Evolutionary Biology

, Volume 38, Issue 3, pp 287–305 | Cite as

Life-History Correlates of Placental Structure in Eutherian Evolution

  • Eric Lewitus
  • Christophe Soligo
Research Article


The eutherian placenta shows remarkable evolutionary plasticity. To date, however, success in identifying selection pressures behind the observed diversity of placental structures has been limited. Evolutionary convergence among definitive placental morphologies and between placental morphologies and life-history variables can be used to suggest functions of derived aspects of placentation. In this paper, we use, for the first time, a comprehensive phylogenetic comparative approach to map phenotypic character states of both placental morphologies and life-history characteristics of species onto hypotheses of phylogenetic relationships in Eutheria. We employ phylogenetic methods for ancestral reconstruction, mutational mapping, and association analysis to resolve associations between five aspects of placental structure and to identify dominant combinations, or syndromes, of placental morphology. We map twenty life-history characters onto the eutherian phylogeny to examine how they correlate, over evolutionary time, with the multivariate diversification of placental structures. We identify two distinct eutherian constellations, based on associations between life-history and placental structure, which broadly reflect a dichotomy between slow and fast life-history strategies. In addition, we suggest that the observed association between placental invasiveness and group size is indicative of the effect of social behavior on the utility of genomic-imprinting in eutherian evolution.


Placentation Mutational mapping Character association Ancestral state reconstruction Genomic-imprinting Viviparity 



We thank ORP Bininda-Emonds for providing updated branch length data and ECL for useful discussion.

Supplementary material

11692_2011_9115_MOESM1_ESM.xls (79 kb)
Supplementary material 1 (XLS 79 kb)
11692_2011_9115_MOESM2_ESM.doc (78 kb)
Supplementary material 1 (DOC 79 kb)


  1. Abd-Elnaeim, M. M., Pfarrer, C., Saber, A. S., Abou-Elmagd, A., Jones, C. J., & Leiser, R. (1999). Fetomaternal attachment and anchorage in the early diffuse epitheliochorial placenta of the camel (Camelus dromedarius). Light, transmission, and scanning electron microscopic study. Cells Tissues Organs, 164, 141–154.PubMedCrossRefGoogle Scholar
  2. Allen, W. R., Mathias, S., Wooding, F. B. P., Skidmore, J., & van Aarde, R. J. (2002). Placentation in the African elephant, Loxodonta africana. I. Endocrinological aspects. Reproduction Supplement, 60, 105–116.Google Scholar
  3. Allen, W. R., Mathias, S., Wooding, F. B. P., & van Aarde, R. J. (2003). Placentation in the African elephant (Loxodonta africana) II. Morphological aspects. Placenta, 24, 598–617.PubMedCrossRefGoogle Scholar
  4. Amoroso, E. C. (1959). Comparative anatomy of the placenta. Annals of the New York Academy of Sciences, 75, 855–872.PubMedCrossRefGoogle Scholar
  5. Archibald, J., & Rose, K. (2005). In J. Archibald & K. Rose (Eds.), The rise of placental mammals (pp. 1–8). Baltimore: Johns Hopkins University Press.Google Scholar
  6. Armstrong, T. (2003). Symptoms experience: A concept analysis. Oncology Nursing Forum, 30, 601–660.PubMedCrossRefGoogle Scholar
  7. Arnold, S. J., & Futuyma, D. (2009). The ultimate causes of phenotypic integration: Lost in translation. Evolution, 59, 2059–2061.Google Scholar
  8. Asher, R. J., Novacek, M. J., & Geisler, J. H. (2003). Relationships of endemic African mammals and their fossil relatives based on morphological and molecular evidence. Journal of Mammalian Evolution, 10, 131–194.CrossRefGoogle Scholar
