The evolution of epitheliochorial placentation

Annual Review of Animal Biosciences

Volumn 1, Issue , 2013, Pages 443-467

  Carter, Anthony M ^a   Enders, Allen C ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

glucose transporters; macrophages; natural killer cells; placental hormones; regulatory T cells; uteroferrin

Indexed keywords

ANIMAL; EVOLUTION; FEMALE; GENETICS; MAMMAL; PHYSIOLOGY; PLACENTA; PREGNANCY;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; MAMMALS; PLACENTA; PREGNANCY;

EID: 84901504996     PISSN: 21658102     EISSN: 21658110     Source Type: Journal    
DOI: 10.1146/annurev-animal-031412-103653     Document Type: Article

References (134)

1. Mossman HW. 1987. Vertebrate Fetal Membranes. New Brunswick, NJ: Rutgers Univ. Press
2. Huxley TH. 1880. On the application of the laws of evolution to the arrangement of the Vertebrata, and more particularly of the Mammalia. Proc. Zool. Soc. Lond. 43:649-62
3. Wislocki GB. 1929. On the placentation of primates, with a consideration of the phylogeny of the placenta. Contrib. Embryol. 20:51-80
4. Vogel P. 2005. The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta 26:591-96
5. Prasad MR, Mossman HW, Scott GL. 1979. Morphogenesis of the fetal membranes of an American mole, Scalopus aquaticus. Am. J. Anat. 155:31-68
6. Carter AM, Enders AC. 2010. Placentation in mammals once grouped as insectivores. Int. J. Dev. Biol. 54:483-93
7. Ginther OJ. 1992. Reproductive Biology of the Mare. Cross Plains, WI: Equiservices. 2nd ed.
8. Carter AM 2007. Animal models of human placentation-a review. Placenta 28(Suppl. A): S41-47
9. Vasey N. 2007. The breeding system of wild red ruffed lemurs (Varecia rubra): A preliminary report. Primates 48:41-54
10. Martin RD. 2007. The evolution of human reproduction: A primatological perspective. Am. J. Phys. Anthropol. 134(Suppl. 45):59-84
11. Enders AC 2009. Reasons for diversity of placental structure. Placenta 30(Suppl. A):S15-18
12. Longo LD, Power GG, Forster RE. 1969. Placental diffusing capacity for carbon monoxide at varying partial pressures of oxygen. J. Appl. Physiol. 26:360-70
13. Wooding FB, Fowden AL. 2006. Nutrient transfer across the equine placenta: Correlation of structure and function. Equine Vet. J. 38:175-83
14. Longo LD, Ching KS. 1977. Placental diffusing capacity for carbon monoxide and oxygen in unanesthetized sheep. J. Appl. Physiol. 43:885-93
15. Bissonnette JM, Longo LD, Novy MJ, Murata Y, MartinCB Jr. 1979. Placental diffusing capacity and its relation to fetal growth. J. Dev. Physiol. 1:351-59
16. Hill EP, Power GG, Longo LD. 1973. A mathematical model of carbon dioxide transfer in the placenta and its interaction with oxygen. Am. J. Physiol. 224:283-99
17. Barcroft J, Kennedy JA, Mason MF. 1939. The direct determination of the oxygen consumption of the foetal sheep. J. Physiol. 95:269-75
18. Young M. 1992. Classics revisited: Researches on pre-natal life by Sir Joseph Barcroft. Placenta 13:607-12
19. Meschia G, Cotter JR, Breathnach CS, Barron DH. 1965. The hemoglobin, oxygen, carbon dioxide and hydrogen ion concentrations in the umbilical bloods of sheep and goats as sampled via indwelling plastic catheters. Q. J. Exp. Physiol. Cogn. Med. Sci. 50:185-95
20. Longo LD. 1987. Respiratory gas exchange in the placenta. In Handbook of Physiology. Section 3: The Respiratory System. Volume 4: Gas Exchange, ed. LE Farhi, SM Tenney, pp.351-401. Bethesda, MD: Am. Physiol. Soc.
