The trophoblast sometimes but not always invades the uterine wall displacing and/or replacing one or more layers of tissue. Grosser's classification of placentas 6, based on the number of tissues separating maternal from fetal blood, has had an enormous influence 7. According to whether the trophoblast is apposed to uterine epithelium, the endothelium of maternal vessels, or directly to maternal blood, placentas are classified as, respectively, epitheliochorial, endotheliochorial or hemochorial. Nevertheless, once placentas could be studied at the ultrastructural level, it became apparent that this classification is of limited functional significance, since extensive thinning of the tissues reduces the diffusion distance between fetal and maternal blood even in epitheliochorial placentas 8. At the same time, studies of placental ultrastructural made it clear that there were many variations in the structure of the interhemal area (Table 1).

The list in Table 1 by no means exhausts the known number of placental types. Many placentas have specialized areas concerned with histiotrophic nutrition, that is, absorption of secretions from the uterine glands or phagocytosis of cellular debris. A large number have hemophagous regions in which maternal erythrocytes are taken up as a source of iron for the fetus. There are often large areas that seem to be concerned more with protein synthesis than materno-fetal exchange, as they are not penetrated by fetal blood vessels; examples are the spongy zones of rodent and hyrax placentas. Not surprisingly, there are many variations in placental shape, from the diffuse and cotyledonary forms in hoofed mammals through the circumferential ("zonary") placenta of carnivores to the familiar discoid form of the human or mouse placenta.

Clearly each placental type is able to support a successful pregnancy. Nevertheless, students of placental structure have continued to ask why there is so much variability and how the placenta evolved. The debate started with Huxley and Owen in the nineteenth century (reviewed by Pijnenborg and Vercruysse 9), continued with Wislocki 10 and Portmann 11, and culminated with the publications of Mossman 1213 and Luckett 14. The success of molecular phylogenetics in identifying the relations between the orders of mammals allows us to view placental structure from a new perspective 1516. It appears that all extant eutherian mammals can be classed in four superorders. These have been named Afrotheria, Xenarthra, Euarchontoglires and Laurasiatheria 1718. Accordingly, the approach taken here will be to review placentation in each superorder in turn.

The rodent order is so rich in species that only a small sample of placentas has been described 40. However, the placentas of rodents and lagomorphs tend to conform to a basic pattern. They are discoid to spherical in shape, the exchange area is labyrinthine and hemochorial, and there is a well developed spongy zone. An inverted or partially inverted yolk sac placenta supports the early development of the embryo and is retained until term.

There are three principal types of interhemal area in Glires 414243. Hystricomorph rodents, such as the guinea pig and capybara, have hemomonochorial placentas with a single layer of syncytial trophoblast in the interhemal barrier. So do the sciuromorph rodents or squirrels (Figure 4B). In lagomorphs the placenta is hemodichorial with an outer layer of syncytial and inner layer of cellular trophoblast. In most myomorph rodents the interhemal area is hemotrichorial (Figure 4A). Although the outer layer is cellular, it contains large pores and the inner layers of syncytial trophoblast are thought to constitute the placental barrier 44.

There are some notable exceptions. The kangaroo rats Dipodomys and Microdipodops are sciuromorph rodents, but in this family (Heteromyidae) the interhemal area is endotheliochorial and contains cellular trophoblast (Figure 4D) 45. In two families of myomorph rodents, jerboas (Dipodidae) and jumping mice (Zapodidae), there is a reduction in the trophoblast layers and the maternal blood channels are lined by trophoblastic giant cells (Figure 4C) 46.

In most rodent placentas the labyrinth and spongy zone form distinct layers. In hystricomorph rodents, however, folding gives rise to a lobed placenta. The lobes are the exchange areas and they are separated by interlobular trophoblast that is the equivalent of a spongy zone. In addition, hystricomorphs have a unique structure of unknown function, the subplacenta 47.

Rodents represent the only order of eutherian mammals for which placentation has been subjected to a strict cladistic analysis. Mess 43 concluded that the stem pattern was labyrinthine and hemochorial with a single layer of syncytial trophoblast in the exchange area. She did not extend this analysis to include the lagomorphs. It is pertinent to note that, on this analysis, the mouse placenta represents an elaboration of the stem pattern. This has potential implications for discussion of structural and functional homologies between mouse and human placentas 4849.

