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. discoid shape ͉ Eutheria ͉ hemochorial ͉ maternofetal interdigitation ͉ villous type

Evolution of the placenta and associated reproductive characters in bats

“…Not unexpectedly, the discoid placenta is part of the stem species pattern of all major lineages of bats, and represents an ancient condition within placental mammals, which is in accordance with the reconstruction of their stem species pattern (Mess and Carter, 2006;Wildman et al, 2006). The minimum/maximum numbers of character state transformations are 1 and 5.…”

“…Recent authors agree that the epitheliochorial type is a derived state (Martin, 2003;Vogel, 2005;Mess andCarter, 2006, 2007;Wildman et al, 2006;Carter and Mess, 2007). However, attempts at character mapping have given contradictory results with either endotheliochorial (Martin, 2003;Wildman et al, 2006) or hemochorial (Mess and Carter, 2006) emerging as the derived state. Continued ambiguity about how to root the placental tree and the branch order in critical groups such as Afrotheria, as well as the taxon sampling in the individual trees, contributes to this uncertainty .…”

“…This approach was chosen because of the basal position of Chiroptera within Laurasiatheria (Murphy et al, 2001) and the derived form of placentation in other orders (Vogel, 2005;Mess and Carter, 2006;Wildman et al, 2006), which makes most members of Laurasiatheria of limited value for analyzing the course of placental evolution in bats. Finally, we compared the results of the current analysis with reconstructions on placental and fetal membrane characters in the stem species pattern of Placentalia (Vogel, 2005;Mess and Carter, 2006;Wildman et al, 2006) and Chiroptera (Simmons and Geisler, '98;Gunnell and Simmons, 2005).…”

A review of inter- and intraspecific variation in the eutherian placenta

“…This shape was present in the most recent common ancestor of placental mammals [3,8,9]. The zonary placenta was the first shape to diverge from the ancestral discoid placenta and is present in some afrotherians such as the members of Sirenia and the African elephants as well as the carnivores of the laurasiatherian clade [3,[9][10][11][12]. Another evolutionarily derived placental shape is the diffuse placenta present in some primates and most of the cetartiodactyls (i.e.…”

“…Another evolutionarily derived placental shape is the diffuse placenta present in some primates and most of the cetartiodactyls (i.e. cetaceans and artiodactyls) except bovines [3,4]. The diffuse placenta has a large surface area for contact with the uterine wall, allowing a high surface area for maternal-fetal nutrient exchange.…”