21. Carter AM. 1989. Factors affecting gas transfer across the placenta and the oxygen supply to the fetus. J. Dev. Physiol. 12:305-22
22. Wilkening RB, Meschia G. 1992. Current topic: Comparative physiology of placental oxygen transport. Placenta 13:1-15
23. Llanos AJ, Riquelme RA, Sanhueza EM, Hanson MA, Blanco CE, et al. 2003. The fetal llama versus the fetal sheep: Different strategies to withstand hypoxia. High Alt. Med. Biol. 4:193-202
24. Llanos AJ, Ebensperger G, Herrera EA, Reyes RV, PulgarVM,et al. 2011. Fetal and postnatal pulmonary circulation in the Alto Andino. Placenta 32(Suppl. 2):S100-3
25. Comline RS, Silver M. 1974. A comparative study of blood gas tensions, oxygen affinity and red cell 2,3 DPG concentrations in foetal and maternal blood in the mare, cow and sow. J. Physiol. 242:805-26
26. Fowden AL, Forhead AJ, White KL, Taylor PM. 2000. Equine uteroplacental metabolism at mid-and late gestation. Exp. Physiol. 85:539-45
27. Comline RS, Silver M. 1976. Some aspects of foetal and uteroplacental metabolism in cows with indwelling umbilical and uterine vascular catheters. J. Physiol. 260:571-86
28. Reynolds LP, Ferrell CL, Ford SP. 1985. Transplacental diffusion and blood flow of gravid bovine uterus. Am. J. Physiol. 249:R539-43
29. Ferrell CL. 1991. Maternal and fetal influences on uterine and conceptus development in the cow: II. Blood flow and nutrient flux. J. Anim. Sci. 69:1954-65
30. Reynolds LP, Ford SP, Ferrell CL. 1985. Blood flow and steroid and nutrient uptake of the gravid uterus and fetus of sows. J. Anim. Sci. 61:968-74
31. Turner W. 1876. On the placentation of the lemurs. Philos. Trans. R. Soc. Lond. B Biol. Sci. 166:569-87
32. King BF. 1984. The fine structure of the placenta and chorionic vesicles of the bush baby, Galago crassicaudata. Am. J. Anat. 169:101-16
33. Njogu A, Owiti GO, Persson E, Oduor-Okelo D. 2006. Ultrastructure of the chorioallantoic placenta and chorionic vesicles of the lesser bush baby (Galago senegalensis). Placenta 27:771-79
34. Wooding FB, Burton GJ. 2008. Comparative Placentation: Structures, Functions And Evolution. Heidelberg: Springer-Verlag
35. Klisch K, Mess A. 2007. Evolutionary differentiation of Cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta 28:353-60
36. Baur R. 1977. Morphometry of the placental exchange area. Adv. Anat. Embryol. Cell Biol. 53:3-65
37. Martin RD. 2008. Evolution of placentation in primates: Implications of mammalian phylogeny. Evol. Biol. 35:125-45
38. Reng R. 1977. Die Placenta von Microcebus murinus Miller. Z. Saugetierkd. 42:201-14
39. Battaglia FC, Meschia G. 1978. Principal substrates of fetal metabolism. Physiol. Rev. 58:499-527
40. Regnault TRH, de Vrijer B, Battaglia FC. 2002. Transport and metabolism of amino acids in placenta. Endocrine 19:23-41
41. Hay WW Jr. 2006. Placental-fetal glucose exchange and fetal glucose metabolism. Trans. Am. Clin. Climatol. Assoc. 117:321-39
42. Wooding FB, Fowden AL, Bell AW, Ehrhardt RA, Limesand SW, Hay WW. 2005. Localisation of glucose transport in the ruminant placenta: Implications for sequential use of transporter isoforms. Placenta 26:626-40
43. Wooding FB, Morgan G, Fowden AL, Allen WR. 2000. Separate sites and mechanisms for placental transport of calcium, iron and glucose in the equine placenta. Placenta 21:635-45
44. Enders AC, Carter AM. 2006. Comparative placentation: Some interesting modifications for histotrophic nutrition-a review. Placenta 27(Suppl. A):S11-16
45. Mahaboob Basha SM, Bazer FW, Roberts RM. 1979. The secretion of a uterine specific, purple phosphatase by cultured explants of porcine endometrium: Dependency upon the state of pregnancy of the donor animal. Biol. Reprod. 20:431-41
46. Renegar RH, Bazer FW, Roberts RM. 1982. Placental transport and distribution of uteroferrin in the fetal pig. Biol. Reprod. 27:1247-60
