Evolution of the placenta during the early radiation of placental mammals

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 148, Issue 4, 2007, Pages 769-779

  Mess, Andrea ^a   Carter, Anthony M ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Chorioallantoic placenta; Endotheliochorial placenta; Epitheliochorial placenta; Fetal membranes; Gas exchange; Haemochorial placenta; Phylogenetics; Placentalia

Indexed keywords

BAT; EDENTATA; FETUS MEMBRANE; GAS EXCHANGE; NONHUMAN; PHYLOGENY; PLACENTA; PLACENTA FUNCTION; REVIEW;

EUTHERIA;

EID: 34447636502     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2007.01.029     Document Type: Review

References (85)

1. Amoroso E.C. Placentation. In: Parkers A.S. (Ed). Marshall's Physiology of Reproduction vol. II (1952), Longmans, London 127-311
2. Archibald J.D. Timing and biogeography of the eutherian radiation: fossils and molecules compared. Mol. Phylogenet. Evol. 28 (2003) 350-359
3. Badwaik N.K., and Rasweiler J.J. Pregnancy. In: Crichton E.G., and Krutzsch P.H. (Eds). Reproductive Biology of Bats (2000), Academic Press, New York 221-293
4. Baur R. Morphometric data and questions concerning placental transfer. Placenta Suppl. 2 (1981) 35-44
5. Becher H. Placenta und Uterusschleimhaut von Tamandua tetradactyla (Myrmecophaga). Gegenbaurs Morphol. Jahrb. 67 (1931) 381-458
6. Beck F. Comparative placental morphology and function. Environ. Health Perspect. 18 (1976) 5-12
7. Beck R.M.D., Bininda-Emonds O.R.P., Cardillo M., Liu F.-G.R., and Purvis A. A higher-level MRP supertree of placental mammals. Evol. Biol. 6 (2006) 93
8. Benirschke K., and Powell H.C. On the placentation of sloths. In: Montgomery G.G. (Ed). The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas (1985), Smithsonian Institution Press, Washington 237-241
9. Blackburn D.G. Chorioallantoic placentation in squamate reptiles: structure, function, development, and evolution. J. Exp. Zool. 266 (1993) 414-430
10. Burton G.J. Placental uptake of maternal erythrocytes: a comparative study. Placenta 3 (1982) 407-434
11. Carter A.M. Factors affecting gas transfer across the placenta and the oxygen supply to the fetus. J. Dev. Physiol. 12 (1989) 305-322
12. Carter A.M. Placental oxygen transfer and the oxygen supply to the fetus. Fetal Matern. Med. Rev. 11 (1999) 151-161
13. Carter A.M. Placental oxygen consumption. Part I: in vivo studies-a review. Placenta 21 Suppl. A (2000) 31-37
14. Carter A.M., and Enders A.C. Comparative aspects of trophoblast development and placentation. Reprod. Biol. Endocrinol. 2 (2004) 46
15. Carter A.M., and Mess A. Evolution of the placenta in eutherian mammals. Placenta (2007) (Electronic publication ahead of print, June 14, 2006)
16. Carter A.M., Enders A.C., Kunzle H., Oduor-Okelo D., and Vogel P. Placentation in species of phylogenetic importance: the Afrotheria. Anim. Reprod. Sci. 82-83 (2004) 35-48
17. Carter A.M., Enders A.C., Miglino M.A., and da Silva V.M.F. Placentation in the Amazonian manatee, Trichechus inunguis. Placenta 26 (2005) A15
18. Carter A.M., Blankenship T.N., Enders A.C., and Vogel P. The fetal membranes of the otter shrews and a synapomorphy for Afrotheria. Placenta 27 (2006) 258-268
19. Carter, A.M., Enders, A.C., Jones, C.J.P., Mess, A., Pfarrer, C., Pijnenborg, R., Soma, H., 2006b. Comparative placentation and animal models: patterns of trophoblast invasion - a workshop report. Placenta 27, Suppl. A, 20, S30-S33.
