Cell and Tissue Research (2019) 377:369–382 https://doi.org/10.1007/s00441-019-03038-2 REVIEW The digestive system of xenacoelomorphs B. Gavilán1 & S. G. Sprecher2 & V. Hartenstein3 & P. Martinez 1,4 Received: 21 February 2019 /Accepted: 16 April 2019 /Published online: 16 May 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Interest in the study of Xenacoelomorpha has recently been revived due to realization of its key phylogenetic position as the putative sister group of the remaining Bilateria. Phylogenomic studies have attracted the attention of researchers interested in the evolution of animals and the origin of novelties. However, it is clear that a proper understanding of novelties can only be gained in the context of thorough descriptions of the anatomy of the different members of this phylum. A considerable literature, based mainly on conventional histological techniques, describes different aspects of xenacoelomorphs’ tissue architecture. However, the focus has been somewhat uneven; some tissues, such as the neuro-muscular system, are relatively well described in most groups, whereas others, including the digestive system, are only poorly understood. Our lack of knowledge of the xenacoelomorph digestive system is exacerbated by the assumption that, at least in Acoela, which possess a syncytial gut, the digestive system is a derived and specialized tissue with little bearing on what is observed in other bilaterian animals. Here, we try to remedy this lack of attention by revisiting the different studies of the xenacoelomorph digestive system, and we discuss the diversity present in the light of new evolutionary knowledge. Keywords Xenacoelomorpha . Xenoturbella . Nemertodermatida . Acoela . Digestive system . Syncytium . Lumen . Ultrastructure Introduction this is not a complete consensus since some researchers have suggested an alternative view of xenacoelomorphs as the most Xenacoelomorphs have become a group of animals that is basal deuterostomian clade (Philippe et al. 2011). While most central to many debates of the evolutionary origin of molecular phylogenies agree on the monophyly of Bilateria. Though relatively unknown, their key position as xenacoelomorpha (i.e., Philippe et al. 2011), there is still some the sister group of the remaining bilaterians suggests they have incongruence in the morphology (such as in the spermatozoa) intrinsic value as putative proxies for the origin of many that challenges this view (see Buckland-Nicks et al. 2018). bilaterian novelties; see Baguñà and Riutort (2004)and Xenacoelomorpha is composed of three major clades: Hejnol and Pang (2016). It is important to state, though, that Acoela, Nemertodermatida and Xenoturbellida. The first two constitute Acoelomorpha, the sister clade of Xenoturbellida. The majority of species in this phylum are * V. Hartenstein marine animals and of all the nominal species recognized [email protected] today, more than 90% belong to Acoela. Nemertodermatida * P. Martinez and Xenoturbellida are represented by only a few species, [email protected] though there are many others recognized as cryptic and prob- 1 Departament de Genètica, Microbiologia i Estadística, Universitat de ably inhabitants of unexplored habitats (Meyer-Wachsmuth Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain et al. 2014; Arroyo et al. 2016). Xenacoelomorphs have al- B ^ 2 Department of Biology, University of Fribourg, 10, ch. Du Musée, ways been considered as having a simple morphology 1700 Fribourg, Switzerland (Achatz et al. 2013;Hejnol2015). They are all characterized 3 Department of Biology, University of California, Los Angeles, CA, by the presence of a single digestive opening, located at dif- USA ferent positions along the major body axis, with ciliated epi- 4 Institut Català de Recerca i Estudis Avançats (ICREA), thelia and they are innervated by a basiepidermal net of neu- Barcelona, Spain rons, which are in most cases, condensed, to different 370 Cell Tissue Res (2019) 377:369–382 degrees, at the anterior end of the animal (Achatz and along the walls (defined as necrotic digestion by O. Raikova) Martinez 2012; Martinez et al. 2017). The nervous system Actinoposthia beklemischevi (Raikova 1987); (4) central lu- includes a statocyst at the frontal end plus, in some cases, a men and permanent syncytial structures along the walls— pair of eyespots. Xenacoelomorphs move by gliding in sand Hofsteniidae, Haploposthia opisthorchis, Aphanostoma and mud substrates, using their epidermal cilia. A film of virescens and Paedomecynostomum (Smith 1981). mucus produced by scattered ventral glands helps locomo- Interestingly, in some families, species with lumen and others tion. Muscles are preferentially organized as bands of circu- with syncytium