The evolution of the placenta

Abstract

The very apt definition of a placenta is coined by Mossman, namely apposition or fusion of the fetal membranes to the uterine mucosa for physiological exchange. As such, it is a specialized organ whose purpose is to provide continuing support to the developing young. By this definition, placentas have evolved within every vertebrate class other than birds. They have evolved on multiple occasions, often within quite narrow taxonomic groups. As the placenta and the maternal system associate more intimately, such that the conceptus relies extensively on maternal support, the relationship leads to increased conflict that drives adaptive changes on both sides. The story of vertebrate placentation, therefore, is one of convergent evolution at both the macromolecular and molecular levels. In this short review, we first describe the emergence of placental-like structures in nonmammalian vertebrates and then transition to mammals themselves. We close the review by discussing the mechanisms that might have favored diversity and hence evolution of the morphology and physiology of the placentas of eutherian mammals.

Figure 1

Viviparity in reptiles: A, Drawing from a section of the mature chorio-allantoic placenta of the Australian skink Egernia cunninghami carrying developing young, showing the maternal capillaries closely adjoining the allantoic capillaries on the fetal side. B, Drawing from a section of the immature chorio-allantoic placenta of the Australian skink Egernia entrecasteaux. The section illustrates the folded placental face likely involved in releasing histotrophic material that can be taken up by the chorionic ectoderm. Note also the close apposition of maternal blood capillaries with the epithelium of the reproductive tract. The diagrams are based on Fig. 15.5 and 15.7 from E.C. Amoroso’s review on placentation (Amoroso 1952), which were redrawn from Weekes (Weekes 1935).

Figure 2

Cartoon illustrating the diversity of placental morphologies encountered in placental mammals

Figure 3

Cartoon indicating how placentas can be classified according to the numbers and kinds of cell layers that separate the bloodstreams of the mother and conceptus

Figure 4

The evolution of the placental interface in terms of degree of invasiveness of the placental tissue into maternal tissue, with epitheliochorial being the least invasive and hemochorial being most invasive. From Fig. 2 of Wildman et al. (Wildman, et al. 2006), with permission; Copyright (2006) National Academy of Sciences, U.S.A.

Figure 5

The porcine placenta: A, Fetal capillaries (FC) at d 58 of pregnancy protrude deeply into the trophoblast, with the diffusion distance between fetal bloodstream and maternal uterine epithelium (UE) reduced to a few μm; B, At d 110 of pregnancy maternal capillaries (MC) project between uterine epithelial cells bringing the maternal and fetal capillaries within 3–5 μm; C, At d 30 of pregnancy, the microvilli on the trophoblast surface (TR) interdigitate with ones on the uterine epithelium (UE) to provide an intimate contact layer. Maternal capillaries (MC) are placed just below the basal lamina of the UE; D, A general view of a dome-shaped areola (AE) situated above the mouth of a uterine gland (UG) at d 30 of pregnancy. Figures 5A-C are from Friess et al. (1980) (Friess, et al. 1980); Figure 5D is from Friess et al. (1981)(Friess, et al. 1981) with permission.