Reasons for Diversity of Placental Structure
Article Outline
- Abstract
- 1. Introduction
- 2. Placental diversity as illustrated by hemomonochorial placentas
- 3. Major factors tending to increase diversity of placental structure
- 4. Lessons from placental variation
- 5. Conflict of interest
- References
- Copyright
Abstract
Many early embryonic stages are nearly indistinguishable in different Eutheria. However, implantation stages and placental morphological types vary tremendously. A number of factors favor this conflicting diversity. 1. Whereas embryo development takes place in the isolation of the amniotic cavity, the extraembryonic membranes of the conceptus develop in close association with the uterus of a genetically different organism. 2. Early conditions for the developing conceptus are anaerobic whereas later in development efficient aerobic conditions are essential for continued growth of the fetus. 3. Developing extraembryonic membranes have the potential to form two partially sequential placentas. The yolk sac can participate in forming a choriovitelline placenta, including an interhemal region, and can be adapted to various non-respiratory functions as gestation proceeds. Development of the chorioallantoic placenta begins later than the choriovitelline placenta but can overlap with this before supplanting it. The original development of the extraembryonic membranes occurs when the conceptus is sufficiently small that neither its nutritional requirements nor its respiratory needs are the burden to the maternal organism that they are later in gestation. Despite these developmental factors promoting different methods of forming the definitive placenta, the placental type is consistent within most families indicating that the divergence in placental structure accompanied evolution of differences between groups.
Keywords: Comparative placentation, Fetal membranes, Hemochorial placentation, Trophoblast
1. Introduction
Development of the embryo appears to be similar in different species, and is tightly controlled. Neural fold stages, somite stages, and other early embryonic stages are nearly indistinguishable in different Eutheria. However, placental types vary as do the implantation stages leading to these types. Therefore there must be factors favoring placental diversity and mechanisms by which this diversity can be achieved.
There are also non-variable features of placental development, including formation of viable young, decrease in size of the placenta relative to the fetus as gestation proceeds, early anaerobic conditions but later increasing aerobic needs, and first erythrocyte formation in the extraembryonic membranes. While it might be thought that the definitive placental type should always be one in which efficiency is greatest, i.e. least amount of increased energy expenditure by the maternal organism per increment of fetal weight gain, this is not necessarily the case. Taking just the condition of young at birth, altricial (immature) vs. precocial (highly developed): when the later involves large animals with the necessity to run or swim soon after birth, there is a relatively long gestation period. Extending the period of growth to limit the drain on the maternal system, i.e. decreasing the conflict between maternal well-being and fetal growth [1], may be more important than absolute efficiency. Similarly it may be particularly important to diminish the possibility of excessive exchanges of fetal and maternal cells when there is a longer gestation period, which could increase the possibility of various immunological and other problems [2].
No matter what the possible advantages and disadvantages of different placental types are, there is no question that there is a great deal of placental diversity among mammals.
2. Placental diversity as illustrated by hemomonochorial placentas
Recently Wildman [3] listed 41 eutherian species in which some of the genomics was known to compare with their placental type. Of those, more than 60% were listed as having hemochorial placentas. Many years ago I suggested that hemochorial placentas could be divided roughly into three types: hemomonochorial, hemodichorial and hemotrichorial, depending on the number of trophoblast layers in the interhemal region [4]. However, even taking just the hemomonochorial type, there is a great deal of structural difference (Fig. 1, Fig. 2, Fig. 3). For example, the villous hemomonochorial placenta with syncytial trophoblast may have persistent cellular trophoblast along the villi as in the human (Fig. 1A) [5], or may lack cellular trophoblast in this position with cytotrophoblast only at the villus tips as in the armadillo (Fig. 1B) [6]. In labyrinthine placental types with syncytial trophoblast, the trophoblast may have intrasyncytial bays and laminae as in sciuromorph rodents such as the marmot (Figs. 1C and 3A) [7] and elephant shrews [8], or may not have bays such as various of the hystricognath rodents illustrated here in the guinea pig (Fig. 1D) [9]. The hyena, in addition to being a labyrinthine placental type with syncytial trophoblast and intrasyncytial bays, has hemophagous regions (Fig. 2A) [10]. In species with a labyrinthine placenta but cellular trophoblast, some have intratrophoblast bays and laminae, such as molossid bats (Figs. 2B and 3B) [11], while others such as the jumping mouse (Fig. 2C) and jerboa do not [12], nor do hyraxes [13]. Some of the Tenrecidae such as the hedgehog tenrec Echinops (Fig. 2D) and the shrew tenrec Microgale not only have cellular trophoblast in the placental labyrinth, but in addition have hemophagous regions [14]. It should be noted that, despite the widespread distribution of intrasyncytial and intratrophoblast bays and laminae, their function is almost totally unknown and underinvestigated [15].
