A non-bilaterian perspective on the development and evolution of animal digestive systems

Abstract

Digestive systems and extracellular digestion are key animal features, but their emergence during early animal evolution is currently poorly understood. As the last common ancestor of non-bilaterian animal groups (sponges, ctenophores, placozoans and cnidarians) dates back to the beginning of animal life, their study and comparison provides important insights into the early evolution of digestive systems and functions. Here, I have compiled an overview of the development and cell biology of digestive tissues in non-bilaterian animals. I will highlight the fundamental differences between extracellular and intracellular digestive processes, and how these are distributed among animals. Cnidarians (e.g. sea anemones, corals, jellyfish), the phylogenetic outgroup of bilaterians (e.g. vertebrates, flies, annelids), occupy a key position to reconstruct the evolution of bilaterian gut evolution. A major focus will therefore lie on the development and cell biology of digestive tissues in cnidarians, especially sea anemones, and how they compare to bilaterian gut tissues. In that context, I will also review how a recent study on the gastrula fate map of the sea anemone Nematostella vectensis challenges our long-standing conceptions on the evolution of cnidarian and bilaterian germ layers and guts.

Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals

“…It is possible that Syssomonas secretes hydrolytic enzymes that provide near-membrane extracellular digestion. The appearance of extracellular digestion is considered to be a major step in animal evolution [57], since it is central to the breakdown of many organic molecules when combined with the direct absorption of nutrient monomers by the gut epithelia using transmembrane transport in animals [58].…”

Structure, development and evolution of the digestive system

“…For some bilateran clades, in particular annelids (Kermack 1955) and echinoderms (Chia and Koss 1991), motile macrophages (coelomocytes) also become associated with the intestinal epithelium, where they could be involved in immune functions, as well as food uptake. An intriguing evolutionary scenario, based on recent studies in cnidarians, is proposed by Steinmetz (2019;this issue), according to which the phagocytes and other cell types of the endoderm of the cnidarianbilateran ancestor gave rise to the bilaterian mesoderm; the bilaterian endoderm and its products, including gland cells and endocrine cells, evolved from the ectoderm of the cnidarian-bilateran ancestor. This sequence of events would explain how endodermal phagocytes, initially involved in food uptake in the cnidarian-bilateran ancestor, evolved into macrophages in the bilaterian lineage.…”

“…and Mayorova (2019; Placozoa), Godefroy et al (2019; Porifera), Gavilán et al (2019; Xenacoelomorpha), Lobo-da-Cunha (2019; Mollusca), Štrus et al (2019; Crustacea) andCaccia et al (2019; Hexapoda) and for prebilaterian and bilaterian clades in more general, bySteinmetz (2019) andHartenstein and Martinez (2019), respectively.…”

Cell shape changes during larval body plan development in Clytia hemisphaerica

“…NvFoxA is expressed early during blastopore formation in the same domain as NvBra (Fritzenwanker et al, 2004;Magie et al, 2007), later giving rise to the pharyngeal ectoderm. Cells of his domain will develop exocrine digestive functions, linking it evolutionarily to endoderm domains in bilaterian species (Steinmetz, 2019;Steinmetz et al, 2017). In contrast Amfkh is only transiently expressed in the developing blastopore, and this pattern is spatially and temporally separated from its later expression in the pharynx (Hayward et al, 2015).…”