47. Nuttleman PR, Roberts RM. 1990. Transfer of iron from uteroferrin (purple acid phosphatase) to transferrin related to acid phosphatase activity. J. Biol. Chem. 265:12192-99
48. Ellenberger C, Wilsher S, Allen WR, Hoffmann C, Kolling M, et al. 2008. Immunolocalisation of the uterine secretory proteins uterocalin, uteroferrin and uteroglobin in the mare's uterus and placenta throughout pregnancy. Theriogenology 70:746-57
49. Padua MB, Lynch VJ, Alvarez NV, Garthwaite MA, Golos TG, et al. 2012. ACP5 (Uteroferrin): Phylogeny of an ancient and conserved gene expressed in the endometrium of mammals. Biol. Reprod. 86:1-8
50. Vallet JL, Fahrenkrug SC. 2000. Structure of the gene for uteroferrin. DNA Cell Biol. 19:689-96
51. McDowell KJ, Sharp DC, Grubaugh W. 1987. Comparison of progesterone and progesterone \+ oestrogen on total and specific uterine proteins in pony mares. J. Reprod. Fertil. Suppl. 35:335-42
52. Simmen RC, Simmen FA, Bazer FW. 1991. Regulation of synthesis of uterine secretory proteins: Evidence for differential induction of porcine uteroferrin and antileukoproteinase gene expression. Biol. Reprod. 44:191-200
53. Fazleabas AT, Bazer FW, Hansen PJ, Geisert RD, Roberts RM. 1985. Differential patterns of secretory protein localization within the pig uterine endometrium. Endocrinology 116:240-45
54. Burton GJ. 1982. Review article. Placental uptake of maternal erythrocytes: A comparative study. Placenta 3:407-34
55. Hill JP, Ince FE, Rau AS. 1928. The development of the foetal membranes in Loris, with special reference to the mode of vascularisation of the chorion in the Lemuroidea and its phylogenetic significance. Proc. Zool. Soc. Lond. 98:699-716
56. Guillomot M, Michel C, Gaye P, Charlier N, Trojan J, Martal J. 1990. Cellular localization of an embryonic interferon, ovine trophoblastin and its mRNA in sheep embryos during early pregnancy. Biol. Cell 68:205-11
57. Noel S, Herman A, Johnson GA, Gray CA, Stewart MD,et al. 2003. Ovine placental lactogen specifically binds to endometrial glands of the ovine uterus. Biol. Reprod. 68:772-80
58. Han CS, Mathialagan N, Klemann SW, Roberts RM. 1997. Molecular cloning of ovine and bovine type I interferon receptor subunits from uteri, and endometrial expression of messenger ribonucleic acid for ovine receptors during the estrous cycle and pregnancy. Endocrinology 138: 4757-67
59. Roberts RM, Liu L, Guo Q, Leaman D, Bixby J. 1998. The evolution of the type I interferons. J. Interferon Cytokine Res. 18:805-16
60. Leaman DW, Roberts RM. 1992. Genes for the trophoblast interferons in sheep, goat, and musk ox and distribution of related genes among mammals. J. Interferon Res. 12:1-11
61. Enders AC, Liu IK. 1991. Trophoblast-uterine interactions during equine chorionic girdle cell maturation, migration, and transformation. Am. J. Anat. 192:366-81
62. Allen WR, Hamilton DW, Moor RM. 1973. The origin of equine endometrial cups. II. Invasion of the endometrium by trophoblast. Anat. Rec. 177:485-501
63. Sherman GB, Lund LA, Bunick D, Winn RJ. 1997. Characterization and phylogenetic significance of rhinoceros luteinizing hormone beta (LHb) subunit messenger RNA structure, complementary DNA sequence and gene copy number. Gene 195:131-39
64. Forsyth IA, Wallis M. 2002. Growth hormone and prolactin-molecular and functional evolution. J. Mammary Gland Biol. Neoplasia 7:291-312
65. Larson JH, Kumar CG, Everts RE, Green CA, Everts-van der Wind A, et al. 2006. Discovery of eight novel divergent homologs expressed in cattle placenta. Physiol. Genomics 25:405-13
66. Kessler MA, Schuler LA. 1997. Purification and properties of placental prolactin-related protein-I. Placenta 18:29-36
67. Kappes SM,Warren WC, Pratt SL, Liang R, Anthony RV. 1992. Quantification and cellular localization of ovine placental lactogen messenger ribonucleic acid expression during mid-and late gestation. Endocrinology 131:2829-38