  9. Ashwal, S., Dale, P. S., & Longo, L. D. (1984). Regional cerebral blood flow: Studies in the fetal lamb during hypoxia, hypercapnia, addosis, and hypotension. Pediatric Research, 18, 1309–1316.PubMedCrossRefGoogle Scholar
  10. Baur, R. (1977). Morphometry of the placental exchange area. Advances in Anatomy, Embryology and Cell Biology, 53, 3–65.Google Scholar
  11. Baur, R. (1981). Morphometric data and questions concerning placental transfer. Placenta Supplement, 53, 1–65.Google Scholar
  12. Beese, K., Armbruster, G., Beier, K., & Baur, B. (2008). Evolution of female sperm-storage organs in the carrefour of stylommatophoran gastropods. Journal of Zoological Systematics and Evolutionary Research, 47(1), 49–60.CrossRefGoogle Scholar
  13. Belanger, C., Shome, B., Friesen, H., & Myers, R. E. (1971). Studies of the secretion of monkey placental lactogen.Google Scholar
  14. Benirschke, K. (2010). Comparative placentation. Retrieved April 2010, from
  15. Benirschke, K., & Kaufmann, P. (2000). Pathology of the human placenta. New York: Springer.Google Scholar
  16. Bianchi, D., & Lo, Y. (2001). Fetomaternal cellular and plasma DNA trafficking. Annals of the New York Academy of Sciences, 945, 119–131.PubMedCrossRefGoogle Scholar
  17. Bininda-Emonds, O., Cardillo, M., Jones, K., MacPhee, R., Beck, R., Grenyer, R., et al. (2007). The delayed rise of present-day mammals. Nature, 446, 507–512.PubMedCrossRefGoogle Scholar
  18. Bollback, J. P. (2005). Posterior mapping and predictive distributions. In R. Nielsen (Ed.), Statistical methods in molecular evolution (pp. 189–203). New York: Springer Verlag New York, Inc.Google Scholar
  19. Bollback, J. (2006). SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics, 7, 88.PubMedCrossRefGoogle Scholar
  20. Braunstein, G., Rasor, J., Engvall, E., & Wade, M. (1980). Interrelationships of human chorionic gonadotropin, human placental lactogen, and pregnancy-specific beta 1-glycoprotein throughout normal human gestation. American Journal of Obstetrics and Gynecology, 138, 1205–1213.PubMedGoogle Scholar
  21. Bressan, F. F., De Bem, T. H. C., Perecin, F., Lopes, F. L., Ambrosio, C. E., Meirelles, F. V., et al. (2009). Unearthing the roles of imprinted genes in the placenta. Placenta, 30, 823–834.PubMedCrossRefGoogle Scholar
  22. Burton, G., Watson, A., Hempstock, J., Skepper, J., & Jauniaux, E. (2002). Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. Journal of Clinical Endocrinology and Metabolism, 87, 2954–2959.PubMedCrossRefGoogle Scholar
  23. Calsbeek, R., Irschick, D. J., & Pfenning, D. (2009). The quick and the dead: Correlational selection on morphology, performance, and habitat use in island lizards. Evolution, 61, 2493–2503.CrossRefGoogle Scholar
  24. Carter, A. M. (1989). Factors affecting gas transfer across the placenta and the oxygen supply to the fetus. Journal of Developmental Physiology, 12, 305–322.PubMedGoogle Scholar
  25. Carter, A. M. (1999). J. P. Hill on placentation in primates. Placenta, 20, 513–517.PubMedCrossRefGoogle Scholar
  26. Carter, A. M. (2001). Evolution of the placenta and fetal membranes seen in the light of molecular phylogenetics. Placenta, 22, 800–807.PubMedCrossRefGoogle Scholar
  27. Carter, A. M. (2009). Evolution of factors affecting placental oxygen transfer. Placenta, 30, 19–25.CrossRefGoogle Scholar
  28. Carter, A. M., Blankenship, T. N., Kunzle, H., & Enders, A. C. (2004). Structure of the definitive placenta of the tenrec, Echinops telfairi. Placenta, 25, 218–232.PubMedCrossRefGoogle Scholar
