Evolution of the mammalian placenta revealed by phylogenetic analysis

Perinatology Research Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 03/2006; 103(9):3203-8. DOI: 10.1073/pnas.0511344103
Source: PubMed


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.

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    • "In fact , ( pre - ovipositional ) matrotrophy is ancestral for extant mammals , as the monotreme situation indicates ( Blackburn 2005 , 2006 ) . The epitheliochorial placentation of various eutherian groups is derived within that group ( Wildman et al . , 2006 ; Elliot and Crespi , 2009 ; Carter and Enders , 2013 ) , and as noted above , may have arisen to limit placental nutrient transfer ( Mess and Carter , 2007 ) . One way to look at the difference between the two groups is that in eutherians , placentotrophy and a degree of fetal control over nutrient investment is ancestral , whereas in "
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    ABSTRACT: In placentotrophic viviparous reptiles, pregnant females deliver nutrients to their developing fetuses by diverse morphological specializations that reflect independent evolutionary origins. A survey of these specializations reveals a major emphasis on histotrophy (uterine secretion and fetal absorption) rather than hemotrophy (transfer between maternal and fetal blood streams). Of available hypotheses for the prevalence of histotrophic transfer, the most promising derives insights from the theoretical parent-offspring conflict over nutrient investment. I suggest that histotrophy gives pregnant females greater control over nutrient synthesis, storage, and delivery than hemotrophic transfer, reflecting maternal preeminence in any potential parent-offspring competition over nutrient investment. One lizard species shows invasive ovo-implantation and direct contact between fetal tissues and maternal blood vessels, potentially conferring control over nutrient transfer to the embryo. Future research on squamates will benefit from application of parent-offspring conflict theory to the transition from incipient to substantial matrotrophy, as well as by testing theory-derived predictions on both facultatively and highly placentotrophic forms. J. Exp. Zool. (Mol. Dev. Evol.) 9999B: 1-17, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Journal of Experimental Zoology Part B Molecular and Developmental Evolution 05/2015; 324(6). DOI:10.1002/jez.b.22624 · 2.31 Impact Factor
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    • "Many of them suggest that matrotrophy evolved to facilitate the evolution of some other feature of the life history. For example, it has been proposed that matrotrophy evolved to facilitate the evolution of larger litter size, larger offspring size at birth, improved survivorship early in life or earlier maturity (Thibault & Schultz 1978; Blackburn, Vitt & Beuchat 1984; Wourms & Lombardi 1992; Wourms 1993; Trexler 1997; Holbrook & Schal 2004; Schrader & Travis 2005; Wildman et al. 2006). We reference these hypotheses collectively as 'life history facilitation hypotheses' because they all share the attribute of predicting that matrotrophy evolves to facilitate the evolution of some other life-history trait. "
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    ABSTRACT: Most of what we know about placentas comes from mammals, yet little can be learned from them about the adaptive significance of the placental mode of reproduction because they all derived their placenta from a single common ancestor that lived over 100 million years ago. We can make inferences about the adaptive significance of placentation from fish in the family Poeciliidae because there have been multiple, recent origins of placentation, affording an opportunity to compare close relatives with and without placentas and to seek properties that are common to each origin of placentation.Here, we used field collections and a common garden study to quantify the degree of placentation and related it to aspects of the life history in two clades of live-bearing fish from the genus Poeciliopsis that each contains an independent origin of placentation. Doing so enables us to test the ‘life history facilitation hypothesis’, or the proposal that the placenta evolved to facilitate the evolution of some other feature of the life history.We found that the evolution of placentation in each clade is tightly correlated with the evolution of other components of the life history, but that the nature of the association is radically different across the two clades. In the Northern Clade the magnitude of post-fertilization maternal provisioning is negatively correlated with age at maturity, mass at maturity, offspring dry mass and interlitter interval. In contrast, degree of matrotrophy in the Southern Clade is positively correlated with age at maturity, mass at maturity, offspring dry mass and inter-litter interval.There is thus no consistent relationship between the evolution of placentas and other features of the life history, which negates those proposals that the placenta evolved to facilitate the evolution of other features of the life history. However, there is a negative correlation between degree of placentation and ovary dry mass and reproductive allocation common to both clades, suggesting that placentation may be an adaptation that facilitates a reduction in reproductive allocation.
    Functional Ecology 08/2014; 28(4). DOI:10.1111/1365-2435.12233 · 4.83 Impact Factor
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    • "Because there is little detailed information on the foundational processes of mammalian trophoblast invasion and its restriction, it is unclear whether the ontogenetic establishment of the carnivore paraplacenta follows similar processes as do the epitheliochorial placentas of close relatives within Laurasiatheria [2,32]. However, regarding the main fetomaternal exchange region of the placenta, comparative data [4-21] have confirmed that endotheliochorial, labyrinthine placentation belongs to the ancestral carnivore pattern [2,32]. Within the group, only hyenas have haemochorial placentas [13,14], which are hemomonochorial in nature, consisting of a continuous layer of syncytial trophoblasts, a basal lamina, and the fetal capillary endothelium [35]. "
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    ABSTRACT: Background Placental research in carnivores has concentrated on domestic species, which have zonary, labyrinthine placentas with an endotheliochorial barrier. Although the coati, Nasua nasua, is a widely distributed species in South America, data on the development of the placenta and the fetal membranes in this species are very sparse. Findings Four placentas from mid-gestation to near term were collected from wild individuals and were investigated based on gross morphology, histology, immunohistochemistry and electron microscopy. The available data support the concept that the ancestral condition of placentation in carnivores is phylogenetically characterized by a zonary and labyrinthine placental type with an endotheliochorial fetomaternal barrier, comprising extended epitheliochorial and haemochorial zones, such as hemophagous organs for iron supply and histiotrophe uptake and a yolk sac placenta. Conclusions Because of the foundational mechanisms that lead to the considerable complexity of fetomaternal contact zones in carnivores have not been studied, carnivores are interesting animal models for interhaemal barrier differentiation.
    Reproductive Biology and Endocrinology 06/2014; 12(1):57. DOI:10.1186/1477-7827-12-57 · 2.23 Impact Factor
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