20. Clementi M.E., Scatena R., Mordente A., Condo S.G., Castagnola M., and Giardina B. Oxygen transport by fetal bovine hemoglobin. J. Mol. Biol. 12 (1996) 229-234
21. Crespi B.J., and Semeniuk C. Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am. Nat. 163 (2004) 635-653
22. Delsuc F., Scally M., Madsen O., Stanhope M.J., de Jong W.W., Catzeflis F.M., Springer M.S., and Douzery E.J. Molecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Mol. Biol. Evol. 19 (2002) 1656-1671
23. Delsuc F., Vizcaino S.F., and Douzery E.J. Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evol. Biol. 4 (2004) 11
24. Douady C.J., Chatelier P.I., Madsen O., de Jong W.W., Catzeflis F., Springer M.S., and Stanhope M.J. Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews. Mol. Phylogenet. Evol. 25 (2002) 200-209
25. Elliot M.G., and Crespi B.J. Placental invasiveness mediates the evolution of hybrid inviability in mammals. Am. Nat. 168 (2006) 114-120
26. Enders A.C. Electron microscopic observations on the villous hemochorial placenta of the nine-banded armadillo (Dasypus novemcinctus). J. Anat. 94 (1960) 205
27. Enders A.C., and Carter A.M. Comparative placentation: some interesting modifications for histotrophic nutrition-a review. Placenta 27 Suppl. A (2006) S11-S16
28. Enders A.C., Blankenship T.N., Lantz K.C., and Enders S.S. Morphological variation in the interhemal areas of chorioallantoic placentae - a review. In: Carter A.M., Dantzer V., and Jansson T. (Eds). The Maternal Fetal Interface. Trophoblast Research vol. 12 (1998) 1-19
29. Enders, A.C., Blankenship, T.N., Goodman, S.M., Soarimalala, V., Carter, A.M., (in press). 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. [Electronic publication ahead of print, November 16, 2006].
30. Falkowski P.G., Katz M.E., Milligan A.J., Fennel K., Cramer B.S., Aubry M.P., Berner R.A., Novacek M.J., and Zapol W.M. The rise of oxygen over the past 205 million years and the evolution of large placental mammals. Science 309 (2005) 2202-2204
31. Freyer C., Zeller U., and Renfree M.B. The marsupial placenta: a phylogenetic analysis. J. Exp. Zool., A Comp. Exp. Biol. 299 (2003) 59-77
32. Gaudin T.J., Wible J.R., Hopson J.A., and Turnbull W.D. Reexamination of the morphological evidence for the Cohort Epitheria (Mammalia, Eutheria). J. Mamm. Evol. 3 (1996) 31-79
33. Gingerich P.D. Cetacea. In: Rose K.D., and Archibald J.D. (Eds). The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades (2005), Johns Hopkins University Press, Baltimore 234-252
34. Grosser O. Vergleichende Anatomie und Entwicklungsgeschichte der Eihäute und der Placenta (1909), W. Braumüller, Vienna
35. Haig D. Genetic conflicts in human pregnancy. Q. Rev. Biol. 68 (1993) 495-532
36. Hamlett W.C. Evolution and morphogenesis of the placenta in sharks. J. Exp. Zool. 252 (1989) 35-52
37. Hunter J.P., and Janis C.M. Spiny Norman in the Garden of Eden? Dispersal and early biogeography of Placentalia. J. Mamm. Evol. 13 (2006) 89-123
38. Jelkmann W., and Bauer C. Embryonic hemoglobins: dependency of functional characteristics on tetramer composition. Pflugers Arch. 377 (1978) 75-80
39. Ji Q., Luo Z.X., Yuan C.X., Wible J.R., Zhang J.P., and Georgi J.A. The earliest known eutherian mammal. Nature 416 (2002) 816-822
40. Johnson R.M., Buck S., Chiu C.H., Gage D.A., Shen T.L., Hendrickx A.G., Gumucio D.L., and Goodman M. Humans and old world monkeys have similar patterns of fetal globin expression. J. Exp. Zool. 288 (2000) 318-326
41. King B.F., Pinheiro P.B., and Hunter R.L. The fine structure of the placental labyrinth in the sloth, Bradypus tridactylus. Anat. Rec. 202 (1982) 15-22