  29. Carter, A. M., Blankenship, T. N., Künzle, H., & Enders, A. C. (2005). Development of the haemophagous region and labyrinth of the placenta of the tenrec, Echinops telfairi. Placenta, 26, 251–261.PubMedCrossRefGoogle Scholar
  30. Carter, A. M., Croy, B. A., Dantzer, V., Enders, A. C., Hayakawa, S., Mess, A., et al. (2007). Comparative aspects of placental evolution: A workshop report. Placenta, 28, S129–S132.PubMedCrossRefGoogle Scholar
  31. Carter, A., & Enders, A. (2004). Comparative aspects of trophoblast development and placentation. Reproductive Biology and Endocrinology, 2, 46.PubMedCrossRefGoogle Scholar
  32. Carter, A. M., & Mess, A. (2007). Evolution of the placenta in eutherian mammals. Placenta, 28, 259–262.PubMedCrossRefGoogle Scholar
  33. Carter, A. M., Miglino, M. A., Ambrósio, C. E., Santos, T., Rosas, F., et al. (2008). Placentation in the Amazonian manatee (Trichechus inunguis). Reproduction, Fertility, and Development, 20, 537–545.PubMedCrossRefGoogle Scholar
  34. Chard, T. (1982). Human placental lactogen in the monitoring of high-risk pregnancy. International Journal of Clinical and Laboratory Research, 12(1), 207–220.Google Scholar
  35. Cifelli, R. L., & Gordon, C. L. (2007). Evolutionary biology: Re-crowning mammals. Nature, 447, 918–920.PubMedCrossRefGoogle Scholar
  36. Collar, D. C., Wainwright, P. C., & Alfaro, M. E. (2008). Integrated diversification of locomotion and feeding in labrid fishes. Biology Letters, 4, 84–86.PubMedCrossRefGoogle Scholar
  37. Crespi, B., & Semeniuk, C. (2004). Parent-offspring conflict in the evolution of vertebrate reproductive mode. The American Naturalist, 163, 635–653.PubMedCrossRefGoogle Scholar
  38. Croy, B., Van Den Heuvel, M. J., Borzychowski, A. M., & Tayade, C. (2006). Uterine natural killer cells: A specialized differentiation regulated by ovarian hormones. Immunological Reviews, 214, 161–185.PubMedCrossRefGoogle Scholar
  39. Cunningham, C. W. (1999). Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Systematic Biology, 48, 665–674.CrossRefGoogle Scholar
  40. Dobson, F., & Oli, M. (2007). Fast and slow life histories of rodents. In J. Wolff & P. Sherman (Eds.), Rodent societies (pp. 99–105). Chicago: University of Chicago Press.Google Scholar
  41. Elliot, M. G., & Crespi, B. J. (2006). Placental invasiveness mediates the evolution of hybrid inviability in mammals. American Naturalist, 168, 114–120.PubMedCrossRefGoogle Scholar
  42. Elliot, M., & Crespi, B. (2008). Placental invasiveness and brain-body allometry in eutherian mammals. Journal of Evolutionary Biology, 21, 1763–1778.PubMedCrossRefGoogle Scholar
  43. Elliot, M. G., & Crespi, B. J. (2009). Phylogenetic evidence for early hemochorial placentation in Eutheria. Placenta, 30, 949–967.PubMedCrossRefGoogle Scholar
  44. Enders, A., Blankenship, T., Lantz, K., & Enders, S. (1998). Morphological variations in the interhemal areas of chorioallantoic placentas. Trophoblast Research, 12, 1–19.Google Scholar
  45. Enders, A. C. (1965). A comparative study of the fine structure of the trophoblast in several hemochorial placentas. The American Journal of Anatomy, 116, 29–68.PubMedCrossRefGoogle Scholar
  46. Enders, A. C. (2009). Reasons for diversity of placental structure. Placenta, 30, 15–18.CrossRefGoogle Scholar
  47. Enders, A. C., & Carter, A. M. (2004). What can studies of comparative placental structure tell us? Placenta, 25, S3–S7.PubMedCrossRefGoogle Scholar
  48. Enders, A. C., & Carter, A. M. (2006). Comparative placentation: some interesting modifications for histotrophic nutrition—A review. Placenta, 27, 11–16.CrossRefGoogle Scholar
