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Placentation in Mammals pp 41–60Cite as

Placentation in Marsupials

Part of the Advances in Anatomy, Embryology and Cell Biology book series (ADVSANAT,volume 234)

Abstract

It is sometimes implied that marsupials are “aplacental,” on the presumption that the only mammals that have a placenta are the eponymous “placental” mammals. This misconception has persisted despite the interest in and descriptions of the marsupial placenta, even in Amoroso’s definitive chapter. It was also said that marsupials had no maternal recognition of pregnancy and no placental hormone production. In addition, it was thought that genomic imprinting could not exist in marsupials because pregnancy was so short. We now know that none of these ideas have held true with extensive studies over the last four decades definitively showing that they are indeed mammals with a fully functional placenta, and with their own specializations.

Keywords

  • Marsupial
  • Tammar wallaby
  • Placenta
  • Yolk sac
  • Trophoblast
  • Endometrium
  • Diapause
  • Inflammation
  • Transcriptome
  • Omphalopleure
  • Genomic imprinting
  • ALID

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References

  • Ager E, Suzuki S, Pask A, Shaw G, Ishino F, Renfree MB (2007) Insulin is imprinted in the placenta of the marsupial, Macropus eugenii. Dev Biol 309:317–328

    CAS  PubMed  Google Scholar 

  • Ager EI, Pask AJ, Gehring HM, Shaw G, Renfree MB (2008a) Evolution of the CDKN1C-KCNQ1 imprinted domain. BMC Evol Biol 8:163

    PubMed  PubMed Central  Google Scholar 

  • Ager EI, Pask AJ, Shaw G, Renfree MB (2008b) Expression and protein localisation of IGF2 in the marsupial placenta. BMC Dev Biol 8:17

    PubMed  PubMed Central  Google Scholar 

  • Amoroso EC (1952) Placentation, Marshall’s physiology of reproduction. Longman, Green and Co., London, pp 127–311

    Google Scholar 

  • Armstrong DL, McGowen MR, Weckle A, Pantham P, Caravas J, Agnew D, Benirschke K, Savage-Rumbaugh S, Nevo E, Kim CJ, Wagner GP, Romero R, Wildman DE (2017) The core transcriptome of mammalian placentas and the divergence of expression with placental shape. Placenta 57:71–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beckman DA, Brent RL, Lloyd JB (1996) Sources of amino acids for protein synthesis during early organogenesis in the rat. 4. Mechanisms before envelopment of the embryo by the yolk sac. Placenta 17:635–641

    CAS  PubMed  Google Scholar 

  • Buentjen I, Drews B, Frankenberg SR, Hildebrandt TB, Renfree MB, Menzies BR (2015) Characterisation of major histocompatibility complex class I genes at the fetal-maternal interface of marsupials. Immunogenetics 67:385–393

    CAS  PubMed  Google Scholar 

  • Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E (2002) Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab 87:2954–2959

    CAS  PubMed  Google Scholar 

  • Carter AM (2018) Recent advances in understanding evolution of the placenta: insights from transcriptomics. F1000Res 7:89

    PubMed  PubMed Central  Google Scholar 

  • Carter AM (2020) The role of mammalian foetal membranes in early embryogenesis: lessons from marsupials. J Morphol:1–3

    Google Scholar 

  • Carter AM, Enders AC (2016) Placentation in mammals: definitive placenta, yolk sac, and paraplacenta. Theriogenology 86:278–287

    CAS  PubMed  Google Scholar 

  • Cha J, Sun X, Bartos A, Fenelon J, Lefevre P, Daikoku T, Shaw G, Maxson R, Murphy BD, Renfree MB, Dey SK (2013) A new role for muscle segment homeobox genes in mammalian embryonic diapause. Open Biol 3:130035

    PubMed  PubMed Central  Google Scholar 

  • Cha J, Fenelon J, Murphy BD, Shaw G, Renfree MB, Dey SK (2020) A role for Msx genes in mammalian embryonic diapause. Biosci Proc 10:44–51

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chavan AR, Griffith OW, Stadtmauer D, Maziarz J, Pavlicev M, Fishman R, Koren L, Romero R, Wagner GP (2018) Evolution of embryo implantation was enabled by the origin of decidual cells in eutherian mammals. BioRxiv. https://doi.org/10.1101/429571

