Temereva E.N., Malakhov V.V. 2012. Embryogenesis in phoronids // Invertebrate Zoology. Vol.9. No.1: 1–39 [in English].
Department of Invertebrate Zoology, Biological Faculty, Moscow State University, Moscow 119992, Russia. E-mail: temereva@mail.ru
doi: 10.15298/invertzool.09.1.01
KEY WORDS: Phoronida, Lophotrochozoa, embryogenesis, development, phylogeny.
ABSTRACT: The Phoronida is a phylum of marine animals whose position in the Bilateria has radically changed as a result of recent molecular phylogenetic analysis. Although molecular data have confirmed the position of phoronids among typical Trochozoa, supporting data from comparative embryology and morphology are lacking. This paper reviews the available literature and also provides original results concerning the early embryonic and larval development of phoronids. Phoronid egg cleavage can be regarded as transitory between a typical radial and typical spiral pattern. The presence of oblique furrows in early phoronid development should not be interpreted to mean that phoronid cleavage is typically radial. At the same time, phoronids lack a specific mosaic of blastomeres, whose presence is characteristic of true spiral development. Phoronids also lack trochoblasts, rosettes, and cross cells. Nondeterministic cleavage with an oblique position of furrows allows the blastula to form at the 16-cell stage, which is very important for species with holopelagic development. In phoronid species that brood, a brick-like embryo appears as a result of early egg development. In phoronids, there are two distinctive sources of coelomic mesoderm: anterior and posterior. Both sources are multicellular and originate from the anterior wall of the archenteron (the anterior mesoderm) or by entherocoely (the posterior mesoderm). Organogenesis starts in the later gastrula. The ectoblast gives rise to the epidermis, ciliated bands, nervous system, excretory system, and some parts of digestive tract (esophagus and proctodaeum). The ultrastructure of the epidermis differs depending on body part. The activity of ciliated bands in phoronid larvae combines features of the Protostomia and Deuterostomia. In actinotrocha, the preoral ciliated band functions as it does in protostomian larvae (the preoral ciliated band beats from anterior to posterior), whereas the postoral ciliated band functions as it does in deuterostomian larvae (the postoral ciliated band beats from anterior to posterior). The first neurons are serotonergic; they appear in the epidermis of the apical plate. In the young larva of Phoronopsis harmeri, the serotonergic nervous system consists of apical ganglion, which contains a U-shaped field of monopolar perikarya, and two groups of bipolar (or multipolar) perikarya; the tentacular neurite bundle, which runs dorsally from the left and right groups of bipolar (or multipolar) perikarya; two nerve rings of the telotroch; the oral nerve ring; and the nervous net around the proctodaeum and pyloric sphincter. In the early larva, serotonergic perikarya originate along the edge of the preoral lobe and then disappear. At this stage, the perikarya on the ventral body side form the ventral nerve cord and then also disappear. The FMRFamidergic nervous system is very complex; the main nervous tracts underline the main muscles. The FMRFamidergic ventral nerve cord appears in the 6-day-old larva and remains in older stages. The excretory system forms as an unpaired ectodermal protrusion under the postoral ciliated band in front of the anus. The protrusion develops two branches (left and right), which then separate and form two protonephridia. The entoblast gives rise to other parts of digestive tract (cardiac sphincter, stomach, midgut). The posterior part arises from ectoderm. Mesoblast is the source of the coelomic lining of the preoral and (in future) tentacular coeloms, muscles, and blood corpuscles. In the early embryo, muscle cells and coelothelial cells have similar ultrastructures and form a continuous layer; all cells bear desmosomes. Then the myofilaments appear in the muscle cells, which lose desmosomes and become cross-striated. In summary, phoronids combine features of Protostomia and Deuteroatomia. Apparently, these features (nondeterministic cleavage of the egg; formation of blastule early in development; two sources of mesoderm; simultaneous occurrence of the mouth, nervous system, and muscles; etc.) are plesiomorphic and inherited from the common Bilateria ancestor. On the phylogenetic tree, phoronids should therefore be regarded as one of the basal groups of the Lophortochozoa.