Early development and embryology of the platypus.

Information on the pre-hatching development of the platypus, Ornithorhynchus anatinus, is reliant on a small number of specimens, whose precise age is unknown. Material collected for J. P. Hill and now housed in the Hubrecht International Embryological Laboratory, Utrecht, contributes a major source of specimens. This paper presents new observations on developmental stages from the Hill collection, which allow for a more complete description of pre-hatching development. A feature of the pre-embryonic development of the platypus is the incomplete meroblastic cleavage. A column of fine yolk spheres extends from beneath the embryonic blastodisc towards the centre of a yolky vitellus, as seen in birds. The major expansion of extra-embryonic membranes occurs after the formation of the primitive streak. The primitive streak develops within an embryonal area as part of the superficial wall of the yolk-sac, a feature also shared with marsupials, birds and reptiles. The full-term, subspheroidal, intrauterine egg of the platypus has a major axis of about 17 mm and contains a flat, 19-20 somite, neurula-stage embryo which has prominent trigeminal ganglion primordia. The embryo at this stage is in a period of rapid modelling of the major early organ primordia of the nervous system, cardiovascular system, excretory system, and somite-derived components of the body wall. Soon after laying, five primary brain vesicles are present, the trigeminal ganglia CN5 as well as CN7, CN8, CN9, CN10, CN11 and CN12 are well developed. The alimentary system has an expanded stomach, pancreatic primordia and a gall bladder. Mesonephric tubules are associated with patent mesonephric ducts, which empty laterally into the cloaca. Extra-embryonic membranes at this stage show an extensive chorioamniotic connection that extends through the greater part of the caudal half of fused amniotic folds. The vascularized yolk-sac consists of a superficial yolk-sac omphalopleura and a deep yolk-sac splanchnopleure. The non-vascularized yolk-sac comprises one-quarter of the ahembryonal pole. Some distinctive monotreme features have developed by the mid-incubation period. The head is bent at an acute angle to the main body axis. The blunt upturned snout marks the site of the future oscaruncle and on the maxilla there is a median primordial papilla representing the egg tooth. The eye is open with a partly pigmented retinal ring. The forelimbs have partly separated digits, and the hindfeet are paddles. Just before hatching the upturned snout contains an oscaruncle and a sharp recurved median egg tooth. Forelimbs are pronated with separate digits possessing claw primordia. Portions of the highly vascularized extra-embryonic membranes are attached to the umbilical region and the flattened vesicular allantois has a distal region fused with the chorion. Prominent features of the hatchling are the presence of a bluntly conical oscaruncle and a translucent, horn-like egg tooth. These structures are though to enable the hatchling to extricate itself from the egg shell. At hatching, the forelimbs exhibit clawed digits and are capable of digitopalmar prehension. Hindlimbs are still paddles with digital rays. A prominent yolk-sac navel is present. The newly hatched platypus has an external form similar to that of a new-born marsupial. The early development of the platypus has many major differences to the developmental sequence for humans, which has been categorized by the use of Carnegie Stages. The rate of somitogenesis of the platypus is faster in relation to the central nervous system morphogenesis than seen in humans, and the size of the early platypus embryonal area is massive in relation to that of humans. The unique morphology and function of extra-embryonic membranes in the platypus defies comparative staging with human development. Structures adapted for altricial survival of the platypus hatchling require the acquisition of functional competence at an earlier stage of organogenesis than seen in eutherians, although they are reminiscent of those found in new-born marsupials.