68. Sakal E, Bignon C, Chapnik-Cohen N, Daniel N, Paly J, et al. 1998. Cloning, preparation and characterization of biologically active recombinant caprine placental lactogen. J. Endocrinol. 159: 509-18
69. Ushizawa K, Takahashi T, Hosoe M, Ohkoshi K, Hashizume K. 2007. Expression and characterization of novel ovine orthologs of bovine placental prolactin-related proteins. BMC Mol. Biol. 8:95
70. Ushizawa K, Takahashi T, Hosoe M, Kizaki K, Abe Y, et al. 2007. Gene expression profiles of novel caprine placental prolactin-related proteins similar to bovine placental prolactin-related proteins. BMC Dev. Biol. 7:16
71. Wooding FB, Morgan G, Forsyth IA, Butcher G, Hutchings A, et al. 1992. Light and electron microscopic studies of cellular localization of oPL with monoclonal and polyclonal antibodies. J. Histochem. Cytochem. 40:1001-9
72. Buttle HL. 1978. The maintenance of pregnancy in hypophysectomized goats. J. Reprod. Fertil. 52:255-60
73. Gluckman PD, Kaplan SL, Rudolph AM, Grumbach MM. 1979. Hormone ontogeny in the ovine fetus. II. Ovine chorionic somatomammotropin in mid-and late gestation in the fetal and maternal circulations. Endocrinology 104:1828-33
74. Schoknecht PA, Nobrega SN, Petterson JA, Ehrhardt RA, Slepetis R, Bell AW. 1991. Relations between maternal and fetal plasma concentrations of placental lactogen and placental and fetal weights in well-fed ewes. J. Anim. Sci. 69:1059-63
75. Herman A, Helman D, Livnah O, Gertler A. 1999. Ruminant placental lactogens act as antagonists to homologous growth hormone receptors and as agonists to human or rabbit growth hormone receptors. J. Biol. Chem. 274:7631-39
76. Haig D 2008. Placental growth hormone-related proteins and prolactin-related proteins. Placenta 29(Suppl. A):S36-41
77. Kimura J, SasakiM, Endo H, Fukuta K. 2004. Anatomical and histological characterization of the female reproductive organs of mouse deer (Tragulidae). Placenta 25:705-11
78. Wooding FB, Kimura J, Fukuta K, Forhead AJ. 2007. A light and electron microscopical study of the Tragulid (mouse deer) placenta. Placenta 28:1039-48
79. Wallis OC, Mac-Kwashie AO, Makri G, Wallis M. 2005. Molecular evolution of prolactin in primates. J. Mol. Evol. 60:606-14
80. Wallis M, Lioupis A, Wallis OC. 1998. Duplicate growth hormone genes in sheep and goat. J. Mol. Endocrinol. 21:1-5
81. Gootwine E. 2004. Placental hormones and fetal-placental development. Anim. Reprod. Sci. 82-83: 551-66
82. Papper Z, Jameson NM, Romero R, Weckle AL, Mittal P, et al. 2009. Ancient origin of placental expression in the growth hormone genes of anthropoid primates. Proc. Natl. Acad. Sci. USA 106:17083-88
83. Wallis OC, Zhang Y-P, Wallis M. 2001. Molecular evolution of GHin primates: Characterisation of the GH genes from slow loris and marmoset defines an episode of rapid evolutionary change. J. Mol. Endocrinol. 26:249-58
84. Adkins RM, Nekrutenko A, Li WH. 2001. Bushbaby growth hormone is much more similar to nonprimate growth hormones than to rhesus monkey and human growth hormones. Mol. Biol. Evol. 18:55-60
85. Hughes AL, Green JA, Garbayo JM, Roberts RM. 2000. Adaptive diversification within a large family of recently duplicated, placentally expressed genes. Proc. Natl. Acad. Sci. USA 97:3319-23
86. Szafranska B, Panasiewicz G, Majewska M. 2006. Biodiversity of multiple Pregnancy-Associated Glycoprotein (PAG) family: Gene cloning and chorionic protein purification in domestic and wild eutherians (Placentalia)-a review. Reprod. Nutr. Dev. 46:481-502
87. Telugu BP, Walker AM, Green JA. 2009. Characterization of the bovine pregnancy-associated glycoprotein gene family-analysis of gene sequences, regulatory regions within the promoter and expression of selected genes. BMC Genomics 10:185
88. Wooding FB, Roberts RM, Green JA. 2005. Light and electron microscope immunocytochemical studies of the distribution of pregnancy associated glycoproteins (PAGs) throughout pregnancy in the cow: Possible functional implications. Placenta 26:807-27
