By contrast, there is only a single copy of the PRL gene in the human, whereas there are 23 members in the mouse, 24 in the rat, and 12 in cattle (Haig 1993). Longmans, London, pp 127311, Bell AW, Ehrhardt RA (2002) Regulation of placental nutrient transport and implications for fetal growth. They are transcribed from multiple, structurally conserved genes that have probably arisen by duplications and gene conversion events from another Type 1 IFN gene, interferon omega (IFNW). Haig D . Cell Mo Immunol 8: 111. In marsupials, the yolk sac forms the definitive placenta being responsible for physiological exchange whereas eutherian mammalian placentae can be deeply invasive into the maternal endometrium (haemochorial), requiring increased maternalfoetal co-adaptation. Some 13 genes have been reported as specifically expressed in the mouse placenta all of which are maternally expressed (Hudson et al., 2010). Managing mom's health concerns. Such matching may be important for coordination of downstream gene expression to specifics cell types (placenta, neurons) and coordinate specific functions. This condition occurs when the blood vessels and other parts of the placenta grow too deeply into the uterine wall. An overview of sex and reproductive immunity from an evolutionary Expect your health care provider to monitor your condition closely throughout the pregnancy. No evidence for interaction of the mothers immune response by immunological T-cell recognition has been found for the invasive placenta of humans and rodents, which may explain how has the placenta evolved to avoid rejection. Advancing computational tools coupled with increasing genome availability across species that utilize different reproductive strategies promise to reveal the molecular underpinnings of the ancestral transition of oviparity to viviparity. Mol Ecol. Uterine NK cells produce a variety of growth factors and angiogenic factors and are major regulators of vascular remodelling in the early stages of pregnancy, declining as pregnancy progresses (Zhang et al., 2011). Phil Trans Roy Soc B 368: 20110327. Inclusion in an NLM database does not imply endorsement of, or agreement with, pp 2134. We close the review by discussing mechanisms that might have favored diversity and hence evolution of the morphology and physiology of the placentas of eutherian mammals. The IFNT proteins are secreted from mononucleated trophoblasts and act on the uterus by binding to type I interferon receptors, with the period of release occurring before the trophoblast has formed definite attachment to the uterine epithelium (Bazer, et al. Not only have more genes been recruited to ICRs, but many of these genes form extensive networks with other imprinted genes (Sumida and Ohlsson, 2010). Denner J. Phillips JE, Corces VG . Conversely, ERVV2 is expressed in human placenta but does not appear to be involved in cytotrophoblast fusion (Blaise, et al. 1. amnion encloses the compartment of fluid that bathes the embryo and acts as a shock absorber 2. chorion - attached to all antis, gas exchange between embryo and air 3. all antis - has blood vessels, functions in waste removal and gas exchange 4. yolk sac - contains yolk/nutrients and transports them to the embryo. (2012). Structure Placental mammals, including humans, have a chorioallantoic placenta that forms from the chorion and allantois. DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Viviparity apparently evolves from oviparity via egg-retention, and such taxa may thus stillhave the machinery to produce thick-shelled eggs. Bazer FW, Spencer TE, Ott TL. Facultative oviparity in a viviparous skink ( Saiphos equalis). Placentation in the eastern water skink (Eulamprus quoyii): a placentome-like structure in a lecithotrophic lizard. 2015). The mature embryo of the cownose ray, for example, weighs 3000 times as much as the egg as a result of reliance on the mother rather than the egg yolk (Hamlett, et al. (2009). Natural killer cell-triggered vascular transformation: maternal care before birth? In utero development cannot tolerate errors. (2002). Martin RJ, et al., eds. Accessed Feb. 6, 2020. Shufaro Y, Lacham-Kaplan O, Tzuberi BZ, McLaughlin J, Trounson A, Cedar H . Parental responsiveness is feminized after neonatal castration in virgin male prairie voles, but is not masculinized by perinatal testosterone in virgin females. Accessed Feb. 7, 2020. (2012). There is also evidence for expression of active transporters at the sites of maternal-fetal apposition in some species (Murphy, et al. Also products of multi-gene families likely overlap in function, so that a loss of one gene may be compensated by the presence of one or more of its orthologs. PMID: 24569636 PMCID: