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.
Highlights
Nutrient availability is rate limiting for most metabolic and cellular processes such as cell growth, cell division, motility or sensory activities
Transmembrane nutrient uptake from the environment typically involves transporters for amino acids or sugar monomers, which are shared between animals, plants and fungi (Wilson-O'Brien et al 2010; Wipf et al 2002). These are used in gut enterocytes as well as peripheral tissues of many bilaterian animals to take up nutrients from the digestive tube or blood stream
The functional similarities between the through-guts of ctenophores and bilaterians raised speculations about their common ancestry, but the lack of diagnostic genes for cnidarian or bilaterian pharynx, midgut or anus in ctenophores makes a comparison of these regions on a molecular level currently difficult (Hejnol and Martin-Duran 2015; Steinmetz et al 2017)
Summary
Nutrient availability is rate limiting for most metabolic and cellular processes such as cell growth, cell division, motility or sensory activities. The functional similarities between the through-guts of ctenophores and bilaterians raised speculations about their common ancestry, but the lack of diagnostic genes for cnidarian or bilaterian pharynx, midgut or anus (e.g. foxA, hex, nkx2.1, evx, goosecoid) in ctenophores makes a comparison of these regions on a molecular level currently difficult (Hejnol and Martin-Duran 2015; Steinmetz et al 2017) This phylum is represented by Trichoplax adhaerens and a few cryptic species, and most likely forms the phylogenetic sister group of cnidarians and bilaterians (Fig. 1b) (Osigus et al 2019; Srivastava et al 2008; Voigt et al 2004). The specification of exocrine cells within the ectoderm near the blastopore margin suggests an ancestral digestive or protective (defence against pathogens) function of this region, as partly proposed previously in the ‘mucociliary sole’ concept (Arendt et al 2015)
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