Ever since the seminal work of Hill 50, the evolution of placentation in primates has posed some interesting questions 51. Clearly there is a striking difference between the lemurs and lorises (Strepsirhini) and other primates (Haplorhini). The former have epitheliochorial and the latter hemochorial placentation. The recognition that tree shrews were closely related to primates, which receives further support from molecular studies, adds a further layer of complexity, since tree shrews (Scandentia) have endotheliochorial placentas 52. Finally Hill, who regarded hemochorial placentation as the derived state, opined that it had evolved separately in the tarsiers than in the monkeys and apes.

The colugos or flying lemurs (Dermoptera) have attracted less attention. Molecular phylogeneticists group them with primates and tree shrews, although the relations between the three orders are not well resolved 53. Their placenta has been little studied. It is discoid and appears to contain labyrinthine and villous areas. The interhemal area is hemodichorial 13.

In contrast, the fetal membranes of tree shrews have been well studied 5254 and were included in an early cladistic analysis by Luckett 55. 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.

Lemurs and lorises present a curious case in that they have diffuse, non-deciduate and epitheliochorial placentas (Figure 5A). The resemblance to placentation in pigs extends to the presence of thickened areas of trophoblast opposite the openings of the uterine glands 50, which parallel the areolae of the porcine placenta. There is a large allantoic vesicle, which is lobed as in the afrotherians. A temporary yolk sac placenta supports development of the early embryo.

Tarsiers have a discoid, hemochorial placenta. Except that it is labyrinthine rather than villous, the placenta is generally similar to that of monkeys and apes. The allantois is not vesicular, as in lemurs, but forms an almost solid connecting stalk of mesodermal tissue as in higher primates, a point to which Hill 50 attached particular importance.

There are strong resemblances in the early development of the platyrrhine or New World monkeys, the catarrhine monkeys of the Old World and the anthropoid apes. However, in platyrrhine monkeys, proliferation of the trophoblast continues until much later in gestation and connections persist between the villi, which form a trabecular network, not unlike that of the tarsier placenta. Only at a late stage of fetal development are branched villi found within a more or less continuous intervillous space. In catarrhine monkeys, on the other hand, arborescent chorionic villi are present from a very early stage, as they are in the human placenta. Although macaque and baboon implantation sites develop – sequentially – trophoblastic plate, lacunar and villous stages as do the anthropoid apes, in the former animals trophoblast taps maternal vessels early and the lacunae expand the placenta into the uterine lumen 56. Macaques also form a secondary placenta on the opposite side of the uterus from the original implantation. In man and anthropoid apes the trophoblast proceeds further into the uterus and the abembryonic as well as the polar trophoblast forms lacunae, resulting in an interstitial placenta. 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. This argument went to the very heart of the current debate about parallelism in the evolution of the placenta. Many found it difficult to accept that rodents, insectivores and primates arose from a common stem with a diffuse type of placentation. Among the doubters was Wislocki 10, who advanced the view that hemochorial placentation was the more primitive type of placentation and that the epitheliochorial placenta of the lemurs was the result of a secondary simplification.

A lucid discussion of the evolution of placentation in primates is given by Luckett 55. He noted that there is substantial homology in fetal membrane development between taxa with epitheliochorial placentation, but not between those with the endotheliochorial or hemochorial types. He argued that this was indicative of convergent evolution of hemochorial placentation, whereas the epitheliochorial type was part of the primitive eutherian condition.

On the grounds of parsimony, one might argue that the widespread occurrence of hemochorial placentation in Euarchonta reflects their common ancestry and follow Wislocki 10 in regarding the epitheliochorial placenta of strepsirhine primates as a derived state. Tree shrews have many conserved characters and it is possible that endotheliochorial placentation is one of these rather than being derived from a hemochorial type.