  49. Estes, S., & Arnold, S. (2007). Resolving the paradox of stasis: Models with stabilizing selection explain evolutionary divergence on all timescales. The American Naturalist, 169, 227–244.PubMedCrossRefGoogle Scholar
  50. Faber, J. J., Thornburg, K. L., & Binder, N. D. (1992). Physiology of placental transfer in mammals. American Zoologist, 32, 343–354.Google Scholar
  51. Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.CrossRefGoogle Scholar
  52. Felsenstein, J. (1988). Phylogenies from molecular sequences: Inference and reliability. Annual Review of Genetics, 22, 521–565.PubMedCrossRefGoogle Scholar
  53. Flietstra, R., & Voogt, J. (1996). Rat placental lactogens initiate and maintain lactation yet inhibit suckling-induced prolactin release. Endocrine, 5, 103–110.PubMedCrossRefGoogle Scholar
  54. Franzke, R., & Jelkmann, W. (1982). Characterization of the pyruvate kinase which induces the low 2, 3-DPG level of fetal rabbit red cells. Pflugers Archiv, 294, 21–25.Google Scholar
  55. Freyer, C., & Renfree, M. B. (2009). The mammalian yolk sac placenta. Journal of Experimental Zoology, 312B, 5445–5554.Google Scholar
  56. Gill, T., & Wegmann, T. (1987). Immunoregulation and fetal survival. New York: Oxford University Press.Google Scholar
  57. Graves, J. A. M. (2010). Review: Sex chromosome evolution and the expression of sex-specific genes in the placenta. Placenta, 31, S27–S32.PubMedCrossRefGoogle Scholar
  58. Haig, D. (1993). Genetic conflicts in human pregnancy. Quarterly Review of Biology, 68, 495–532.PubMedCrossRefGoogle Scholar
  59. Haig, D. (1996). Altercation of generations: Genetic conflicts of pregnancy. American Journal of Reproductive Immunology, 35, 226–232.PubMedGoogle Scholar
  60. Haig, D. (2004). Evolutionary conflict in pregnancy and calcium metabolism—A review. Placenta (Suppl), 18, 10–15.CrossRefGoogle Scholar
  61. Haig, D. (2008). Placental growth hormone-related proteins and prolactin-related proteins. Placenta, 29, S36–S41.PubMedCrossRefGoogle Scholar
  62. Hallstrom, B. M., Kullberg, M., Nilsson, M. A., & Janke, A. (2007). Phylogenomic data analyses provide evidence that Xenarthra and Afrotheria are sister groups. Molecular Biology and Evolution, 24, 2059–2068.PubMedCrossRefGoogle Scholar
  63. Handwerger, S., & Brar, A. (1992). Placental lactogen, placental growth hormone, and decidual prolactin. Seminars in Reproductive Endocrinology, 10, 106–115.CrossRefGoogle Scholar
  64. Hartigan, J. A., & Wong, M. A. (1979). Algorithm AS 136: A K-means clustering algorithm. Journal of the Royal Statistical Society. Series C (Applied Statistics), 28, 100–108.Google Scholar
  65. Harvey, P. H., & Pagel, M. D. (1991). The comparative method in evolutionary biology. Oxford: Oxford University Press.Google Scholar
  66. Hill, J. P. (1932). The developmental history of the primates. Philosophical Transactions of the Royal Society of London, Series B, 221, 45–178.CrossRefGoogle Scholar
  67. Homko, C. J., Sivan, E., Reece, E. A., & Boden, G. (1999). Fuel metabolism during pregnancy. Seminars in Reproductive Medicine, 17, 119–125.CrossRefGoogle Scholar
  68. Huelsenbeck, J. P., Nielsen, R., & Bollback, J. P. (2003). Stochastic mapping of morphological characters. Systematic Biology, 52, 131–158.PubMedCrossRefGoogle Scholar
  69. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics Applications Note, 17, 754–755.Google Scholar