can be detected, suggesting even greater flex- lar, longitudinal and oblique fibers. Additionally, dorsoventral ibility in the organization of these digestive systems. muscles are prevalent in most animals (Semmler et al. 2008; The cellular organization of the different members of Børve and Hejnol 2014). Many acoels are able to regenerate Xenacoelomorpha has been studied but in this case, we have different body parts (Perea-Atienza et al. 2013; Srivastava few extensive, ultrastructural data except for those relating to et al. 2014) and some of them use regeneration as a repro- some acoels. In Xenoturbellida, the cells in the digestive epi- ductive strategy (Sikes and Bely 2008). Similar capacities are thelium were initially described as syncytial (Westblad not known in xenoturbellids and nemertodermatids. 1949b); though, in more recent papers (Israelsson 1999, 2006), the gut lining is described as a gastrodermis with indi- General characteristics of the xenacoelomorph viduated cells, organized as an epithelia. Within the digestive systems gastrodermis, there are numerous small granular glands. In members of the Nemertodermatida, the intestine seems to be The digestive system (originally named Bcentral formed of two different cell types: the so-called amoeboid and parenchyma^) of xenacoelomorphs, which is a sack-like gut, gland cells (traditionally called BKörnerkolben^ auctorem, or has been regarded as peculiar in terms of its ultrastructure and mucous cells). cellular composition. The assumed phylogenetic position of In the syncytial acoels (most of the species described to this phylum as the sister group of the remaining bilaterians has date), two major cell types seem to be present: the cellular prompted some authors to consider that this peculiar architec- mass that constitutes the central syncytium and the surround- ture could represent an ancestral condition for bilateria. This is ing, wrapping cells. There are two (e.g., Diopisthoporus c.f. consistent with the overall organization of the Xenoturbellida longitubus)orthree(e.g.,Convoluta convoluta)typesof gut: a simple epithelial gut with a single opening and a central wrapping cells reported. The distribution of these cells seems empty cavity. However, Acoelomorpha present different ar- to vary among species. Recently and in the case of I. pulchra, rangements of cells and the progressive loss of a central cavity an excretory function for some of these cells has been in favor of a consolidated central syncytium of digestive cells, suggested. which is definitely a derived condition within the phylum. In There are a few other cases where further specialization of fact, the syncytial state of the central parenchyma in Acoela the gut is observed (e.g., Actinoposthia beklemischevi) where has been regarded as a specialization corresponding to the the arrangement and types of cells seem slightly different, with intracellular digestion of food items that are too large to be the presence of necrotic fragments contributing to the histol- digested intracellularly in a single cell (Mamkaev and Seravin ogy of the central tissue. 1963;Kozloff1972). The diversity and peculiarity of the different As with many other anatomical structures (i.e., position of xenacoelomorph digestive systems are described in more de- the mouth, arrangement of muscles and neural components tail in the next sections. and the copulatory organs; see Achatz et al. (2013), the struc- ture of the digestive system in Xenacoelomorpha presents The digestive system of Xenoturbellida considerable variation, a feature that some consider a reflec- tion of plesiomorphy [called the BMamkaev principle^ Xenoturbellida is represented by a small number of marine (Mamkaev 1986), by Haszprunar (Haszprunar 2015)]. As species, mostly living at considerable depths: from 50 to mentioned above, Xenoturbellida and Nemertodermatida 2500 m below the marine surface. We only have reliable data have cellular, epithelial guts (Fig. 1). However, where the on the digestive system for one species, Xenoturbella bocki,in plastic nature of the digestive system is most clear is within the work of Einar Westblad (Westblad 1949b). In the classical the Acoela. Here, one can distinguish at least four different description of this species, Westblad states that the mouth structural arrangements that could be defined as (see also orifice is small and only visible on sectioned specimens; a Fig. 2): (1) permanent central syncytium enclosed by wrap- statement corroborated by recent observations by Nakano ping cells—most acoels, especially Convolutidae but also (cited in Bourlat et al. 2008), which specifies the size of this Diopisthoporus sp. (Smith 1981); (2) lacking syncytial struc- opening as 1–2 mm. A true pharynx, containing