Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan

Abstract

Sponges usually produce, release, and capture gametes via the aquiferous system, and so the absence of both choanocytes and an aquiferous system in the carnivorous sponge Asbestopluma occidentalis has led to unusual characteristics of development for this Phylum. Sperm are highly specialized elongate cells tightly packed into spermatic cysts in the peripheral tissue of the sponge. Mature spermatozoa have proacrosomal vesicles at the anterior end and a ciliary pit surrounding the flagellum. Clusters of four to five oocytes are in synchronous stages of cleavage, suggesting that fertilization is synchronous. All stages of embryos occur in the same individual. Early cleavage was holoblastic and equal; blastomeres in two-, four- and eight-cell embryos were compact and 16-cell stage embryos were bi-layered. Late-stage embryos show three cellular regions along the anterior-posterior axis: the anterior hemisphere with heterogeneous cells, a mid-region with cells lying perpendicular to the A-P axis in a collagenous matrix, and small cells at the posterior pole. Unusually for Porifera, multiciliated cells cover all but the posterior pole. It is inferred that fertilization occurs by capture of intact spermatic cysts whose surrounding forceps spicules become trapped in the anisochelae of neighboring sponges. The elongate shape of sperm may be designed to penetrate the loose collagenous mesohyl, such that the arrival of a packet of sperm would lead to simultaneous fertilization of oocytes in a cluster. Loss of the water canal system in carnivorous sponges has allowed the evolution of features that are highly specialized for the habitat of this animal, but such modifications were not necessarily a prerequisite for the subsequent evolution of metazoans. Given the extremely versatile mechanisms of gametogenesis, embryogenesis, and tissue/body structure in sponges, generalizations regarding basal metazoan reproduction, development, and structure must be approached with caution.