PMC4105457 DOI: 10.1038/hdy.2014.8 Abstract Evolution of mammalian reproductive success has witnessed a strong dependence on maternal resources through placental in utero development. Although there are clear morphological similarities in the steps leading to blastocyst formation in rodents, humans, and domestic mammalian species, there are differences in how events are timed and subsequently play out. FOXL2 versus SOX9: a lifelong battle of the sexes. Molecular genetic studies have identified several of the imprinted genes, which are co-expressed in the developing hypothalamus and placenta, to be concerned with regulation of maternal behaviour and physiology (Keverne, 2012). Viviparity involves some form of placental exchange between mother and fetus and may have evolved to help offspring survive in cooler climates (Bellairs 1969f; Palmer et al. A placenta, as defined originally by Mossman, is the apposition or fusion of the fetal membranes to the uterine mucosa for physiological exchange (Burton and Jauniaux 2015). How did viviparity originate and evolve? Iron deficiency anemia during pregnancy: Prevention tips. Although the control of imprints (ICR and DMR) is matrilineal, many imprinted genes are paternally expressed by virtue of this maternal silencing. BioEssays 31: 13181326. Landon MB, et al., eds. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. Pask AJ, Papenfuss AT, Ager EL, MColl KA, Speed TP, Renfree MB . It is a phenomenon whereby developing embryos are retained within the reproductive tract, leading to release of live offspring as an alternative to the more fecund egg laying or spawning. A more primitive condition, known as ovoviviparity and found in certain snakes, is the simple retention of the egg until it hatches. (1997). When and how trophoblast emerged in the presumed metatherian ancestors of the Class Mammalia is mysterious and unlikely ever to be revealed from the fossil record. In this short review of placental evolution, we first describe the emergence of placental-like structures in non-mammalian vertebrates and then transition to mammals themselves. Here's what you need to know about these conditions: Placenta previa. Amorosos review on placentation (Amoroso 1952), which were redrawn from Weekes (Weekes 1935). In addition to providing resources from mother over lengthy pregnancies, the placenta has to hormonally prime the mothers hypothalamus to ensure maternal care and provision of milk. Emergence of an evolutionary innovation: Gene expression differences associated with the transition between oviparity and viviparity. The Evolution of Viviparity in Vertebrates - PubMed FOIA It is also notable that ERVW-1 is not involved in trophoblast fusion in Old World monkeys, despite being present in their genomes (Cceres, et al. 2011 Jul;181(5):575-94. doi: 10.1007/s00360-011-0584-0. Very few publications on genomic imprinting had appeared at the time when parentoffspring conflict was formulated (Haig, 1992) or indeed the theory of parentoffspring co-adaptation (Curley et al., 2004; Wolf and Hager, 2006). The https:// ensures that you are connecting to the The placenta might partially or completely cover the cervix, as shown here. Although the placentas of marsupials are generally regarded as non-invasive and of the epitheliochorial type (see next section), an area of syncytium forms in the yolk sac placenta of the gray short-tailed opossum and possibly related species. This is supported by Missouri Mission Enhancement Funds (LCS), Food for the 21st Cnetury Support from the University of Missouri (RMR & JAG) and a NIH Eunice Kennedy Shriver National Institute of Child Health and Human Development Grant (R01 HD069979) (RMR). Correspondence should be addressed to R Michael Roberts; The publisher's final edited version of this article is available at. Hubrecht AA. Moore KL, et al. Placental development and physiology. Cartoon illustrating the diversity of placental morphologies encountered in placental mammals, 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. 5A), often squeezing down to the tight junctions between the trophoblast cells on the one side and uterine epithelial cells on the other, probably allowing efficient exchange of small molecules (Friess, et al. Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogen-related genes is not associated with their position in the locus. H19 may have tumour-suppressor activity when combined with Igf2, whereas Peg10 encodes a protein with homologies to retrotransposons. The section illustrates the folded placental face likely involved in releasing histotrophic material that can be taken up by the chorionic ectoderm. Thus, some genes may evolve imprinting status because selection favours parent-of-origin dependent status, other genes may evolve imprinting as a co-evolutionary response to match the expression pattern of their interacting neighbours (Wolf, 2013). In: Parkes A, editor. In the mouse (Mus musculus), the first visible differentiation event, called compaction, occurs between the 8- and 16-cell stage of embryonic development when the blastomeres polarize to form extended contact zones with their neighbors and an outward-facing apical surface (Posfai, et al. (2009). Haig D . Kulinski TM, Barlow DP, Hudson QJ . (2008). (2010). Fowden AL, Constancia M. Maternal-fetal resource allocation. 2009). Cambridge University Press: New York. The placenta attaches to the wall of the uterus, and the baby's umbilical cord arises from it. Tunster SJ, Jensen AB, John RM . What can comparative studies of placental structure tell us?A review. Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis. Broad KD, Keverne EB . Familari M, Au PC, de Iongh RU, Cruz Y, Selwood L. Expression analysis of Cdx2 and Pou5f1 in a marsupial, the stripe-faced dunnart, during early development. Widespread monoallelic expression on human autosomes. Evolution of mammalian reproductive success has witnessed a strong dependence on maternal resources through placental in utero development. The trophoblast cells originating from the marsupial blastocyst combine with yolk sac endoderm and extra-embryonic mesoderm to form a yolk sac placenta, which can be bi- or trilaminar (Renfree 2010). Also such placentas have a resemblance to placentas described earlier for non-mammalian species, such as skinks (Fig. Accessibility 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. The evolutionary clustering in the organisation of these imprinted genes enables the epigenetic initiator to extend imprinted silencing of paternal alleles over broad chromosomal domains (Kulinski et al., 2013). 2014). Although a balanced regulation of in utero foetal growth under control of Igf2 and its receptor still hold, the complexity of balanced paternal gene expression (H19 and Mir675) and the importance of maternal CTCF in enabling Igf2 expression are difficult to reconcile with conflict. The human and mouse placenta have a trichorial structure with two multinucleated syncytiotrophoblast layers representing a barrier between the maternal and foetal vascular systems. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. Placental protection of the fetal brain during short-term food deprivation. Find out what it does, issues that might affect the placenta and how the placenta is delivered. 2006) (Fig. 5C) (Renegar, et al. Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal-fetal hormone exchange. Keverne EB . This non-coding RNA targets the growth-promoting Igf2 receptor and functions in limiting the growth of the eutherian placenta later in pregnancy. Evolution of Oviductal Gestation in Amphibians. The story of vertebrate placentation, therefore, is one of convergent evolution at both the macro- and molecular levels. 25th ed. Analysis of the platypus genome suggests a transposon origin for mammalian imprinting. information highlighted below and resubmit the form. Accessed Feb. 6, 2020. Non-coding RNA is thought to be primarily responsible for paternal silencing of this particular form of placental-specific imprinting (Pauler et al., 2012). The young lick the milk from a mammary patch on the mother's belly. Also tell your health care provider if you've had surgery on your uterus in the past. Wolf JB . Bethesda, MD 20894, Web Policies Methylation of cytosines in ICRs increases the rate of C-T transition mutations, higher in the male germline because of the longer germline passage and the greater number of cell divisions. Paternal ICRs are intergenic and tend to evolve neutrally while maternal ICRs coincide with CpG-rich promoters that are under selection pressure for conserving sequences that are linked to promoter functions. (2009). -. Nat Rev Genet 2: 538548. This chapter will briefly explore the vertebrate modes of reproduction using a phylogenetic framework and where possible highlight the role of potential candidate genes that may help explain the polygenic origins of live birth. We thank Dennis Reith for editorial help, Susan Roberts, Nico Zevallos, and Dr. Ye Yuan for assistance in preparing Figures. Proc Natl Acad Sci USA 108: 1523715241. The marsupial placenta: A phylogenetic analysis. It provides the trigger for sex determination by activating Sox9 that not only brings about testes formation but blocks the genetic pathway to the differentiation of ovarian cells (Veitia, 2010). Keverne, E. Mammalian viviparity: a complex niche in the evolution of genomic imprinting. For details on how placentas subsequently develop and begin to diverge in morphology, the reader is directed to the still germane reviews by Amoroso (Amoroso 1952) and Renfree (Renfree 1982). (2010). Implantation and Placentation Vol 2, Reproduction in Mammals: Embryonic and Fetal Development. (2012). (2006). Sato Y, Shinka Y, Sakamoto K, Ewis AA, Nakahori Y . Amoroso E. Placentation. Weinreich DM, Watson RA, Chao L. Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. (2013). Heredity It is also possible that the hypomethylated state of the placental genome (Chuong 2013) has permitted relaxed silencing of gene control elements, including those of ERVs. It is hemotrichorial, i.e. A second force driving placental evolution is undoubtedly avoidance of immune rejection (Hemberger 2013), a process still little understood, although speculation abounds. Mechanisms of activation of the paternally expressed genes by the Prader-Willi imprinting center in the Prader-Will/Angelman syndrome domains. Placentas, whatever their anatomic features, share a number of common functions, all of which require cooperative interactions with the maternal system. Placenta previa can cause severe vaginal bleeding during pregnancy or delivery. Cceres M, NCS Program. 1993), which becomes closely apposed to the epithelium of a highly vascularized oviduct. Such genomic dysregulation does not occur in the foetal hypothalamus where Peg3 expression increases with maternal food deprivation. There are 10 intact PSG genes in the human genome and 17 in mouse (McLellan, et al. The placental hormones terminate fertility and suppress sexual behaviour in most female species, ensuring that maternal feeding time and energy expenditure are directed towards a successful pregnancy. Click here for an email preview. Frequently asked questions: Pregnancy FAQ038: Bleeding during pregnancy. the contents by NLM or the National Institutes of Health. Although placentation arose once in the common ancestor of mammals, it has arisen independently multiple times within other classes, and even families. No placenta: Usually a simple placenta, but some species more complex than others: Complex placenta: Highly altricial young Echidna Lay (usually) 1 egg that hatches in 9 days After hatching it lives in its mother's pouch (really just a groove in the abdomen) for 12 weeks Spines at 8 weeks Gimelbrant A, Hutchinson JN, Thompson BR, Chess A . The prolactin family: effectors of pregnancy-dependent adaptations. Before Singh P, Lee DH, Szabo PE . How do viviparity and the placenta affect mammalian reproduction? Moreover, the organization of the domains in human and mouse PSG proteins are quite different (McLellan, et al. (2010). These same placental hormones induce nest building in advance of birth and also prime the hypothalamus for post-partum maternal care and milk letdown (Figure 1). The ICRs appear to be gaining more genes from rodents to humans and are particularly important for regulation of gene dosage, as revealed from the complex disrupted phenotypes that are produced by perturbations to the ICR without any effects on the imprinted genes themselves in PraderWilli syndrome and Angelmans syndrome (Rabinovitz et al., 2012) and SilverRussell syndrome (Kagami et al., 2007). (2005). 5C). The degree of contact and exchange between developing embryos and the father range from minimal to situations that display all the defining features of placentation (Wilson, et al. This type of reproduction involves the mother giving birth to live offspring that have fully matured inside her body. Placenta previa. In rare cases, the placenta might attach in the lower area of the uterus. Veitia RA . -, Blackburn DG (1999) Viviparity and oviparity: evolution and reproductive strategies. Malassine A, Blaise S, Handschuh K, Lalucque H, Dupressoir A, Evain-Brion D, Heidmann T. Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta: How it works, what's normal - Mayo Clinic Which of the following deuterostomes is most likely to be found in nature? Proc Natl Acad Sci USA 104: 1772517729. In the pig, where maternal recognition of pregnancy is also achieved during the period when the conceptuses are elongating within the uterine lumen, the antiluteolytic factor appears not to be a protein, but is instead the steroid hormone estrogen (Spencer, et al. A different placental type, the yolk sac placenta, has evolved multiple times in the ground sharks(Wourms and Lombardi 1992). The placenta as a model for understanding the origin and - Nature Amey KL, Bae E, Olsen C, Drewell RA . Mechanisms of long range silencing by imprinted macro non-coding RNAs. Check out these best-sellers and special offers on books and newsletters from Mayo Clinic Press. Hemberger M. Immune balance at the foeto-maternal interface as the fulcrum of reproductive success. (2012). Although exposed to the maternal immune system, this foeto-placental interface does not express leucocyte T-cell antigens. Placental PAGs: gene origins, expression patterns, and use as markers of pregnancy. Reik W, Constancia M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, Tycko B, Sibley C. