Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

Abstract

Prerequisite for tracing nervous system evolution is understanding of the body plan, feeding behaviour and locomotion of the first animals in which neurons evolved. Here, a comprehensive scenario is presented for the diversification of cell types in early metazoans, which enhanced feeding efficiency and led to the emergence of larger animals that were able to move. Starting from cup-shaped, gastraea-like animals with outer and inner choanoflagellate-like cells, two major innovations are discussed that set the stage for nervous system evolution. First, the invention of a mucociliary sole entailed a switch from intra- to extracellular digestion and increased the concentration of nutrients flowing into the gastric cavity. In these animals, an initial nerve net may have evolved via division of labour from mechanosensory-contractile cells in the lateral body wall, enabling coordinated movement of the growing body that involved both mucociliary creeping and changes of body shape. Second, the inner surface of the animals folded into metameric series of gastric pouches, which optimized nutrient resorption and allowed larger body sizes. The concomitant acquisition of bilateral symmetry may have allowed more directed locomotion and, with more demanding coordinative tasks, triggered the evolution of specialized nervous subsystems. Animals of this organizational state would have resembled Ediacarian fossils such as Dickinsonia and may have been close to the cnidarian–bilaterian ancestor. In the bilaterian lineage, the mucociliary sole was used mostly for creeping, or frequently lost. One possible remnant is the enigmatic Reissner's fibre in the ventral neural tube of cephalochordates and vertebrates.

Ediacaran pre-placozoan diploblasts in the Avalonian biota: the role of chemosynthesis in the evolution of early animal life

“…Otherwise, the growth of extensive surfaces in direct contact with reducing pore waters makes no logical sense. Chemosynthetic feeding modes require no gut and are energetically efficient because there is no production of exoenzymes as required by the mucociliary digestive sole of a placozoan grade organism (Sperling & Vinther 2010;Arendt et al 2015). A phagotrophic or chemosymbiotic organism does not need to compete with smaller eukaryotes or prokaryotes for the products of extracellular digestion.…”

“…Epithelial surfaces of immotile Ediacaran chemosynthetic phagotrophs could, at their simplest, consist of cells with an apical microvillar layer, specialized in nutrient uptake. Chemosynthetic phagotrophy could therefore be considered to be an evolutionary precursor to the placozoan grade of organization, characterized by a digestive ventral epithelium (Arendt et al 2015) that requires, in its most simple form, mucociliary motility to find new food resources.…”

“…Epithelial surfaces involved in chemosynthetic phagotrophy require fewer cell types than a placozoan-like mucociliary sole that releases exoenzymes. Animals at the gastraeal or pre-gastraeal grade of organization have four cell types: mucocytes, glandular cells for digestive enzyme production, ciliary cells, and cells specialized in nutrient uptake (Arendt et al 2015). The placozoan Trichoplax secretes mucus to: (1) facilitate ciliary locomotion; (2) provide a substrate for micro-algal digestion; and (3) allow the cilia of the ventral surface to produce both co-ordinated motility and the churning action that facilitates ingestion (Smith et al 2015a).…”

“…McIlroy et al 2009). Feeding using a placozoan-like ventral digestive sole has been proposed as a stage in metazoan evolution that predates the evolution of a gut (Arendt et al 2015). Motile placozoans such as Trichoplax use ciliary gliding and amoeboid movement following the local digestion of microbial mats, as is invoked for the Ediacaran organisms Yorgia and Dickinsonia (Ivantsov & Malakovskaya 2002;Dzik 2003;Fedonkin 2003;Gehling et al 2005;Seilacher 2007;Sperling & Vinther 2010) on the basis of Epibaion trace fossils (Ivantsov 2013).…”

Introduction to ‘Origin and evolution of the nervous system’

“…However, as described by Kelava et al [33], recent work that is elucidating the molecular networks responsible for the development of an anthozoan nervous system reveals a conserved underpinning of nervous system development across Cnidaria and Bilateria, in particular with respect to genes that contribute to the determination of neuronal differentiation. When nervous systems first appeared is further discussed by Arendt et al [34] who provides a panorama of ideas regarding cell type diversification relating to the effectiveness of feeding, which he suggests resulted in the evolution of large motile animals, the internalization of ciliated digestive surfaces, and the consequent evolution of neurons that initially contributed to the control of the first gut. The proposition follows that further elaboration, in particular the evolution of gastric pouches, enabled natural selection to promote larger body mass and body organization that demanded greater coordination provided by a nervous system with greater differentiation of cell types and network organization.…”