89. Leiser R, Pfarrer C, Abd-Elnaeim M, Dantzer V. 1998. Feto-maternal anchorage in epitheliochorial and endotheliochorial placental types studied by histology and microvascular corrosion casts. In The Maternal Fetal Interface, ed. AM Carter, V Dantzer, T Jansson, pp. 21-39. Rochester, NY: Univ. Rochester Press
90. Challis JRG, Matthews SG, Gibb W, Lye SJ. 2000. Endocrine and paracrine regulation of birth at term and preterm. Endocr. Rev. 21:514-50
91. Jurke MH, Czekala NM, Jurke S, Hagey LR, Lance VA, et al. 1998. Monitoring pregnancy in twinning pygmy loris (Nycticebus pygmaeus) using fecal estrogen metabolites. Am. J. Primatol. 46:173-83
92. Shideler SE, Czekala NM, Benirschke K, Lasley BL. 1983. Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biol. Reprod. 28:963-69
93. HoltanDW,Houghton E, SilverM,Fowden AL, Ousey J, Rossdale PD. 1991. Plasma progestagens in the mare, fetus and newborn foal. J. Reprod. Fertil. Suppl. 44:517-28
94. Ousey JC, Forhead AJ, Rossdale PD, Grainger L, Houghton E, Fowden AL. 2003. Ontogeny of uteroplacental progestagen production in pregnant mares during the second half of gestation. Biol. Reprod. 69:540-48
95. Fowden AL, Forhead AJ, Ousey JC. 2008. The endocrinology of equine parturition. Exp. Clin. Endocrinol. Diabetes 116:393-403
96. Hodges JK, van Aarde RJ, HeistermannM, Hoppen HO. 1994. Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana). J. Reprod. Fertil. 102:163-68
97. Meyer HH, Jewgenow K, Hodges JK. 1997. Binding activity of 5a-reduced gestagens to the progestin receptor from African elephant (Loxodonta africana). Gen. Comp. Endocrinol. 105:164-67
98. AllenWR.2006. Ovulation, pregnancy, placentation and husbandry in the African elephant (Loxodonta africana). Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:821-34
99. MoffettA,Loke C. 2006. Immunologyofplacentation in eutherianmammals. Nat. Rev. Immunol. 6:584-94
100. Hansen PJ. 2011. The immunology of early pregnancy in farm animals. Reprod. Domest. Anim. 46(Suppl. 3):18-30
101. Meeusen E, Fox A, Brandon M, Lee CS. 1993. Activation of uterine intraepithelial gd T cell receptorpositive lymphocytes during pregnancy. Eur. J. Immunol. 23:1112-17
102. Fox A, Maddox JF, de Veer MJ, Meeusen EN. 2010. gdTCR\+ cells of the pregnant ovine uterus express variable T cell receptors and contain granulysin. J. Reprod. Immunol. 84:52-56
103. Fox A, Meeusen E. 1999. Sheep perforin: Identification and expression by gd T cells from pregnant sheep uterine epithelium. Vet. Immunol. Immunopathol. 68:293-96
104. Nasar A, Rahman A, Meeusen EN, Lee CS. 2002. Peri-partum changes in the intraepithelial lymphocyte population of sheep interplacentomal endometrium. Am. J. Reprod. Immunol. 47:132-41
105. Lee CS, Meeusen E, Gogolin-Ewens K, Brandon MR. 1992. Quantitative and qualitative changes in the intraepithelial lymphocyte population in the uterus of nonpregnant and pregnant sheep. Am. J. Reprod. Immunol. 28:90-96
106. Lee CS, Wooding FB, Morgan G. 1997. Quantitative analysis throughout pregnancy of intraepithelial large granular and non-granular lymphocyte distributions in the synepitheliochorial placenta of the cow. Placenta 18:675-81
107. Oliveira LJ, Hansen PJ. 2009. Phenotypic characterization of macrophages in the endometrium of the pregnant cow. Am. J. Reprod. Immunol. 62:418-26
108. Oliveira LJ, McClellan S, Hansen PJ. 2010. Differentiation of the endometrial macrophage during pregnancy in the cow. PLoS ONE 5:e13213
109. Bainbridge DR, Sargent IL, Ellis SA. 2001. Increased expression of major histocompatibility complex (MHC) class I transplantation antigens in bovine trophoblast cells before fusion with maternal cells. Reproduction 122:907-13
110. Walker CG, LittlejohnMD,MitchellMD,Roche JR, Meier S. 2012. Endometrial gene expression during early pregnancy differs between fertile and subfertile dairy cow strains. Physiol. Genomics 44:47-58