  70. Jauniaux, E., Cindrova-Davies, T., Johns, J., Dunster, C., Hempstock, J., Kelly, F., et al. (2004). Distribution and transfer pathways of antioxidant molecules inside the first trimester human gestational sac. Journal of Clinical Endocrinology and Metabolism, 89, 1452–1458.PubMedCrossRefGoogle Scholar
  71. Jelkmann, W., & Bauer, C. (1977). Oxygen affinity and phosphate compounds of red blood cells during intrauterine development of rabbits. Pflugers Archiv, 372, 149–156.PubMedCrossRefGoogle Scholar
  72. Jenks, G., & Caspall, F. (1971). Error on choroplethic maps: Definition, measurement, reduction. Annals of the Association of American Geographers, 61, 217–244.CrossRefGoogle Scholar
  73. Jones, A. G., Arnold, S. J., & Burger, R. (2003). Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution, 57, 1747–1760.PubMedGoogle Scholar
  74. Kastendieck, E., & Moll, W. (1977). The placental transfer of lactate and bicarbonate in the guinea-pig. Pflugers Archiv, 370, 165–171.PubMedCrossRefGoogle Scholar
  75. Kaufmann, P. (1981). Functional anatomy of the non-primate placenta. Placenta (Suppl), 1, 13–28.Google Scholar
  76. King, B., & Enders, A. (1993). Comparative development of the mammalian yolk sac. In F. Nogales (Ed.), The human yolk sac and the yolk sac tumors (pp. 1–32). Berlin: Springer.Google Scholar
  77. Klisch, K., & Mess, A. (2007). Evolutionary differentiation of cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis. Placenta, 28, 353–360.PubMedCrossRefGoogle Scholar
  78. Kriegs, J., Churakov, G., Kiefmann, M., Jordan, U., Brosius, J., & Schmitz, J. (2006). Retroposed elements as archives for evolutionary history of placental mammals. PLoS Biology, 4, e91.PubMedCrossRefGoogle Scholar
  79. Lande, L., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37, 1210–1226.CrossRefGoogle Scholar
  80. Le Gros Clark, W. (1959). The antecedents of man. Edinburgh: Edinburgh University Press.Google Scholar
  81. Leutenegger, W. (1973). Maternal-fetal weight relationships in primates. Folia Primatologica, 20, 280–293.CrossRefGoogle Scholar
  82. Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50(6), 913–925.PubMedCrossRefGoogle Scholar
  83. Lillegraven, J., Thompson, S., McNab, B., & Patton, J. (1987). The origin of eutherian mammals. Biological Journal of the Linnean Society London, 32, 281–336.CrossRefGoogle Scholar
  84. Lin, Y., McLenachan, P., Gore, A., Phillips, M., et al. (2002). Four new mitochondrial genomes and the increased stability of evolutionary trees of mammals from improved taxon sampling. Molecular Biology and Evolution, 19, 2060–2070.PubMedGoogle Scholar
  85. Longo, L. D., & Ching, K. S. (1977). Placental diffusing capacity for carbon monoxide and oxygen in unanesthetized sheep. Journal of Applied Physiology, 43, 885–893.PubMedGoogle Scholar
  86. Luckett, W. P. (1974). The comparative development and evolution of the placenta in primates. Contributions to Primatology, 3, 142–234.PubMedGoogle Scholar
  87. Luckett, W. P. (1976). Cladistic relationship among higher primate categories: Evidence of the fetal membranes and placenta. Folia Primatologica, 25, 245–276.CrossRefGoogle Scholar
  88. Luckett, W. P. (1977). Ontogeny of amniote fetal membranes and their application to phylogeny. In M. Hecht, P. Goody, & B. Hecht (Eds.), Major patterns in vertebrate evolution (pp. 439–516). New York: Plenum Press.Google Scholar
  89. Luckett, W. P. (1993). Uses and limitations of mammalian fetal membranes and placenta for phylogenetic reconstruction. Journal of Experimental Zoology, 266, 514–527.PubMedCrossRefGoogle Scholar
  90. MacArthur, R., & Wilson, E. (1967). The theory of island biogeography. New Jersey: Princeton University Press.Google Scholar