  • Cheng Y, Wakefield M, Siddle HV, Coggill PC, Herbert CA, Beck S, Belov K, Eldridge MD (2009) Isolation and characterization of 10 MHC Class I-associated microsatellite loci in tammar wallaby (Macropus eugenii). Mol Ecol Resour 9:346–349

    CAS  PubMed  Google Scholar 

  • Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, Nilsson MA, Menzies BR, Renfree MB, Pierron G, Zeller U, Heidmann O, Dupressoir A, Heidmann T (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A 112:E487–E496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz YP, Selwood L (1997) Histological differences between gravid and non-gravid uteri in the dasyurid marsupial, Sminthopsis macroura (Spencer). J Reprod Fertil 111:319–325

    CAS  PubMed  Google Scholar 

  • Denker HW, Tyndale-Biscoe CH (1986) Embryo implantation and proteinase activities in a marsupial (Macropus eugenii). Histochemical patterns of proteinases in various gestational stages. Cell Tissue Res 246:279–291

    PubMed  Google Scholar 

  • Dudley JS, Murphy CR, Thompson MB, McAllan BM (2015) Desmoglein-2 during pregnancy and its role in the evolution of viviparity in a marsupial (Sminthopsis crassicaudata; Dasyuridae). J Morphol 276:261–272

    CAS  PubMed  Google Scholar 

  • Dudley JS, Murphy CR, Thompson MB, McAllan BM (2017) Epithelial cadherin disassociates from the lateral plasma membrane of uterine epithelial cells throughout pregnancy in a marsupial. J Anat 231:359–365

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enders AC, Carter AM (2006) Comparative placentation: some interesting modifications for histotrophic nutrition—a review. Placenta 27(Suppl A):S11–S16

    PubMed  Google Scholar 

  • Fenelon JC, Murphy BD (2019) New functions for old factors: the role of polyamines during the establishment of pregnancy. Reprod Fertil Dev 31:1228–1239

    CAS  PubMed  Google Scholar 

  • Fenelon JC, Shaw G, Frankenberg SR, Murphy BD, Renfree MB (2017) Embryo arrest and reactivation: potential candidates controlling embryonic diapause in the tammar wallaby and minkdagger. Biol Reprod 96:877–894

    PubMed  Google Scholar 

  • Flynn TT (1923) The yolk-sac and allantoic placenta in Perameles. Q J Microsc Sci 67:123–182

    Google Scholar 

  • Flynn TT (1930) The uterine cycle of pregnancy and pseudo-pregnancy as it is in the diprotodont marsupial Bettongia cuniculus. Proc Linn Soc N S W 55:506–531

    Google Scholar 

  • Freyer C (2003) The placenta in the original marsupial stem species, zoology. The Universiyt of Melbourne, Parkville

    Google Scholar 

  • Freyer C, Renfree MB (2009) The mammalian yolk sac placenta. J Exp Zool B Mol Dev Evol 312:545–554

    PubMed  Google Scholar 

  • Freyer C, Zeller U, Renfree MB (2002) Ultrastructure of the placenta of the tammar wallaby, Macropus eugenii: comparison with the grey short-tailed opossum, Monodelphis domestica. J Anat 201:101–119

    PubMed  PubMed Central  Google Scholar 

  • Freyer C, Zeller U, Renfree MB (2003) The marsupial placenta: a phylogenetic analysis. J Exp Zool A Comp Exp Biol 299:59–77

    PubMed  Google Scholar 

  • Freyer C, Zeller U, Renfree MB (2007) Placental function in two distantly related marsupials. Placenta 28:249–257

    CAS  PubMed  Google Scholar 

  • Griffith OW, Chavan AR, Protopapas S, Maziarz J, Romero R, Wagner GP (2017) Embryo implantation evolved from an ancestral inflammatory attachment reaction. Proc Natl Acad Sci U S A 114:E6566–E6575

    CAS  PubMed  Google Scholar 

  • Griffith OW, Chavan AR, Pavlicev M, Protopapas S, Callahan R, Maziarz J, Wagner GP (2019) Endometrial recognition of pregnancy occurs in the grey short-tailed opossum (Monodelphis domestica). Proc Biol Sci 286:20190691

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guernsey MW, Chuong EB, Cornelis G, Renfree MB, Baker JC (2017) Molecular conservation of marsupial and eutherian placentation and lactation. Elife 6