42. Klisch K., and Mess A. Evolutionary differentiation of cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta (2007) [Epub ahead of print, May 17, 2006]
43. Kriegs J.O., Churakov G., Kiefmann M., Jordan U., Brosius J., and Schmitz J. Retroposed elements as archives for the evolutionary history of placental mammals. PLoS Biol. 4 (2006) e91
44. Lillegraven J.E. Polarities in mammalian evolution seen through homologs of the inner cell mass. J. Mamm. Evol. 10 (2003) 277-333
45. Lombardi J., and Wourms J.P. The trophotaenial placenta of a viviparous goodeid fish. III: protein uptake by trophotaeniae, the embryonic component. J. Exp. Zool. 236 (1985) 165-179
46. Longo L.D. Respiratory gas exchange in the placenta. In: Farhi L.E., and Tenney S.M. (Eds). Handbook of Physiology, Section 3. The Respiratory System, Gas Exchange vol. 4 (1987), American Physiological Society, Bethesda 351-401
47. Luo Z.X., Ji Q., Wible J.R., and Yuan C.X. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302 (2003) 1934-1940
48. Maddison W.P., and Maddison D.R. MacClade 4: Analysis of Phylogeny and Character Evolution (2000), Sinauer, Sunderland, MA
49. Madsen O., Scally M., Douady C.J., Kao D.J., DeBry R.W., Adkins R., Amrine H.M., Stanhope M.J., de Jong W.W., and Springer M.S. Parallel adaptive radiations in two major clades of placental mammals. Nature 409 (2001) 610-614
50. Malassine A., Frendo J.L., and Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum. Reprod. Updat. 9 (2003) 531-539
51. Martin R.D. Human reproduction: a comparative background for medical hypotheses. J. Reprod. Immunol. 59 (2003) 111-135
52. Maston G.A., and Ruvolo M. Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol. Biol. Evol. 19 (2002) 320-335
53. Mayhew T.M. Stereology and the placenta: where's the point? - a review. Placenta 27 Suppl. A (2006) S17-S25
54. McKenna M.C., and Bell S.K. Classification of Mammals Above the Species Level (1997), Columbia University Press, New York
55. Mess A. Evolutionary transformations of chorioallantoic placental characters in Rodentia with special reference to hystricognath species. J. Exp. Zool., A Comp. Exp. Biol. 299 (2003) 78-98
56. Mess A., and Carter A.M. Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. J. Exp. Zool., B Mol. Dev. Evol. 306 (2006) 140-163
57. Mess A., Blackburn D.G., and Zeller U. Evolutionary transformations of fetal membranes and reproductive strategies. J. Exp. Zool., A Comp. Exp. Biol. 299 (2003) 3-12
58. Moffett A., and Loke C. Immunology of placentation in eutherian mammals. Nat. Rev., Immunol. 6 (2006) 584-594
59. Mossman H.W. The principal exchange vessels of the chorioallantoic placenta of mammals. In: DeHaan R.L., and Ursprung H. (Eds). Organogenesis (1965), Holt, Rhinehart and Winston, New York 771-786
60. Mossman H.W. Vertebrate Fetal Membranes: Comparative Ontogeny and Morphology; Evolution; Phylogenetic Significance; Basic Functions; Research Opportunities (1987), Macmillan, Houndmills
61. Murphy W.J., Eizirik E., Johnson W.E., Zhang Y.P., Ryder O.A., and O'Brien S.J. Molecular phylogenetics and the origin of placental mammals. Nature 409 (2001) 614-618
62. Murphy W.J., Eizirik E., O'Brien S.J., Madsen O., Scally M., Douady C.J., Teeling E., Ryder O.A., Stanhope M.J., de Jong W.W., and Springer M.S. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294 (2001) 2348-2351
63. Oduor-Okelo D., Musewe V.O., and Gombe S. Electron microscopic study of the chorioallantoic placenta of the rock hyrax (Heterohyrax brucei). J. Reprod. Fertil. 68 (1983) 311-316