  91. Maddison, W., & Maddison, D. (2009). Mesquite: A modular system for evolutionary analysis, version 2.7.
  92. Madsen, O., Scally, M., Douady, C. J., Kao, D., et al. (2001). Parallel adaptive radiations in two major clades of placental mammals. Nature, 409, 610–614.PubMedCrossRefGoogle Scholar
  93. Martin, R. D. (1990). Primate origins and evolution: A phylogenetic reconstruction. Princeton: Princeton University Press.Google Scholar
  94. Martin, R. D. (2003). Human reproduction: A comparative background for medical hypotheses. Journal of Reproductive Immunology, 59, 111–135.PubMedCrossRefGoogle Scholar
  95. Martin, R. (2007). The evolution of human reproduction: A primatological perspective. American Journal of Physical Anthropology, 134, 59–84.CrossRefGoogle Scholar
  96. Martin, R. (2008). Evolution of placentation in primates: Implications of mammalian phylogeny. Evolutionary Biology, 35, 125–145.CrossRefGoogle Scholar
  97. Martins, E. P. (2000). Adaptation and the comparative method. Trends in Ecology and Evolution, 15(7), 296–299.PubMedCrossRefGoogle Scholar
  98. McVean, G., & Hurst, L. (1997). Molecular evolution of imprinted genes: No evidence for antagonistic coevolution. Proceedings. Biological Sciences, 264, 739–746.CrossRefGoogle Scholar
  99. Mess, A., Blackburn, D. G., & Zeller, U. (2003). Evolutionary transformations of fetal membranes and reproductive strategies. Journal of Experimental Zoology, Part A: Comparative Experimental Biology, 299A(1), 3–12.Google Scholar
  100. Mess, A., & Carter, A. M. (2006). Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 306B, 140–163.CrossRefGoogle Scholar
  101. Mess, A., & Carter, A. M. (2007). Evolution of the placenta during the early radiation of placental mammals. Comparative Biochemistry and Physiology—Part A: Molecular & Integrative Physiology, 148, 769–779.CrossRefGoogle Scholar
  102. Mess, A. M., & Carter, A. M. (2009). Evolution of the interhaemal barrier in the placenta of rodents. Placenta, 30, 914–918.PubMedCrossRefGoogle Scholar
  103. Metcalfe, J., Bartels, H., & Moll, W. (1967). Gas exchange in the pregnant uterus. Physiological Reviews, 47, 782–838.PubMedGoogle Scholar
  104. Miglino, M. A., Carter, A. M., Ambrósio, C. E., Bonatelli, M., De Oliveira, M. F., Dos Santos Ferraz, R. H., et al. (2004). Vascular organization of the hystriocomorph placenta: A comparative study in the agouti, capybara, guinea pig, paca and rock cavy. Placenta, 25, 438–449.PubMedCrossRefGoogle Scholar
  105. Miglino, M. A., Franciolli, A. L. R., de Oliveira, M. F., Ambrósio, C. E., Bonatelli, M., Machado, M. R. F., et al. (2008). Development of the inverted visceral yolk sac in three species of Caviids (Rodentia, Caviomorpha, Caviidae). Placenta, 29, 748–752.PubMedCrossRefGoogle Scholar
  106. Moffett, A., & Loke, C. (2006). Immunology of placentation in eutherian mammals. Nature Reviews Immunology, 6, 584–594.PubMedCrossRefGoogle Scholar
  107. Moll, W. (1972). Gas exchange in concurrent, countercurrent and cross current flow system. The concept of the fetoplacental unit. In L. D. Longo & H. Bartel (Eds.), Respiratory gas exchange and blood flow in the placenta. Bethesda, MD: US Department of Health, Education and Welfare.Google Scholar
  108. Moore, T., & Haig, D. (1991). Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell, 64, 1045–1046.CrossRefGoogle Scholar
  109. Mossman, H. (1987). Vertebrate fetal membranes: Comparative ontogeny and morphology, evolution, phylogenetic significance, basic functions, research opportunities. New Brunswick, NJ: Rutgers University Press.Google Scholar
  110. Mossman, H. (1991). Classics revisited: Comparative morphogenesis of the fetal membranes and accessory uterine structures. Placenta, 12, 1–5.PubMedCrossRefGoogle Scholar
  111. Murphy, W. J., Eizirik, E., O’Brien, S. J., Madsen, O., Scally, M., Douady, C. J., et al. (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science, 294, 2348–2351.PubMedCrossRefGoogle Scholar