    Google Scholar 

  • Gulbis B, Jauniaux E, Decuyper J, Thiry P, Jurkovic D, Campbell S (1994) Distribution of iron and iron-binding proteins in first-trimester human pregnancies. Obstet Gynecol 84:289–293

    CAS  PubMed  Google Scholar 

  • Gulbis B, Jauniaux E, Cotton F, Stordeur P (1998) Protein and enzyme patterns in the fluid cavities of the first trimester gestational sac: relevance to the absorptive role of secondary yolk sac. Mol Hum Reprod 4:857–862

    CAS  PubMed  Google Scholar 

  • Heap RB, Renfree MB, Burton RD (1980) Steroid metabolism in the yolk sac placenta and endometrium of the tammar wallaby, Macropus eugenii. J Endocrinol 87:339–349

    CAS  PubMed  Google Scholar 

  • Hill JP (1897) The placenation of Perameles. Q J Microsc Sci 40:385–446

    Google Scholar 

  • Hill JP (1900) Contributions to the embryology of the Marsupialia. 2. On a further stage of placentation of Perameles. 3. On the foetal membrane of Macropus purma. Q J Microsc Sci 43:1–22

    Google Scholar 

  • Hughes RL (1974) Morphological studies on implantation in marsupials. J Reprod Fertil 39:173–186

    CAS  PubMed  Google Scholar 

  • Hughes RL, Green RH (1998) Placentation and adaptations for survival at birth in the common wombat Vombatus ursinus. In: Wells RT, Pridmore PA (eds) Wombats. Sulley Beatty and Sons/Royal Zoological Society of South Australia, Chipping Norton, NSW, pp 86–108

    Google Scholar 

  • Jauniaux E, Gulbis B, Jurkovic D, Campbell S, Collins WP, Ooms HA (1994) Relationship between protein concentrations in embryological fluids and maternal serum and yolk sac size during human early pregnancy. Hum Reprod 9:161–166

    CAS  PubMed  Google Scholar 

  • Jones CJP, Jauniaux E (1995) Ultrastructure of the materno-embryonic interface in the first trimester of pregnancy. Micron 26:145–173

    CAS  PubMed  Google Scholar 

  • King B, Enders A (1993) Comparative development of the mammalian yolk sac. In: Nogales FF (ed) The human yolk sac and yolk sac tumors. Springer, Berlin, pp 1–32

    Google Scholar 

  • Kojima T, Hinds LA, Muller WJ, O’Neill C, Tyndale-Biscoe CH (1993) Production and secretion of progesterone in vitro and presence of platelet activating factor (PAF) in early pregnancy of the marsupial, Macropus eugenii. Reprod Fertil Dev 5:15–25

    CAS  PubMed  Google Scholar 

  • Laird MK, Thompson MB, Murphy CR, McAllan BM (2014) Uterine epithelial cell changes during pregnancy in a marsupial (Sminthopsis crassicaudata; Dasyuridae). J Morphol 275:1081–1092

    PubMed  Google Scholar 

  • Laird MK, Dargan JR, Paterson L, Murphy CR, McAllan BM, Shaw G, Renfree MB, Thompson MB (2017a) Uterine molecular changes for non-invasive embryonic attachment in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae). Mol Reprod Dev 84:1076–1085

    CAS  PubMed  Google Scholar 

  • Laird MK, McShea H, McAllan BM, Murphy CR, Thompson MB (2017b) Uterine remodelling during pregnancy and pseudopregnancy in the brushtail possum (Trichosurus vulpecula; Phalangeridae). J Anat 231:84–94

    PubMed  PubMed Central  Google Scholar 

  • Laird MK, McShea H, Murphy CR, McAllan BM, Shaw G, Renfree MB, Thompson MB (2018) Non-invasive placentation in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae) involves redistribution of uterine Desmoglein-2. Mol Reprod Dev 85:72–82

    CAS  PubMed  Google Scholar 

  • Lawton BR, Carone BR, Obergfell CJ, Ferreri GC, Gondolphi CM, Vandeberg JL, Imumorin I, O'Neill RJ, O’Neill MJ (2008) Genomic imprinting of IGF2 in marsupials is methylation dependent. BMC Genomics 9:205

    PubMed  PubMed Central  Google Scholar 

  • Lefevre PL, Palin MF, Beaudry D, Dobias-Goff M, Desmarais JA, Llerena VE, Murphy BD (2011) Uterine signaling at the emergence of the embryo from obligate diapause. Am J Physiol Endocrinol Metab 300:E800–E808