111. Maher JK, Tresnan DB, Deacon S, Hannah L, Antczak DF. 1996. Analysis of MHC class I expression in equine trophoblast cells using in situ hybridization. Placenta 17:351-59
112. Noronha LE, Antczak DF. 2010. Maternal immune responses to trophoblast: The contribution of the horse to pregnancy immunology. Am. J. Reprod. Immunol. 64:231-44
113. Grunig G, Triplett L, Canady LK, Allen WR, Antczak DF. 1995. The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells. Placenta 16:539-59
114. de Mestre A, Noronha L, Wagner B, Antczak DF. 2010. Split immunological tolerance to trophoblast. Int. J. Dev. Biol. 54:445-55
115. Noronha LE, Huggler KE, de Mestre AM, Miller DC, Antczak DF. 2012. Molecular evidence for natural killer-like cells in equine endometrial cups. Placenta 33:379-86
116. de Mestre AM, Hanlon D, Adams AP, Runcan E, Leadbeater JC, et al. 2011. Functions of ectopically transplanted invasive horse trophoblast. Reproduction 141:849-56
117. Adams AP, Oriol JG, Campbell RE, Oppenheim YC, Allen WR, Antczak DF. 2007. The effect of skin allografting on the equine endometrial cup reaction. Theriogenology 68:237-47
118. Kammerer R, Zimmermann W. 2010. Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol. 8:12.
119. Gérard P. 1932. Etudes sur l'ovogenèse chez les lémuriens du genre Galago. Arch. Biol. (Liege) 43:93-151
120. Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, et al. 2010. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120:4102-10
121. Older Aguilar AM, Guethlein LA, Adams EJ, Abi-Rached L, Moesta AK, Parham P. 2010. Coevolution of killer cell Ig-like receptors with HLA-C to become the major variable regulators of human NK cells. J. Immunol. 185:4238-51
122. Averdam A, Petersen B, Rosner C, Neff J, Roos C, et al. 2009. A novel system of polymorphic and diverse NK cell receptors in primates. PLoS Genet. 5:e1000688.
123. Engelhardt H, King GJ. 1996. Uterine natural killer cells in species with epitheliochorial placentation. Nat. Immun. 15:53-69
124. Gendzekhadze K, Norman PJ, Abi-Rached L, Graef T, Moesta AK, et al. 2009. Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands. Proc. Natl. Acad. Sci. USA 106:18692-97
125. Mossman HW. 1939. The epitheliochorial placenta of an American mole, Scalopus aquaticus. Proc. Zool. Soc. Lond. 109:373-75
126. Carter AM. 2005. Placentation in an American mole, Scalopus aquaticus. Placenta 26:597-600
127. Prasad MR. 1958. Morphogenesis of the Fetal Membranes of the American Moles Scalopus aquaticus, Scapanus latimanus and Parascalops breweri. Madison: Univ. Wis.-Madison
128. Malassine A, Frendo JL, Evain-Brion D. 2003. A comparison of placental development and endocrine functions between the human and mouse model. Hum. Reprod. Update 9:531-39
129. Siniza S, Lupiañez DG, Jiménez R, Zeller U. 2012. Morphology and ultrastructure of the chorioallantoic placenta of the Iberian mole (Talpa occidentalis) with special reference to heterophagous areolas and the nature of the interhaemal barrier. J. Anat. 221:164-73
130. Conway MS. 2009. The predictability of evolution: Glimpses into a post-Darwinian world. Naturwissenschaften 96:1313-37
131. Castoe TA, de Koning AP, Pollock DD. 2010. Adaptive molecular convergence: Molecular evolution versus molecular phylogenetics. Commun. Integr. Biol. 3:67-69
132. Brambell FW. 1969. The transmission of immune globulins from the mother to the foetal and newborn young. Proc. Nutr. Soc. 28:35-41
133. Marsh H, Heinsohn GE, Channells PW. 1984. Changes in the ovaries and uterus of the dugong, Dugong dugon (Sirenia:Dugongidae), with age and reproductive activity. Aust. J. Zool. 32:743-66
134. Strahl H. 1906. Die Embryonalhüllen der Säuger und die Placenta. In Hertwigs Handbuch der Vergleichenden und Experimentellen Entwicklungslehre der Wirbeltiere, ed. O Hertig, pp. 235-368. Jena, Ger.: G. Fischer