Spiral cleavage and early embryology of a loxosomatid entoproct and the usefulness of spiralian apical cross patterns for phylogenetic inferences

Abstract

BackgroundAmong the four major bilaterian clades, Deuterostomia, Acoelomorpha, Ecdysozoa, and Lophotrochozoa, the latter shows an astonishing diversity of bodyplans. While the largest lophotrochozoan assemblage, the Spiralia, which at least comprises Annelida, Mollusca, Entoprocta, Platyhelminthes, and Nemertea, show a spiral cleavage pattern, Ectoprocta, Brachiopoda and Phoronida (the Lophophorata) cleave radially. Despite a vast amount of recent molecular phylogenetic analyses, the interrelationships of lophotrochozoan phyla remain largely unresolved. Thereby, Entoprocta play a key role, because they have frequently been assigned to the Ectoprocta, despite their differently cleaving embryos. However, developmental data on entoprocts employing modern methods are virtually non-existent and the data available rely exclusively on sketch drawings, thus calling for thorough re-investigation.ResultsBy applying fluorescence staining in combination with confocal microscopy and 3D-imaging techniques, we analyzed early embryonic development of a basal loxosomatid entoproct. We found that cleavage is asynchronous, equal, and spiral. An apical rosette, typical for most spiralian embryos, is formed. We also identified two cross-like cellular arrangements that bear similarities to both, a "molluscan-like" as well as an "annelid-like" cross, respectively.ConclusionsA broad comparison of cleavage types and apical cross patterns across Lophotrochozoa shows high plasticity of these character sets and we therefore argue that these developmental traits should be treated and interpreted carefully when used for phylogenetic inferences.

Entoprocta

“…6.5 ;Merkel et al 2012 ). Gastrulation is preceded by fl attening of the embryo, occurs when the embryo has slightly more than 100 cells, and eventually results in a coeloblastula (Merkel et al 2012 ). This is in accordance with the data provided by Marcus ( 1939 ) on Pedicillina cernua , who found the embryos to gastrulate at around 120 cells.…”

“…Recently, new data have become available on a yet undescribed Loxosomella species employing fl uorescence staining of nuclei and 3D reconstruction of embryogenesis (Figs. 6.3 and 6.4 ;Merkel et al 2012 ). Most authors noted a holoblastic, more or less equal, spiral cleavage pattern, comparable to that of other Spiralia.…”

“…An apical rosette was found in Pedicillina and Loxosomella , together with two spiralian cross-like patterns resembling those of annelids and mollusks at around 43 cells in Loxosomella (Fig. 6.5 ;Merkel et al 2012 ). Gastrulation is preceded by fl attening of the embryo, occurs when the embryo has slightly more than 100 cells, and eventually results in a coeloblastula (Merkel et al 2012 ).…”

A set of simple cell processes are sufficient to model spiral cleavage

“…When cell fates are compared between spiralians, it is often found that the same adult or larval organs in different species arise from the same blastomeres [defined by lineage and relative position in the blastula (Nielsen, 1994;Lyons et al, 2012)]. The first four cell division rounds are synchronous but this synchrony is gradually lost over developmental time and the similarity between groups becomes less obvious (Freeman and Lundelius, 1982;Merkel et al, 2012). In some species with a very derived spiralian cleavage, this synchrony can be lost much earlier (Nielsen, 1994).…”

“…Such gradients promote asymmetric cell division by a differential binding of the spindle microtubules to the cortex that results in asymmetric pulling forces and a displacement of the contractile ring during cytokinesis (Gilbert and Raunio, 1997;Ren and Weisblat, 2006;Lu and Johnston, 2013). Asymmetric cell division may play a role in generating morphological variation among the spiral cleavage patterns because blastomeres of different relative sizes are placed and compacted in different manners due to cell-cell adhesion (Merkel et al, 2012).…”