Fig. 1
Hemomonochorial placentas. A. Note the cytotrophoblast (Langhans) cells underlying the syncytial trophoblast in this villous hemomonochorial placenta of the human. B. Mature villus in the hemomonochorial placenta of the armadillo. Note the epithelioid mesenchymal cells. Inset: Growing villi in a mid-term placenta. Note that the cytotrophoblast cells (ct) are only at the tip of the villus. C. Midgestation labyrinthine placenta of the marmot, a sciuromorph rodent. Note the intrasyncytial bays (arrow). D. Labyrinth of the guinea pig, a hystricognath rodent. Syncytial trophoblast lines the maternal blood space but there are no intrasyncytial bays. (Transmission electron microscopy is definitive in determining the syncytial or cellular nature of trophoblast lining maternal blood spaces and in confirming the presence or absence of intrasyncytial bays.) fc = fetal capillaries. All micrographs except the inset are at the same magnification. Scale bar = 12 μm. Inset: 31 μm.
Fig. 2
Hemomonochorial placentas. A. Labyrinth of a midgestation placenta of the hyena, showing intrasyncytial bays (arrows). The hyena placenta has a number of different hemophagous regions (not shown). B. Labyrinth of the placenta of a molossid bat, Tadarida. This cellular hemomonochorial placenta has intratrophoblast bays (arrows) that are difficult to see with light microscopy. C. Placental labyrinth of the jumping mouse, Zapus. The cytotrophoblast (ct) lining maternal blood spaces does not have intratrophoblast bays. D. Placental labyrinth of the hedgehog tenrec, Echinops. The cytotrophoblast (ct) lining maternal blood spaces lacks intratrophoblast bays. In addition to the labyrinth there is a hemophagous region (not shown) in this placenta. Scale bar = 12 μm.
Fig. 3
Electron micrographs of interhemal regions. A. Labyrinth of a sciuromorph rodent showing the intrasyncytial bays and contained laminar material (arrows). B. Placental labyrinth of a molossid bat, Tadarida, showing intratrophoblast bays and lamina (arrows) in a cellular hemomonochorial placenta. mbs = maternal blood space. Scale bar: A = 2 μm, B = 4 μm.
Thus, without considering the presence or absence of spongy zones or the persistence of inverted or non-inverted yolk sacs, there are eight different types of placenta within the hemomonochorial group.
3. Major factors tending to increase diversity of placental structure
Several factors in development of extraembryonic membranes tend to increase the diversity in placental structure: the fact the early stages are anaerobic; that there are two organisms interacting; and that there are potentially two placental systems, the yolk sac and the chorioallantoic placenta.
3.1. Anaerobic early stages
Since the early stages of development are clearly anaerobic [16], there is no necessity for immediate development of a good system of oxygen transfer. Furthermore the amount of tissue involved and therefore the drain on the maternal organism is very small at this early stage. Therefore some of the areas of potential conflict between needs of the maternal organism and the developing conceptus are minimal, and there is no need for development at this stage to be particularly efficient. Neither do variations in extraembryonic membrane formation necessarily affect embryo formation. An example of this is mutations in the T locus or brachyury in mice, in which the allantois does not form properly but the embryos proceed well until the time of formation of the chorioallantoic placenta [17].