    CAS  PubMed  Google Scholar 

  • Lloyd J, Brent R, Beckman D (1996) Sources of amino acids for protein synthesis during earlyorganogenesis in the rat. 3. Methionine incorporation. Placenta 17:629–634

    CAS  PubMed  Google Scholar 

  • Martin FC, Ang CS, Gardner DK, Renfree MB, Shaw G (2016) Uterine flushing proteome of the tammar wallaby after reactivation from diapause. Reproduction 152:491–505

    CAS  PubMed  Google Scholar 

  • Menzies BR, Pask AJ, Renfree MB (2011) Placental expression of pituitary hormones is an ancestral feature of therian mammals. Evodevo 2:16

    CAS  PubMed  PubMed Central  Google Scholar 

  • Menzies BR, Hildebrandt TB, Renfree MB (2020) Unique reproductive strategy in the swamp wallaby. Proc Natl Acad Sci U S A 117:5938–5942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merad Z, Wild AE (1992) The route of maternal IgM transport to the rabbit fetus. Placenta 13:291–304

    CAS  PubMed  Google Scholar 

  • Mossman HW (1937) Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Inst. Washington Publ. 479. Contrib Embryol 26:129–246

    Google Scholar 

  • Murphy BD, Fenelon J (2020) Models of embryonic diapause in Carnivora. Biosci Proc 10:85–100

    Google Scholar 

  • Murphy BD, Jewgenow K, Renfree MB, Ulbrich SE (2000) Introduction to pregnancy in waiting: embryonic diapause in mammals. Biosci Proc 10:1–4

    Google Scholar 

  • O’Neill MJ, Ingram RS, Vrana PB, Tilghman SM (2000) Allelic expression of IGF2 in marsupials and birds. Dev Genes Evol 210:18–20

    PubMed  Google Scholar 

  • Owen R (1834) On the generation of marsupial animals with a description of the impregnated uterus of the Kangaroo. Philos Trans R Soc Lond 124:333–364

    Google Scholar 

  • Padykula HA, Taylor JM (1976) Ultrastructural evidence for loss of the trophoblastic layer in the chorioallantoic placenta of Australian bandicoots (Marsupialia: Peramelidae). Anat Rec 186:357–385

    CAS  PubMed  Google Scholar 

  • Padykula HA, Taylor JM (1982) Marsupial placentation and its evolutionary significance. J Reprod Fertil Suppl 31:95–104

    CAS  PubMed  Google Scholar 

  • Palis J, Yoder MC (2001) Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 29:927–936

    CAS  PubMed  Google Scholar 

  • Parry LJ, Clark JM, Renfree MB (1997) Ultrastructural localization of relaxin in the corpus luteum of the pregnant and early lactating tammar wallaby, Macropus eugenii. Cell Tissue Res 290:615–622

    CAS  PubMed  Google Scholar 

  • Renfree MB (1972) Influence of the embryo on the marsupial uterus. Nature 240:475–477

    CAS  PubMed  Google Scholar 

  • Renfree MB (1973a) The composition of fetal fluids of the marsupial Macropus eugenii. Dev Biol 33:62–79

    CAS  PubMed  Google Scholar 

  • Renfree MB (1973b) Enzymes of intermediary metabolism in the fetal fluids of the tammar wallaby, Macropus eugenii. J Reprod Fertil 32:330–331

    CAS  PubMed  Google Scholar 

  • Renfree MB (1973c) Proteins in the uterine secretions of the marsupial Macropus eugenii. Dev Biol 32:41–49

    CAS  PubMed  Google Scholar 

  • Renfree MB (1983) Marsupial reproduction: the choice between placentation and lactation. In: Finn C (ed) Oxford reviews of reproductive biology. Oxford University Press, Oxford, pp 1–29

    Google Scholar 

  • Renfree MB (1993) Diapause, pregnancy, and parturition in Australian marsupials. J Exp Zool 266:450–462

    CAS  PubMed  Google Scholar 

  • Renfree MB (2010) Review: Marsupials: placental mammals with a difference. Placenta 31(Suppl):S21–S26

    PubMed  Google Scholar 

  • Renfree MB, Blanden DR (2000) Progesterone and oestrogen receptors in the female genital tract throughout pregnancy in tammar wallabies. J Reprod Fertil 119:121–128