64. Portmann A. Die Ontogenese der Säugetiere als Evolutionsproblem. Biomorphosis 1 (1938) 49-66
65. Price S.A., Bininda-Emonds O.R.P., and Gittleman J.L. A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biol. Rev. 80 (2005) 445-473
66. Prychitko T., Johnson R.M., Wildman D.E., Gumucio D., and Goodman M. The phylogenetic history of New World monkey beta globin reveals a platyrrhine beta to delta gene conversion in the atelid ancestry. Mol. Phylogenet. Evol. 35 (2005) 225-234
67. Sánchez-Villagra M.R., Narita Y., and Kuratani S. Thoracolumbar vertebral number in mammals and a potential morphological synapomorphy for Afrotheria. Systematics and Biodiversity 5 (2007) 1-7
68. Sherman G.B., Wolfe M.W., Farmerie T.A., Clay C.M., Threadgill D.S., Sharp D.C., and Nilson J.H. A single gene encodes the beta-subunits of equine luteinizing hormone and chorionic gonadotropin. Mol. Endocrinol. 6 (1992) 951-959
69. Springer M.S., Stanhope M.J., Madsen O., and de Jong W.W. Molecules consolidate the placental mammal tree. Trends Ecol. Evol. 19 (2004) 430-438
70. Springer M.S., Murphy W.J., Eizirik E., and O'Brien S.J. Molecular evidence for major placental clades. In: Rose K.D., and Archibald J.D. (Eds). The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades (2005), Johns Hopkins University Press, Baltimore 37-49
71. Starck D. Ontogenie und Entwicklungsphysiologie der Säugetiere. In: Kükenthal W. (Ed). Handbuch der Zoologie vol. 8 (1959), de Gruyter, Berlin 1-276
72. Starck D. Embryologie. Ein Lehrbuch auf allgemein biologischer Grundlage (1975), Thieme, Stuttgart
73. Stewart J.R., Thompson M.B., Attaway M.B., Herbert J.F., and Murphy C.R. Uptake of dextran-FITC by epithelial cells of the chorioallantoic placentome and the omphalopleure of the placentotrophic lizard, Pseudemoia entrecasteauxii. J. Exp. Zool., A Comp. Exp. Biol. 305 (2006) 883-889
74. Teeling E.C., Springer M.S., Madsen O., Bates P., O'Brien S.J., and Murphy W.J. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307 (2005) 580-584
75. Thursby-Pelham D. The placentation of Hyrax capensis. Philos. Trans. R. Soc. Lond., B 213 (1923) 1-20
76. Turner W. On the placentation of the sloths (Choloepus hoffmanni). Trans. R. Soc. Edinb. 27 (1873) 71-104
77. Van Dijk J.P. Regulatory aspects of placental iron transfer-a comparative study. Placenta 9 (1988) 215-226
78. Vogel P. The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta 26 (2005) 591-596
79. Waddell P.J., Kishino H., and Ota R. A phylogenetic foundation for comparative mammalian genomics. Genome Inform. 12 (2001) 141-154
80. Wildman D.E., Chen C., Erez O., Grossman L.I., Goodman M., and Romero R. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 3203-3208
81. Wislocki G.B. On the placentation of the tridactyl sloth (Bradypus griseus) with a description of some characters of the fetus. Contrib. Embryol. Carnegie Inst. Washington vol. 19 (1927) 211-228
82. Wislocki G.B. Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus Gray and Choloepus hoffmani Peters). J. Morphol. Physiol. 46 (1928) 317-397
83. Wislocki G.B. On the placentation of the two-toed anteater. Anat. Rec. 39 (1928) 69-82
84. Wooding F.B., Stewart F., Mathias S., and Allen W.R. Placentation in the African elephant, Loxodonta africanus: III. Ultrastructural and functional features of the placenta. Placenta 26 (2005) 449-470
85. Zeh D.W., and Zeh J.A. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. Bioessays 22 (2000) 938-946