Early cleavage in Phoronis muelleri (Phoronida) displays spiral features

Abstract

The view that early cleavage in Phoronida follows a radial pattern is widely accepted. However, data supporting this characterization are ambiguous. Studies have been repeatedly reporting variation between individual embryos, and the occurrence of embryos exhibiting oblique divisions or nonradial cell arrangements. Such embryos were often considered to represent variation within radial cleavage, or artificial appearances. Cleavage in Phoronis muelleri was previously characterized as "derived radial," but also oblique spindles and cell elongations, and shifted cell arrangements were observed. We studied the early cleavage in P. muelleri applying 4D microscopy, fluorescent staining, and confocal laser scanning microscopy. To deal with the problem of variation we provide statistical evaluations of our data. These show that oblique divisions do not represent variational abnormalities. In fact, they reveal that most cells divide obliquely from the third cleavage onwards. What is more, in almost all cells the axis of the third cleavage is inclined dextrally. The fourth cleavage is even stronger sinistrally pronounced. Subsequently, the pattern of alternating cleavage orientation is largely restricted to animal and vegetal blastomeres. As a result of the obliqueness of divisions, four cells encircle the poles in most embryos. Cross furrows are occasionally present. We found no indications for radial cleavage in P. muelleri. In contrast, the observed cleavage displays several characters consistent with the pattern of spiral cleavage. A close relation of phoronid and spiralian cleavage is also suggested by molecular phylogenies, allying both groups in the Lophotrochozoa. We suggest our findings to represent morphological support for this lophotrochozoan/spiralian affinity of Phoronida.

New phylogenomic data support the monophyly of Lophophorata and an Ectoproct-Phoronid clade and indicate that Polyzoa and Kryptrochozoa are caused by systematic bias

“…Alternatively one might assume that Lophophorata is the sister group of the lophotrochozoan phyla that share spiral cleavage. However, the finding that cleavage is spiral in at least some phoronids [59,60] shows how variable cleavage patterns are and that the radial cleavage of lophophorates is probably secondarily derived from spiral cleavage.…”

Phylogenomic Insights into Animal Evolution

“…However, there is no obvious consensus for the relationships between them. Brachiopods and phoronids are very likely linked -phoronids may even be shell-less brachiopods -and molecular phylogenies and recent reports of spiral cleavage link these two phyla to the spirally cleaving annelids, molluscs and nemerteans [42]. The spiral cleavage and trochophora-like Mü ller's larva of some platyhelminths also suggests a link to these phyla.…”

“…The recognition that the Lophotrochozoa are monophyletic -a clade that includes all the phyla with classic spiral cleavage -strongly supports the homology of this mode of early development. Recent reports of spiral cleavage in the lophophorate phoronids [42] and in entoprocts [43] make sense in the light of their inclusion in the Lophotrochozoa alongside the canonical spiral cleavers.…”

Phoronida

“…Although irregular early cleavage stages have been observed (Zimmer 1964 ;Malakhov and Temereva 2000 ), none of these patterns exhibit spiral-like divisions. At the four-cell stage, transient cell contacts between non-sister blastomeres do occur, creating a crossfurrow similar to what is described for Phoronis muelleri (Pennerstorfer and Scholtz 2012 ).…”

“…Cleavage variation also begins at different early cleavage stages among species; some cleave variably at the eight-cell stage (Brooks and Cowles 1905 ;Herrmann 1986 ) and others (more commonly) at the 16-cell stage (Temereva and Malakhov 2007 ). More recently, early cleavage was investigated in Phoronis muelleri using 4D microscopy techniques (Pennerstorfer and Scholtz 2012 ), which showed that oblique rather than perpendicular cell divisions occurred at third and subsequent cleavages of most of the embryos in the study. Interestingly, cell divisions at third cleavage and beyond also exhibited alternating dextral-sinistral twists, a feature typical of spiralian embryos (Hejnol 2010 ).…”