Evolution and morphogenesis of the placenta in sharks

Placental sharks sequentially utilize three modes of embryonic/fetal nutrition to nourish their developing young—viz., vitellogenesis, histotroph secretion, and hematrophic placentation. These are the principal modes employed by vertebrates in general. The progressive shift from reliance on yolk, to histotroph, then to the placenta mirrors the probable stages in the evolution of placentation in sharks. Preimplantation shark embryos begin their ontogenetic development by reliance on yolk. In vitellogenesis, energy-rich precursors of hepatic origin are stored in oocytes prior to ovulation. Following fertilization, embryogenesis and fetal development proceed at the expense of the yolk stores sequestered in the yolk sac. Yolk is made available to the developing young by two means. Yolk is partially solubilized in the yolk syncytium of the yolk sac and subsequently modulated through the yolk sac endoderm. Yolk metabolites are then transported across the vitelline endothelium to reach the fetal circulation. Yolk granules are physically transported to the fetal gut by ciliated cells lining the ductus vitellointestinalis. The ductus is an endodermally lined conduit that extends from the yolk sac to connect to the fetal gut where digestion and absorption occur. Following depletion of the yolk stores and prior to development of the placenta, nutrient substances may be supplied to the fetus by secretory activity of the uterus in the form of histotroph. Histotroph may then be ingested and/or absorbed. In the transition from the yolk-reliant and histotrophic phases to a placental situation, there is a coincident shift in the function of the maternal uterus to one of a nutrient-producing or -transporting organ. Essential adaptations of the uterus include: enhanced secretory function, expansion to accommodate the embryos, respiration, osmoregulation, waste disposal, and protection of the young. As the yolk sac differentiates into a placenta, focal areas of the uterus become modified as uterine attachment sites. It is at the utero-placental complex that nutrient and metabolic exchange between mother and fetus will be effected. Paraplacental uterine sites may also continue to play a role in the elaboration of histotroph. The placenta is specialized into two segments: a proximal, smooth portion that has characteristics of a steroid-producing tissue and a more richly vascularized distal portion that is a nutrient-transporting tissue. Evolution of placentation involves modifications of existing maternal and fetal membranes. The ontogenetic transformation of the shark oviduct into a functional uterus for the retention and metabolic support of developing young certainly is modulated by endocrine regulation. In the developing fetus, the yolk sac and stalk display terminal differentiation into a regionally specialized placenta and an umbilical cord respectively. Accessory vascular structures of the umbilical cord, termed appendiculae, are present in some species.