3.2. Conceptus–uterine interaction
The interaction of the uterus and conceptus can be highlighted by two very different examples of developmental cooperation. In myomorph rodents such as rats and mice, multiple blastocysts implant in a bicornuate uterus. The decidual response of the endometrium is responsible for an extensive series of events aiding implantation and placentation. These include orienting the conceptus and the initial deterioration of the uterine epithelium, especially mesometrial to the implantation site [18], as well as eventual inversion of the yolk sac. In the nine-banded armadillo on the other hand, the blastocyst implanting in the fundus of a simplex uterus takes advantage of pre-existing venous sinuses in the endometrium as a site for chorionic villus proliferation and secretory activity of the endometrium through expansion of the inverted yolk sac into the uterine lumen [6]. It has been suggested that the efficiency of the placental arrangement promoted polyembryony despite the lack of the reduced genetic diversity that this phenomenon leads to. There is no decidual response in this species.
3.3. Two potential placentas
In all eutherian species there are potentially two placentas forming, partially sequentially, with the yolk sac placenta slightly preceding the formation of the chorioallantoic placenta. The standard pattern of yolk sac formation might be considered formation of a vesicle that is partially vascularized and partially in contact with trophoblast, forming both a choriovitelline placenta and an avascular yolk sac [19]. (It should be noted that the yolk sac placenta, although vascularized, is more suitable for nutrition exchange and synthesis of proteins than it is for respiratory exchange.) Subsequently the yolk sac is displaced from proximity to the trophoblast by the expanding exocelom or allantois. All eutherians do start to form a yolk sac, and all retain some of its functions including first erythrocyte formation. Commonly some use is made of the visceral endoderm of the yolk sac in processing materials from the exocelom. But whether or not there is ever a choriovitelline placenta and use of the potential of this structure after the initial stages varies greatly. For example, disintegration of the parietal yolk sac and inversion of the yolk sac by loss of the parietal endoderm and associated trophoblast and decidua in later pregnancy in hystricognath and myomorph rodents make the visceral yolk sac especially well situated for nutritive and immunological transfer purposes [20], [21]. In contrast, the parietal endoderm of the primary yolk sac is used to form the first extraembryonic mesoderm in some primates [22], [23]. It would seem that, although mammals have the genetic potential to form a yolk sac and allantois, aspects of the development of these structures may be down-regulated at different stages in placental development.
Only after the initial stages of placenta formation does the need for efficient respiratory exchange become acute. It has been well known for decades that proximity of the two vascular systems is useful for respiratory exchange and in particular areas of extreme thinness are more efficient than use of a reduced but uniform average thinness. This thinning is accomplished by reducing trophoblast thickness regardless of the number of layers and, in most epitheliochorial and synepitheliochorial placentas, by maternal and fetal capillaries indenting the uterine epithelium and trophoblast, respectively.
4. Lessons from placental variation
Given the great potential for variability, why aren't there more variations in placental structure? While a totally inadequate placenta results in death of the fetus, even a partially inadequate placenta places the fetus in immediate disadvantage in species with multiple offspring (polytocous), and at a postpartum disadvantage in monotocous species, preventing the continuation of that genetic variant. When we look at the comparative data, almost always the placental type within families is the same, and in some instances there are only minor variation within orders. This suggests two things: that the accuracy of our systematics prior to genomics was reasonably good at the family and order levels, and that the evolution of placental differences accompanied the divergence of mammalian groups. It also suggests that placental type is more fundamental than adaptations to seasonal and regional differences such as delayed implantation, delayed development, delayed fertilization, hibernation and estivation, which can vary within families.
Finally, it is instructive to compare placentation in what is considered a relatively primitive mammal such as the hedgehog tenrec [24], [25] and a primate such as the macaque. The hedgehog tenrec retains the allantois as a sac bringing the allantoic vessels to the forming chorioallantoic placenta. It retains a yolk sac during the early stages of development, including a vascularized portion, and it uses cytotrophoblast to ingest erythrocytes and therefore for transfer of iron. The macaque does not form an allantois per se, uses some of the endoderm of the primary yolk sac for extraembryonic mesoderm, and in later pregnancy centralizes all of the functions such as amino acid and glucose transport, hormone secretion, IgG uptake, iron transfer, etc., in the syncytial trophoblast of the chorioallantoic placenta. The placenta of the hedgehog tenrec appears more complicated than that of the macaque, yet it is probable that enabling syncytial trophoblast to perform the vast majority of functions is evolutionarily more difficult than making use of multiple components, similar to those involved in other amniotes, to create a successful placenta.
