Morphology of the ovotestis of Synaptula hydriformis (Holothuroidea, Apoda): An evolutionary model of oogenesis and the origin of egg polarity in echinoderms

The viviparous holothuroid Synaptula hydriformis, a simultaneous hermaphrodite, broods its young in the coelom and releases young year round. Both eggs and sperms develop asynchronously in the two short gonadal tubules that are suspended in the coelomic cavity. Sperms are released into the tubule, but eggs are not. Each gonadal tubule consists of pin outer peritoneum composed of flagellated epithelial cells, muscles, and nerves; an inner germinal epithelium of germinal and somatic cells; and a middle connective-tissue (hemal) compartment bounded by the basal laminas of the peritoneum and germinal epithelium. Spermatogonia and oogonia are flagellated epithelial cells that retain epithelial polarity throughout gametogenesis. During spermatogenesis, spermatocytes emerge towards the lumen from the germinal epithelium and sperms enter the lumen apex (tail) first. Supportive and phagocytic interstitial cells are associated with spermatocytes. During oogenesis, oocytes submerge basally into the hemal sinus and carry the epithelial basal lamina ahead of them. The oocyte apex, however, maintains adhering junctions with somatic (follicle) cells and bears a flagellum, at least into the vitellogenic phase. Full-grown oocytes are enclosed in basal lamina, except apically, where an apical protuberance forms. The apical protuberance is a region of ooplasm, devoid of yolk and rich in microtubules, that terminates apically in an extensive junction between the oolemma and follicle cells of the germinal epithelium. The oogenic pattern of S. hydriformis indicates that the apical-basal polarity of the oocyte becomes the animal-vegetal polarity of the egg, which in turn, becomes the anterior-posterior axis of the larva. Homologous oogenic patterns occur in crinoids and ophiuroids, but not asteroids and echinoids. An outgroup analysis of echinoderm oogenic patterns with those of Cephalochordata and Cnidaria suggests that the pattern common to holothuroids, crinoids, and ophiuroids is plesiomorphic to echinoderms and, in general form, to deuterostome metazoans.