    CAS  PubMed  Google Scholar 

  • Renfree MB, Fenelon JC (2017) The enigma of embryonic diapause. Development 144:3199–3210

    CAS  PubMed  Google Scholar 

  • Renfree MB, Heap RB (1977) Steroid metabolism by the placenta, corpus luteum, and endometrium of the marsupial Macropus eugenii. Theriogenology 8:164

    CAS  Google Scholar 

  • Renfree MB, McLaren A (1974) Foetal origin of transferrin in mouse amniotic fluid. Nature 252:159–161

    CAS  PubMed  Google Scholar 

  • Renfree MB (2000) Maternal recognition of pregnancy in marsupials. Rev Reprod 5:6–11

    CAS  PubMed  Google Scholar 

  • Renfree MB, Shaw G (2000) Diapause. Annu Rev Physiol 62:353–375

    CAS  PubMed  Google Scholar 

  • Renfree MB, Tyndale-Biscoe C (1973a) Transferrin variation between mother and fetus in the marsupial, Macropus eugenii. J Reprod Fertil 32:113–115

    CAS  PubMed  Google Scholar 

  • Renfree MB, Tyndale-Biscoe CH (1973b) Intrauterine development after diapause in the marsupial Macropus eugenii. Dev Biol 32:28–40

    CAS  PubMed  Google Scholar 

  • Renfree MB, Ager EI, Shaw G, Pask AJ (2008) Genomic imprinting in marsupial placentation. Reproduction 136:523–531

    CAS  PubMed  Google Scholar 

  • Renfree MB, Hore TA, Shaw G, Marshall Graves JA, Pask AJ (2009) Evolution of genomic imprinting: insights from marsupials and monotremes. Annu Rev Genomics Hum Genet 10:241–262

    CAS  PubMed  Google Scholar 

  • Renfree MB, Papenfuss AT, Deakin JE, Lindsay J, Heider T, Belov K, Rens W, Waters PD, Pharo EA, Shaw G (2011) Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 12:1–26

    Google Scholar 

  • Renfree MB, Suzuki S, Kaneko-Ishino T (2013) The origin and evolution of genomic imprinting and viviparity in mammals. Philos Trans R Soc Lond B Biol Sci 368:20120151

    PubMed  PubMed Central  Google Scholar 

  • Roberts CT, Breed WG (1994) Embryonic-maternal cell interactions at implantation in the fat-tailed dunnart, a dasyurid marsupial. Anat Rec 240:59–76

    CAS  PubMed  Google Scholar 

  • Shaw G (1983) Effect of PGF-2 alpha on uterine activity, and concentrations of 13, 14-dihydro-15-keto-PGF-2 alpha in peripheral plasma during parturition in the tammar wallaby (Macropus eugenii). J Reprod Fertil 69:429–436

    CAS  PubMed  Google Scholar 

  • Shaw G (1996) The uterine environment in early pregnancy in the tammar wallaby. Reprod Fertil Dev 8:811–818

    CAS  PubMed  Google Scholar 

  • Shaw G, Renfree MB (2001) Fetal control of parturition in marsupials. Reprod Fertil Dev 13:653–659

    CAS  PubMed  Google Scholar 

  • Shaw G, Rose RW (1979) Delayed gestation in the potoroo, Potorous tridactylus (Kerr). Austr J Zool 27:901–912

    Google Scholar 

  • Siddle HV, Deakin JE, Coggill P, Hart E, Cheng Y, Wong ES, Harrow J, Beck S, Belov K (2009) MHC-linked and un-linked class I genes in the wallaby. BMC Genomics 10:310

    PubMed  PubMed Central  Google Scholar 

  • Siddle HV, Marzec J, Cheng Y, Jones M, Belov K (2010) MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. Proc Biol Sci 277:2001–2006

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smits G, Mungall AJ, Griffiths-Jones S, Smith P, Beury D, Matthews L, Rogers J, Pask AJ, Shaw G, VandeBerg JL, McCarrey JR, Renfree MB, Reik W, Dunham I (2008) Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 40:971–976

    CAS  PubMed  Google Scholar 

  • Stringer JM, Suzuki S, Pask AJ, Shaw G, Renfree MB (2012a) Promoter-specific expression and imprint status of marsupial IGF2. PLoS One 7:e41690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stringer JM, Suzuki S, Pask AJ, Shaw G, Renfree MB (2012b) Selected imprinting of INS in the marsupial. Epigenetics Chromatin 5:14

