Evolution of the mammalian placenta revealed by phylogenetic analysis

Abstract

The placenta is essential for the success of therian mammalian reproduction. Intense selective pressure has shaped changes in placental anatomy and function during mammalian cladogenesis. Here we challenge the view that the hemochorial placenta is a derived feature in haplorhine primates. Using phylogenetic and statistical analyses of molecular and morphological data, we demonstrate that the ancestral eutherian mammalian placenta had the distinctive features of (i) hemochorial placental interface, (ii) a discoid shape, and (iii) a labyrinthine maternofetal interdigitation. These results reveal that the first eutherians had a deeply invasive placenta and imply that the major role of the placenta in sustaining pregnancy and promoting gestational development existed throughout the eutherian lineage that descended to humans from the last common ancestor of placental mammals. The ancestral state reconstructions demonstrate both clade-specific patterns of placentation and specific cases of convergent evolution within individual eutherian clades. Determining the mammalian pattern of change in placental morphology is important for understanding the evolutionary pressures faced by these lineages. The effects of selection pressures on the efficiency of placentation may stem from changes in nutritional demand, gestational length, number of embryos per pregnancy, uterine shape, and maternal body constitution. The influence of these factors on placental development needs further investigation.

Fig. 1.

Phylogenetic relationships among major placental mammalian groups. Four major superordinal placental (i.e., eutherian) mammalian clades are supported by molecular data (9, 13). These clades are the Afrotheria, Xenartha, Euarchontaglires, and Laurasiatheria. All studies also support the grouping of Euarchontaglires and Laurasiatheria as sister taxa in a larger clade (Boreoeutheria). The phylogenetic branching order at the root of the tree is controversial (–13). (A) Depiction of the Afrotheria as sister to the remaining three clades (i.e., Notolegia). (B) Depiction of the Xenartha as sister to the remaining three clades. A third choice in which Boreoeutheria is sister to a clade that consists of Xenartha and Afrotheria is not supported by parsimony analysis (Table 1).

Fig. 2.

The evolution of morphological placental features in mammals. Parsimony reconstructions of internal nodes are shown for three morphological features (see Materials and Methods for details of reconstruction methodology). Taxon names and branching order are identical in all panels of the figure. Only the Afrotheria + Notolegia tree (i.e., 9) is shown. The data for all tree topologies examined is available as supporting information. (A) The placental interface describes the degree of invasiveness of fetal (i.e., placental) tissue into maternal tissue, with epitheliochorial being least invasive and hemochorial being most invasive. (B) The shape of the contact zone between fetal and uterine tissues. (C) The form of interdigitation between fetal and maternal tissues. Parsimony and Markov model likelihood reconstructions were constructed by using the data file available as supporting information.

Fig. 3.

The evolution of the placental interface in primates. Parsimony reconstructions of internal nodes are shown for the placental interface character (see Materials and Methods for details of reconstruction methodology). Parsimony and Markov model likelihood reconstructions were constructed by using the data file available as supporting information. Strep., Strepsirrhine; NWM, New World monkeys; OWM, Old World monkeys.