Polyaxial cleavage in sponges (Porifera): a new pattern of metazoan cleavage.

Abstract

Cleavage is an important stage of animal embryo-genesis marked by the emergence of multicellularity ofan organism and by ooplasmic segregation of morpho-genetic determinants. In addition, cleavage is a highlycoordinated process of diagnostic significance. Cleav-age patterns are often used to investigate the phyloge-netic relationships in various animal groups [1].Analysis of early development of sponges( Porifera ), including cleavage, is of particular interestbecause of their key position at the base of the phyloge-netic tree for Metazoa. However, studies speciallyaddressing the stage of egg cleavage in sponges werevery few until the past two decades [2–5]. It is now wellknown that, in all sponge species, the whole egg dividescompletely (holoblastic cleavage). The process is usu-ally uniform, but the cleavage patterns may signifi-cantly vary from species to species. In most species,cleavage division planes are randomly oriented (chaoticcleav age). A unique type of cleavage called tablepalyntomy occurs in some species of the subclassCalcaronea [4]. In the glass sponge Oopsacas minuta (Hexactinellida), cleavage is pseudospiral [5]. In manyoviparous species of the class Demospongiae, cleavagefollows a nearly radial pattern [6].Of particular interest is analysis of cleavage insponges of the order Halisarcida, which are the mostprimitive of Demospongiae [7, 8]. The goal of thisstudy was to reexamine the cleavage period of Hal-isarca dujardini development using light and electron(scanning and transmission) microscopy. Sponges ofthis species are dioecious and viviparous. Theirembryos develop within temporary follicles. Each fol-licle consists of pinacocyte-like follicular cells and anouter collagen layer. Before maturation division, theoocyte is oval, with a round nucleus at the center. Yolkgranules are uniformly distributed throughout theoocyte.The first cleavage division in H. dujardini is uniformand proceeds in the meridional plane. The cleavage fur-rows are of the bipolar type. The subsequent cleavageproceeds asynchronously. During the second cleavagedivision, the orientation of mitotic spindles relative toeach other varies from parallel to perpendicular(Fig. 1a). Thereafter, cleavage goes on asynchronously.From the third cleavage division onward, mitotic spin-dles are always formed parallel to the surface; there-fore, the cleavage furrows run perpendicular to the sur-face (Fig. 1b). The eight-cell embryo is round orslightly oval in the cross-section and never appears as alamina-like structure described earlier [7].Cleavage leads to the formation of an apolar coelo-blastula with a small cavity inside. The cavity isbounded with long wedge-shaped cells (Fig. 1c). At thestage of approximately 100 cells, blastomeres exhibit adistinct apicobasal polarity.In our previous studies [2, 8], some primitive traitswere described in H. dujardini cleavage. These were,first of all, the absence of any determinate spatial rela-tionships among blastomeres within the embryo. Con-ceivably, the origin of these primitive traits should besought in the absence of mature egg patterning (prepat-terning) [9], which is usually regarded to be a commonprimitive trait of egg organization in sponges [10].Throughout the H. dujardini egg, its structure remainsuniform. Holoblastic uniform asynchronous cleavage istypical of all the Halisarcida species studied, such as H. dujardini, H. metschnicovi , and H. nahantensis [2, 7, 8, 11]. A distinctive feature of the cleavage stageof H. dujardini development is the long retention of theblastula-like appearance by the embryo (from the eight-cell to the prelarval stage), which is due to the early for-mation of cleavage division planes of similar type run-ning parallel to the embryo surface [2, 8]. The samecleavage pattern was described for H. nahantensis [11].This cleavage pattern is unique among the viviparousDemospongiae but quite usual in Calcinea (class Cal-carea), which form a monolayer flagellated blastula [12].At present, eight major patterns of holoblastic cleav-age are distinguished in animals [1]. Chaotic cleavageproduces no patterning in blastomere distribution. Pas-sage of all cleavage furrows along the animal–vegetal