  112. Murphy, W. J., Pringle, T., Crider, T., Springer, M. S., & Miller, W. (2007). Using genomic data to unravel the root of the placental mammal phylogeny. Genome Research, 17, 413–421.PubMedCrossRefGoogle Scholar
  113. Nelson, J. L. (2003). Microchimerism in human health and disease. Autoimmunity, 36, 5–9.PubMedCrossRefGoogle Scholar
  114. Nielsen, R. (2002). Mapping mutations on phylogenies. Systematic Biology, 51, 729–732.PubMedCrossRefGoogle Scholar
  115. Nishihara, H., Maruyama, S., & Okada, N. (2009). Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proceedings of the National Academy of Sciences, 106, 5235–5240.CrossRefGoogle Scholar
  116. Pagel, M. (1999). The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology, 48, 612–622.CrossRefGoogle Scholar
  117. Papper, Z., Jameson, N. M., Romero, R., Weckle, A. L., Mittal, P., Benirschke, K., et al. (2009). Ancient origin of placental expression in the growth hormone genes of anthropoid primates. Proceedings of the National Academy of Sciences, 106, 17083–17088.CrossRefGoogle Scholar
  118. Petschow, R., Petschow, D., Bartels, R., Baumann, R., & Bartels, H. (1978). Regulation of oxygen affinity in blood of fetal, newborn and adult mouse. Respiration Physiology, 35, 271–282.PubMedCrossRefGoogle Scholar
  119. Pianka, E. (1970). On r and K selection. American Naturalist, 104, 592–597.CrossRefGoogle Scholar
  120. Pijnenborg, R., & Vercruysse, L. (2004). Thomas Huxley and the rat placenta in the early debates on evolution. Placenta, 25, 233–237.PubMedCrossRefGoogle Scholar
  121. Prasad, A. B., Allard, M. W., Program, N. C. S., & Green, E. D. (2008). Confirming the phylogeny of mammals by use of large comparative sequence data sets. Molecular Biology and Evolution, 25, 1795–1808.PubMedCrossRefGoogle Scholar
  122. Promislow, D., & Harvey, P. H. (1990). Living fast and dying young—a comparative-analysis of life-history variation among mammals. Journal of Zoology, 220, 417–437.CrossRefGoogle Scholar
  123. Reik, W., & Walter, J. (1998). Imprinting mechanisms in mammals. Current Opinion in Genetics and Development, 8, 154–164.PubMedCrossRefGoogle Scholar
  124. Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63, 3258–3268.PubMedCrossRefGoogle Scholar
  125. Revell, L. J., & Harmon, L. J. (2008). Testing quantitative genetic hypotheses about the evolutionary rate matrix for continuous characters. Evolutionary Ecology Research, 10, 311–321.Google Scholar
  126. Revell, L. J., Harmon, L. J., & Collar, D. C. (2010). Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole. Journal of Evolutionary Biology, 23, 407–421.PubMedCrossRefGoogle Scholar
  127. Reznick, D., Mateos, M., & Springer, M. (2002). Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science, 298, 1018–1020.PubMedCrossRefGoogle Scholar
  128. Ronquist, F., Huelsenbeck, J. P., & Mark, P. (2005). MrBayes 3.1 manual. Tallahassee, FL: Florida State University.Google Scholar
  129. Schluter, D., Price, T., Mooers, A., & Ludwig, D. (1997). Likelihood of ancestor states in adaptive radiation. Evolution, 51, 1699–1711.CrossRefGoogle Scholar
  130. Schroder, H. J., & Power, G. G. (1997). Engine and radiator: Fetal and placental interactions for heat dissipation. Experimental Physiology, 82, 403–414.PubMedGoogle Scholar
  131. Schultz, T. R., & Churchill, G. A. (1999). The role of subjectivity in reconstructing ancestral character states: A Bayesian approach to unknown rates, states, and transformation asymmetries. Systematic Biology, 48, 651–664.CrossRefGoogle Scholar
  132. Shoshani, J., & McKenna, M. (1998). Higher taxonomic relationships among extant mammals based on morphology, with selected comparisons of results from molecular data. Molecular Phylogenetics and Evolution, 9, 572–584.PubMedCrossRefGoogle Scholar
  133. Spencer, M., Bryant, D., & Susko, E. (2007). Conditioned genome reconstruction: How to avoid choosing the conditioning genome. Systematic Biology, 56(1), 25–43.PubMedCrossRefGoogle Scholar