5. Conflict of interest
The author does not have any potential or actual personal, political, or financial interest in the material, information, or techniques described in this paper.
References
- . Altercation of generations: genetic conflicts of pregnancy. Am J Reprod Immunol. 1996;35:226–232
- . Why is the fetal allograft not rejected?. J Anim Sci. 2007;85:E32–E35
- . Sources for comparative studies of placentation. II. Genomic resources. Placenta. 2008;29:144–147
- . A comparative study of the fine structure of the trophoblast in several hemochorial placentas. Am J Anat. 1965;116:29–68
- . A re-appraisal of the morphophenotype and basal lamina coverage of cytotrophoblasts in human term placenta. Placenta. 2008;29:215–219
- . Placentation in armadillos, with emphasis on development of the placenta in polyembryonic species. In: Loughry WJ, Vizcaino SF editor. Biology of the Xenarthra. Gainesville: University Press of Florida; 2008;p. 172–180
- . Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol. 2004;2:46
- . Ultrastructural observations on the chorioallantoic placenta of the golden-rumped elephant shrew, Rhynchocyon chrysopygus. Afr J Ecol. 1985;23:155–166
- . Evolutionary transformations of chorioallantoic placental characters in Rodentia with special reference to hystricognath species. J Exp Zool. 2003;299A:78–98
- . Structure of the midterm placenta of the spotted hyena, Crocuta crocuta, with emphasis on the diverse hemophagous regions. Cells Tissues Organs. 2006;183:141–155
- . Development of the discoidal hemochorial placenta in the black mastiff bat, Molossus ater: evidence for a role of maternal endothelial cells in the control of trophoblastic growth. Am J Anat. 1991;191:185–207
- . The fetal membranes and unusual giant cell placenta of the jerboa (Jaculus) and jumping mouse (Zapus). Am J Anat. 1974;140:405–432
- . Electron microscopic study of the chorioallantoic placenta of the rock hyrax (Heterohyrax brucei). J Reprod Fertil. 1983;68:311–316
- . Placental diversity in Malagasy tenrecs: placentation in shrew tenrecs (Microgale spp.), the mole-like rice tenrec (Oryzorictes hova) and the web-footed tenrec (Limnogale mergulus). Placenta. 2007;28:748–759
- . Synthesis and transport studies of the intrasyncytial lamina: an unusual placental basement membrane in the little brown bat, Myotis luciugus. Am J Anat. 1987;178:387–409
- . The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus – a review. Placenta. 2002;24:S86–S93
- . Brachyury is required for elongation and vasculogenesis in the murine allantois. Development. 2006;133:2947–2959
- . Chorioallantoic placenta formation in the rat: I. Luminal epithelial cell death and extracellular matrix modifications in the mesometrial region of implantation chambers. Am J Anat. 1991;192:347–365
- . Comparative development of the mammalian yolk sac. In: Nogales FF editors. The human yolk sac and yolk sac tumors. Berlin: Springer-Verlag; 1993;p. 1–32
- . The transmission of passive immunity from mother to young. Amsterdam: North Holland; 1970;
- . Chorioallantoic and yolk sac placentation in the dassie rat Petromus typicus and its significance for the evolution of hystricognath rodents. Placenta. 2007;28:1229–1233
- . Formation and differentiation of extraembryonic mesoderm in the rhesus monkey. Am J Anat. 1988;181:327–340
- . The origin of extraembryonic mesoderm in experimental animals: relevance to chorionic mosaicism in humans. Am J Med Gen. 1993;46:542–550
- . Structure of the definitive placenta of the tenrec, Echinops telfairi. Placenta. 2004;25:218–232
- . Development of the haemophagous region and labyrinth of the placenta of the tenrec, Echinops telfairi. Placenta. 2005;26:251–261
PII: S0143-4004(08)00333-0
doi:10.1016/j.placenta.2008.09.018
© 2009 IFPA and Elsevier Ltd. All rights reserved.
