, multicellular basidiomycetes and ascomycetes, the only other complex multicellular heterotrophs (the other complex multicellular lineages are all phototrophs), evolved directly from obligate osmotrophs with chitinous cell walls [20]. Indeed, the unique trophic and cytological ancestry of animals exemplifies the uniqueness of animal multicellularity and potentially explains why animal-grade multicellularity evolved only once in the history of life [19].…”

“…This cytological constraint manifests in animals, where terminally differentiated cell types with flagella are unable to divide [27,29]. While other multicellular phagotrophs, such as cellular slime molds, aggregate to form multicellular fruiting bodies, these structures are used for spore dispersal rather than feeding, thereby circumventing the need for phagotrophic feeding while in a multicellular state [19,30]. Colonial choanoflagellates, in contrast with aggregating slime molds, retain the ability to phagocytose prey while in a colonial organization [19], but lack the ability to simultaneously divide, locomote, and feed on the cellular level, as their flagella necessarily retract for mitotic division [26,27].…”

Perspectives on the history of evo-devo and the contemporary research landscape in the genomics era

“…The other major sections illustrate how genomics and other approaches are being applied to gain insights into the evolutionary origins of morphological diversity. Major morphological transitions and innovations are considered first with articles on the origins of animal multicellularity from a classical perspective by Cavalier-Smith [52] and illustrating the impact of genomics by Babonis & Martindale [20] and an article on the evolution of land plants by Harrison [53]; the major transition that created the unique mammalian middle ear is discussed by Tucker [46]. The next section focuses on diversification and modifications of morphology as exemplified by tetrapod limbs by Saxena et al [54], flowers by Pam Soltis and co-workers [55], cranial shape in birds by Abzhanov and co-workers [45] and wing coloration patterns in butterflies by Jiggins et al [56].…”