Placenta has a wide range of functions. Some are supported by novel genes that have evolved following gene duplication events while others require acquisition of gene expression by the trophoblast. Although not expressed in the placenta, high-affinity fetal hemoglobins play a key role in placental gas exchange. They evolved following duplications within the beta-globin gene family with convergent evolution occurring in ruminants and primates. In primates there was also an interesting rearrangement of a cassette of genes in relation to an upstream locus control region. Substrate transfer from mother to fetus is maintained by expression of classic sugar and amino acid transporters at the trophoblast microvillous and basal membranes. In contrast, placental peptide hormones have arisen largely by gene duplication, yielding for example chorionic gonadotropins from the luteinizing hormone gene and placental lactogens from the growth hormone and prolactin genes. There has been a remarkable degree of convergent evolution with placental lactogens emerging separately in the ruminant, rodent, and primate lineages and chorionic gonadotropins evolving separately in equids and higher primates. Finally, coevolution in the primate lineage of killer immunoglobulin-like receptors and human leukocyte antigens can be linked to the deep invasion of the uterus by trophoblast that is a characteristic feature of human placentation.

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.

Analysis of molecular data sets has provided new insights into higher‐level relationships of living Eutheria, including the recognition of Afrotheria as a novel taxon. This offers an opportunity to take a fresh look at the evolution of organ systems, including some that are little used in traditional systematics. In the present study, we attempted a reconstruction of the evolution of characters associated with placentation, the fetal membranes and the female reproductive tract. The evolutionary history of 21 characters has been traced, based on a current hypothesis of eutherian relationships, by applying the computer program MacClade. Accordingly, the analysis provides a first comprehensive interpretation of the stem species pattern of Eutheria. Of particular note, this pattern includes an endotheliochorial chorioallantoic placenta. The reconstructed pattern of Eutheria does not change in the basal nodes of the group. Thus, no character transformations occur on the stem lineages of Laurasiatheria or Euarchontoglires, and even Afrotheria has mostly plesiomorphic character conditions. However, two character transformations occur on the common stem lineage of Afrotheria and its sister taxon Xenarthra, i.e., amniogenesis by cavitation instead of folding and the precocial state of the newborn. In addition, we recognized one character transformation on the stem lineage of Afrotheria, i.e., the occurrence of a four‐lobed allantoic sac. Thus, contrary to previous assertions, it is possible to identify morphological characters that could be synapomorphic for this novel taxon. J. Exp. Zool. (Mol. Dev. Evol.) 306B, 2006.