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stringer JM, Pask AJ, Shaw G, Renfree MB (2014) Post-natal imprinting: evidence from marsupials. Heredity (Edinb) 113:145–155

    CAS  Google Scholar 

  • Suzuki S, Renfree MB, Pask AJ, Shaw G, Kobayashi S, Kohda T, Kaneko-Ishino T, Ishino F (2005) Genomic imprinting of IGF2, p57(KIP2) and PEG1/MEST in a marsupial, the tammar wallaby. Mech Dev 122:213–222

    CAS  PubMed  Google Scholar 

  • Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, Kohda T, Alsop AE, Marshall Graves JA, Kohara Y, Ishino F, Renfree MB, Kaneko-Ishino T (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3:e55

    PubMed  PubMed Central  Google Scholar 

  • Suzuki S, Shaw G, Kaneko-Ishino T, Ishino F, Renfree MB (2011) The evolution of mammalian genomic imprinting was accompanied by the acquisition of novel CpG islands. Genome Biol Evol 3:1276–1283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki S, Shaw G, Renfree MB (2018) Identification of a novel antisense noncoding RNA, ALID, transcribed from the putative imprinting control region of marsupial IGF2R. Epigenetics Chromatin 11:55

    PubMed  PubMed Central  Google Scholar 

  • Tyndale-Biscoe H, Renfree MB (1987) Reproductive physiology of marsupials. Cambridge University Press, Cambridge

    Google Scholar 

  • Walker MT, Hughes RL (1981) Ultrastructural changes after diapause in the uterine glands, corpus luteum and blastocyst of the red-necked wallaby, Macropus rufogriseus banksianus. J Reprod Fertil Suppl 29:151–158

    CAS  PubMed  Google Scholar 

  • Wallace GI (1981) Uterine factors and delayed implantation in macropodid marsupials. J Reprod Fertil Suppl 29:173–181

    CAS  PubMed  Google Scholar 

  • Whittington CM, Griffith OW, Qi W, Thompson MB, Wilson AB (2015) Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. Mol Biol Evol 32:3114–3131

    CAS  PubMed  Google Scholar 

  • Whittington CM, O’Meally D, Laird MK, Belov K, Thompson MB, McAllan BM (2018) Transcriptomic changes in the pre-implantation uterus highlight histotrophic nutrition of the developing marsupial embryo. Sci Rep 8:2412

    PubMed  PubMed Central  Google Scholar 

  • Young IR, Renfree MB (1979) The effects of corpus luteum removal during gestation on parturition in the tammar wallaby (Macorpus eugenii). J Reprod Fertil 56:249–254

    CAS  PubMed  Google Scholar 

  • Young IR, Renfree MB, Mesiano S, Shaw G, Jenkin G, Smith R (2011) The comparative physiology of parturition in mammals. In: Norris D, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 5: mammals. Elsevier, pp 95–116

    Google Scholar 

  • Zeller U, Freyer C (2002) Early ontogeny and placentation of the grey short-tailed opossum, Monodelphis domestica (Didelphidae: Marsupialia): contribution to the reconstruction of the marsupial morphotype. J Zool Syst Evol Res 39:137–158

    Google Scholar 

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Acknowledgments

We thank our many students and colleagues who have contributed to our new understanding of the marsupial placenta and all members of the Walgroup. We thank the late Dr Gordon Lyne for the bandicoot neonate images; Dr Stephen Frankenberg for the dunnart neonate images and Dr Brandon Menzies for the swamp wallaby neonate images.

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  1. School of BioSciences, The University of Melbourne, Melbourne, VIC, Australia

    Marilyn B. Renfree & Geoff Shaw

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  1. Marilyn B. Renfree
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Correspondence to Marilyn B. Renfree .

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Editors and Affiliations

  1. Division of Animal Sciences, University of Missouri, Columbia, MO, USA

    Prof. Rodney D. Geisert

  2. Division of Animal Sciences, University of Missouri, Columbia, MO, USA

    Prof. Thomas Spencer

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Renfree, M.B., Shaw, G. (2021). Placentation in Marsupials. In: Geisert, R.D., Spencer, T. (eds) Placentation in Mammals. Advances in Anatomy, Embryology and Cell Biology, vol 234. Springer, Cham. https://doi.org/10.1007/978-3-030-77360-1_4

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