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. The presence of a micro-RNA (Mir675) embedded in the first exon of paternal H19, and expressed exclusively in the placenta, has recently been identified (Keniry et al., 2012). Rizzoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, Lovell-Badge R . Thus, the foetus controls its own destiny in times of acute starvation, especially in the last trimester of pregnancy, by short-term sacrifice of its placenta to preserve resources critical for brain development. HHS Vulnerability Disclosure, Help 2007). Proc Natl Acad Sci USA 109: 74037408. As a result, the fate of most ERVs is gradual genetic degradation through mutation and homologous recombination. GCM1, a transcription factor that plays a role in controlling the formation of syncytial trophoblast (STB)(Cross, et al. In the vertebrate tree of life, viviparity or live birth has independently evolved many times, resulting in a rich diversity of reproductive strategies. Following ovulation, secretory cells of the vascularized pouch enlarge. The diagrams are based on Fig. Estrus, or "heat," typically coincides with ovulation, and during this time the female is receptive to the male. (2013). Genomic imprinting in the placenta. 2009). Keverne EB . Interferon tau: a novel pregnancy recognition signal. (2001). McLellan AS, Zimmermann W, Moore T. Conservation of pregnancy-specific glycoprotein (PSG) N domains following independent expansions of the gene families in rodents and primates. What is clear is that the mechanisms are highly variable, evolving rapidly, and no one approach is used widely across taxa. The latter situation, of necessity, is expected to lead to increased conflict over how provisions are partitioned between the supplier and the recipient, thus potentially sparking a genetic arms race. The Trophoblast: A Rejoinder. Vaiman D, Mondon F, Garces-Duran A, Mignot TM, Robert B, Rebourcet R et al. doi: 10.1530/REP-13-0309. Sign up for free and stay up to date on research advancements, health tips, current health topics, and expertise on managing health. Mammal - Reproduction & social behavior | Britannica You might be asked to push one more time to deliver the placenta. 1). Retained placenta after vaginal birth and length of the third stage of labor. 2016 Nov; 152(5): R179R189. Chen Z, Hagen DE, Wang J, Elsik CG, Ji T, Siqueira LG, Hansen PJ, Rivera RM. Point mutations, expanded tandem repeats and structural chromosome mutations predominate through partilineal transmission (Marchetti et al., 2007). Gene duplication provides a useful opportunity for natural selection to operate (Hughes 1994) and allows the duplicated genes to acquire new functions, and, through the acquisition or loss of regulatory regions, changes in the temporal, spatial or magnitude of transcription compared to the original gene. Certainly, in the context of genomic imprinting, it is the heritable epigenetic non-coding ICR, which are of primary evolutionary significance. A second env gene from a different endogenous retrovirus (ERVFRD-1; syncytin-2) is expressed in villous trophoblast of the human placenta (Blaise, et al. Study with Quizlet and memorize flashcards containing terms like Which of the following statements best represents evidence supporting the leading hypothesis regarding the evolution of jaws in vertebrates?, Which statement about deuterostomes is correct?, What is the name given to the group of species on the branch leading to contemporary humans? Pink CJ, Hurst LD . Curr Opin Cell Biol 25: 297304. 3) However, this is clearly not the case (Wildman, et al. Mammalian viviparity has to contend with a semi-allogenic foetus, especially during invasive haemochorial placentation, which characterises rodents and primates where foetal trophoblast cells intermingle with maternal tissue (Rossant and Cross, 2001). Nature 489: 91100. In many species, the embryo, relies on egg contents for nutrition, but, in others, a range of adaptations of the female reproductive tract provides a means to exchange gases and nutrients with the conceptus (Stewart 2015). Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting. National Library of Medicine Hutter B, Bieg M, Helms V, Paulsen M . Kalinka AT. In some taxa this includes the evolution of a specialized interface, the placenta, between fetal and maternal tis-