Unusual development of the mitraria larva in the polychaete Owenia collaris

Abstract

Despite the wide variety of larval forms among polychaetes, most are clearly derived from the canonical spiralian trochophore. Within the genus Owenia (family Oweniidae), however, the mitraria larva lacks the characteristic ciliary bands of the trochophore, and those it has are monociliated, typically a deuterostome characteristic. Adult Owenia spp. also possess a monociliated epidermis and deuterostome-like nephridia. This study is the first detailed account of early embryology for any member of the Oweniidae. Light, confocal, and scanning electron microscopy were used to investigate organogenesis from fertilization through metamorphosis in Owenia collaris. Equal spiral cleavage yields an embryo with an unusually large blastocoel for a spiralian. The embryo undergoes gastrulation by invagination, and begins swimming 24 h after fertilization. Three important events deviate markedly from stereotypical polychaete embryogenesis. First, at the 8-cell stage the micromeres are larger than the macromeres, as in nemerteans. Second, the blastopore becomes the anus, as in some deuterostomes, while the stomodeum may form secondarily. Third, the cells that would form the prototroch in a canonical spiralian trochophore (1q(2) descendants) never undergo cleavage arrest, and the primary ciliated band of the mitraria never contains large, multiciliated cells. The mitraria larva thus represents a mixture of protostome and deuterostome developmental traits, suggesting that spiralian development is not so rigidly constrained as it might appear.