Studies on the Onychophora VIII. The relationship between the embryos and the oviduct in the viviparous placental onychophorans Epiperipatus trinidadensis Bouvier and Macroperipatus torquatus (Kennel) from Trinidad

Abstract

Viviparity in the neotropical Onychophora is based on a placental relationship between the embryo and the maternal oviduct, analogous in certain ways to that of mammals. The embryo develops a stalked placenta which becomes intimately associated with the oviduct wall. The tissues of the oviduct wall become highly modified in the placentation zone. The present study provides the first detailed account of the formation and structure of the placentation zone in the neotropical Onychophora and of the events involved in the movement of the embryos along the oviduct. Macroperipatus torquatus is more specialized in certain ways than Epiperipatus trinidadensis , but the general course of gestation is similar in both. The oviduct has a proximal growing region. Each fertilized egg released from the ovary becomes implanted at the midpoint of a newly formed length of proximal oviduct. As the embryo develops, it remains within its associated length of oviduct, while additional lengths containing younger embryos are added more proximally. The embryo is enclosed in an epithelial sac, formed by cells of the lining epithelium of the oviduct. A placental stalk attaches the embryo to the equatorial inner surface of the sac. As the embryo grows, the epithelial sac extends in both directions along the associated oviducal part. The wall of the sac becomes specialized equatorially as an inner placental ring. The wall of the oviducal part develops an outer placental ring external to the inner placental ring, but is partially resorbed and simplified elsewhere along its length. Segment formation and the preliminary differentiation of organ systems are completed while the embryo is enclosed in the epithelial sac. The embryo eventually fills the sac, which then occupies the full length of the associated oviducal part. The embryo now escapes from the epithelial sac and moves into the lower region of the oviduct, where embryonic growth continues. Each escape of an embryo in this way follows the birth of the largest embryo previously contained in the lower region of the oviduct. The placentation zone and associated oviducal part vacated by the escaping embryo are added to the proximal end of the lower region of the oviduct, where resorption of both the placentation zone and the general oviduct wall continue. The lower region of the oviduct is encircled by a sequence of vestigial placentation zones, each indicative of a prior birth. Thus, the neotropical Onychophora combine placentation with the progression of a sequence of embryos towards the genital opening by a simple device. Each embryo occupies a fixed position in the oviduct until its organ systems are fully formed, but the oviduct grows at the proximal end and is resorbed towards the distal end. This procedure is unique among the Onychophora. The embryos of non-placental species are moved along the lumen of the oviduct by muscular action in the normal way. The onychophoran placenta is functionally analogous to the mammalian yolk-sac placenta, but no functional equivalent of a chorio-allantoic placenta is developed in the Onychophora. Most of the growth of the onychophoran embryo takes place after the placenta has been resorbed.