  134. Springer, M. S. (2004). A molecular view on relationships among the extant orders of placental mammals. In K. Rose & J. Archibald (Eds.), Origin, timing, and relationships among the major clades of extant placental mammals. Baltimore: Johns Hopkins University Press.Google Scholar
  135. Springer, M., Murphy, W., Eizirik, E., & O’Brien, S. (2005). Molecular evidence for major placental clades. In J. Archibald & K. Rose (Eds.), The rise of placental mammals (pp. 37–49). Baltimore: Johns Hopkins University Press.Google Scholar
  136. Steven, D. (1983). Interspecies differences in the structure and function of trophoblast. In C. Loke & A. Whyte (Eds.), Biology of trophoblast (pp. 111–136). Amsterdam: Elselvier.Google Scholar
  137. Steven, D., & Morriss, G. (1975). Development of the foetal membranes. In D. H. Steven (Ed.), Comparative placentation: Essays in structure and function (pp. 58–86). London: Academic Press.Google Scholar
  138. Vogel, P. (2005). The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution. Placenta, 26, 591–596.PubMedCrossRefGoogle Scholar
  139. Voogt, J., Robertson, M., & Friesen, H. (1982). Inverse relationship of prolactin and rat placental lactogen during pregnancy. Biology of Reproduction, 26, 800–805.PubMedCrossRefGoogle Scholar
  140. Waddell, J., & Shelley, S. (2003). Evaluating placental interordinal phylogenies with novel sequences including RAG1, g-fibrinogen, ND6, and mt-tRNA, plus MCMC-driven nucleotide, amino acid, and codon models. Molecular Phylogenetics and Evolution, 28, 197–224.PubMedCrossRefGoogle Scholar
  141. Walker, J. A. (2007). A general model of functional constraints on phenotypic evolution. American Naturalist, 170, 681–689.PubMedCrossRefGoogle Scholar
  142. Waters, P., Dobigny, G., Waddell, J., & Robinson, T. (2007). Evolutionary history of LINE-1 in the major clades of placental mammals. PLoS ONE, 2, e158.PubMedCrossRefGoogle Scholar
  143. Wildman, D. E. (2006). Evolution of the mammalian placenta revealed by phylogenetic analysis. Proceedings of the National Academy of Sciences of the United States of America, 103, 3203–3208.PubMedCrossRefGoogle Scholar
  144. Wildman, D. E., Uddin, M., Opazo, J. C., Liu, G., Lefort, V., Guindon, S., et al. (2007). Genomics, biogeography, and the diversification of placental mammals. Proceedings of the National Academy of Sciences, 104, 14395–14400.CrossRefGoogle Scholar
  145. Wilkening, R., & Meschia, G. (1992). Current topic: Comparative physiology of placental oxygen transport. Placenta, 13, 1–15.PubMedCrossRefGoogle Scholar
  146. Wilson, D. E., & Reeder, D. M. (Eds.). (2005). Mammal species of the world. A taxonomic and geographic reference (3rd ed.). Baltimore, MD: Johns Hopkins University Press.Google Scholar
  147. Wislocki, G. B. (1929). On the placentation of the primates, with a consideration of the phylogeny of the placenta. Contributions to embryology Carnegie Institution, 20, 51–80.Google Scholar
  148. Wooding, F., & Burton, G. (2008). Comparative placentation: Structures, functions and evolution. Berlin: Springer.CrossRefGoogle Scholar
  149. Wooding, F. B. P., & Flint, A. P. F. (1994). Placentation. In G. Lamming (Ed.), Marshall’s physiology of reproduction (Vol. 3, pp. 233–460). London: Chapman and Hall.Google Scholar
  150. Zeh, D., & Zeh, J. (2000). Reproductive mode and speciation: The viviparity-driven conflict hypothesis. BioEssays, 22, 938–946.PubMedCrossRefGoogle Scholar
  151. Zeh, J., & Zeh, D. (1996). The evolution of polyandry I: Intragenomic conflict and genetic compatibility. Proceedings. Biological Sciences, 263, 1711–1717.CrossRefGoogle Scholar
  152. Zeh, J., & Zeh, D. (1997). The evolution of polyandry II: Post-copulatory defenses against genetic incompatibility. Proceedings. Biological Sciences, 264, 69–75.CrossRefGoogle Scholar
  153. Zeh, J., & Zeh, D. (2008). Viviparity-driven conflict. Annals of the New York Academy of Sciences, 1133, 126–148.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity College LondonLondonUK

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