Abstract
Based on the number of tissues separating maternal from fetal blood, placentas are classified as epitheliochorial, endotheliochorial or hemochorial. We review the occurrence of these placental types in the various orders of eutherian mammals within the framework of the four superorders identified by the techniques of molecular phylogenetics. The superorder Afrotheria diversified in ancient Africa and its living representatives include elephants, sea cows, hyraxes, aardvark, elephant shrews and tenrecs. Xenarthra, comprising armadillos, anteaters and sloths, diversified in South America. All placentas examined from members of these two oldest superorders are either endotheliochorial or hemochorial. The superorder Euarchontoglires includes two sister groups, Glires and Euarchonta. The former comprises rodents and lagomorphs, which typically have hemochorial placentas. The most primitive members of Euarchonta, the tree shrews, have endotheliochorial placentation. Flying lemurs and all higher primates have hemochorial placentas. However, the lemurs and lorises are exceptional among primates in having epitheliochorial placentation. Laurasiatheria, the last superorder to arise, includes several orders with epitheliochorial placentation. These comprise whales, camels, pigs, ruminants, horses and pangolins. In contrast, nearly all carnivores have endotheliochorial placentation, whilst bats have endotheliochorial or hemochorial placentas. Also included in Laurasiatheria are a number of insectivores that have many conserved morphological characters; none of these has epitheliochorial placentation. Consideration of placental type in relation to the findings of molecular phylogenetics suggests that the likely path of evolution in Afrotheria was from endotheliochorial to hemochorial placentation. This is also a likely scenario for Xenarthra and the bats. We argue that a definitive epitheliochorial placenta is a secondary specialization and that it evolved twice, once in the Laurasiatheria and once in the lemurs and lorises.
Highlights
In mammalian development, the conceptus differentiates into an inner cell mass and an outer sphere of cells, the trophoblast
The tissues of the embryo are all derived from the inner cell mass as are the amnion and major components of the yolk sac and allantois
The yolk sac endoderm may soon become apposed to the trophoblast, but this two layered structure is not regarded as a true placenta
Summary
The conceptus differentiates into an inner cell mass and an outer sphere of cells, the trophoblast. Tree shrews have a quite distinctive form of endotheliochorial placentation (Figure 5B), involving twin discoid attachments to special pads developed on the lining of the uterus Conserved features of their fetal membranes include retention of a large allantoic vesicle and a large yolk sac [55]. In all of these animals the definitive placenta is discoidal with free and anchoring villi and an intervillous space perfused by maternal blood (Figure 5C) Based on their diffuse, non-deciduate and epitheliochorial placentation, Hill [50] argued that the lemurs and lorises were a more primitive form of primate than the tarsiers. Hemochorial placentas are found in insectivores, primates, tenrecs, rodents, bats, hyraxes, elephant shrews, anteaters, armadillos, flying lemurs and even hyenas. This hypothesis needs to be tested and refined in the light of current concepts of mammalian phylogenetics and kidney development [81]
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