The order of insectivores has undergone steady attrition, the most recent exclusions being the tenrecs and golden moles. The relations between the core insectivores (shrews, moles, hedgehogs and Solenodon) continue to puzzle even the molecular phylogeneticists 5758. Most have discoid labyrinthine placentae. The interhemal area is hemochorial in hedgehogs and Solenodon 59. The American mole Scalopus has a circumferential placenta that is considered to be epitheliochorial 60, whereas the European mole Talpa is definitely endotheliochorial 61. However, Prasad et al. 60 had only a single midgestation specimen to examine by electron microscopy, and the looping arrangement of the maternal vessels is more similar to that seen in endotheliochorial placentas than that in typical epitheliochorial placentas. In the short-tailed shrew Blarina the interhemal area is endotheliochorial, but the trophoblast component is fenestrated 62. In the musk shrew Suncus the placenta is endotheliochorial, but there is progressive thinning and fenestration of the trophoblast layer 63. There are even areas where processes from the two endothelial layers contact one another through the pores in the trophoblast.

All insectivores have a partially or completely inverted yolk sac that is maintained to term. The allantoic sac is large in Talpa, medium sized in the hedgehog, small in Scalopus and small or rudimentary in shrews. This is a group of mammals that would repay close study using modern techniques.

As befits a widely diversified adaptive group of mammals 64, bats and especially microbats have evolved a multitude of endotheliochorial and hemochorial placental types (Table 1; reviewed by Badwaik and Rasweiler 65). The most common type of definitive placenta is the hemodichorial placenta, where syncytial trophoblast that has intrasyncytial bays fronts the maternal blood space and is underlain by cytotrophoblast (Figure 6A). Endotheliochorial placentas are found both as a diffuse placenta in midpregnancy and as a cellular endotheliomonochorial discoid placenta in late pregnancy (Figure 6B). In some mollosid bats the central area of the placenta near term is cellular hemomonochorial (Figure 6C). Megabats (fruit eating bats) have hemochorial placentas with Rousettus having a syncytial hemomonochorial type and Pteropus having a hemodichorial one, at least in midpregnancy. Although 13 of the 18 families of bats have been studied 65, there is still a great deal to be learned both about the fine structure and about other advanced features of membrane development 14.

The terrestrial carnivores and their aquatic relatives the pinnipeds (sea lions, walruses and seals) usually have circumferential, labyrinthine and endotheliochorial placentas, although the hyena develops hemochorial placentation late in pregnancy 6667. Carnivore placentas have hemophagous regions of variable size and location 68. Mossman 12 at one time considered the carnivore fetal membranes to be the most primitive type among extant eutherians, because both the yolk sac and allantoic sac are large and persist until term.

The remaining orders of Laurasiatheria are characterized by epitheliochorial placentation. The placenta may be diffuse with villi distributed over the surface of the chorioallantoc sac, as in whales 69, Suiformes (pigs, peccaries, and hippopotamus) 70, camels 71 and pangolins 13, or with microcotyledons as in the horse 1672. Most ruminants have cotyledonary placentas with the cotyledons varying in number from 5–8 in deer to 50–175 in bovids 8. Chevrotains are considered to be the most primitive ruminants and, interestingly, they have diffuse placentas 73.

The epitheliochorial type of arrangement has as its advantage the safety factor of the isolation of fetal and maternal components. The presence of two complete epithelia should diminish immunological problems as well as the deportation of fetal cells to the maternal organism. The disadvantage is the greater difficulty in passage of materials between organisms, but this is overcome by a variety of mechanisms. Most importantly, indenting of trophoblast and uterine epithelium by capillaries decreases the interhemal distance. There are often, but not always, small absorptive and phagocytic areas, for example the areolae of the pig placenta. In equids, girdle cells of fetal origin invade the uterine epithelium to form endometrial cup cells that secrete equine chorionic gonadotropin 747576. However, not all perissodactyls have endometrial cups 8. In ruminants such as sheep and cow, binucleate trophoblast cells fuse with maternal epithelial cells and this facilitates passage of prolactin to the maternal organism 77; this type of placenta is sometimes referred to as synepitheliochorial.

The diffuse type of epitheliochorial placenta usually is associated with an extensive allantoic sac. The cotyledonary type tends to be associated with a long, tubular allantoic cavity, although it is still large. There is a temporary yolk sac placenta early in development, where this has been examined, and a free yolk sac later in gestation. Mossman 13 noted the resemblance in definitive yolk sac placentation between whales, artiodactyls, perissodactyls and pangolins, but grouped them together with some non-laurasiatherians.