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The placenta as a model for understanding the origin and evolution of vertebrate organs

Abstract

How organs originate and evolve is a question fundamental to understanding the evolution of complex multicellular life forms. Vertebrates have a relatively standard body plan with more or less the same conserved set of organs. The placenta is a comparatively more recently evolved organ, derived in many lineages independently. Using placentas as a model, we discuss the genetic basis for organ origins. We show that the evolution of placentas occurs by acquiring new functional attributes to existing tissues, changes in the patterning and development of tissues, and the evolution of novel cell types. We argue that a diversity of genomic changes facilitated these physiological transformations and that these changes are likely to have occurred during the evolution of organs more broadly. Finally, we argue that a key aspect to understanding the evolutionary origin of organs is that they are likely to result from novel interactions between distinct cell populations.

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Figure 1: Major vertebrate organs have ancient origins.
Figure 2: Phylogenetic relationships of vertebrates in lineages in which the evolution of placental structures has been studied.
Figure 3: A small selection of the diverse parental and embryonic tissues involved in placental development in vertebrates.
Figure 4: How placental intimacy can result in new signalling processes supporting the evolution and origin of an organ.

References

  1. 1

    Oakley, T. H. & Speiser, D. I. How complexity originates: the evolution of animal eyes. Annu. Rev. Ecol. Evol. Syst. 46, 237–260 (2015).

    Article  Google Scholar 

  2. 2

    Gregory, T. R. The evolution of complex organs. Evo. Edu. Outreach 1, 358–389 (2008).

    Article  Google Scholar 

  3. 3

    Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).

    CAS  Article  PubMed  Google Scholar 

  4. 4

    Mossman, H. Comparative Morphogenesis of the Fetal Membranes and Accessory Uterine Structures Vol. 26 (Carnegie Institution of Washington, 1937).

    Google Scholar 

  5. 5

    Van Dyke, J. U., Brandley, M. C. & Thompson, M. B. The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes. Reproduction 147, R15–R26 (2014).

    CAS  Article  PubMed  Google Scholar 

  6. 6

    Reznick, D. N., Mateos, M. & Springer, M. S. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298, 1018–1020 (2002).

    CAS  Article  PubMed  Google Scholar 

  7. 7

    Blackburn, D. G. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J. Morphol. 276, 961–990 (2015).

    Article  PubMed  Google Scholar 

  8. 8

    Stewart, J. R. Placental specializations in lecithotrophic viviparous squamate reptiles. J. Exp. Zool. Part B 324, 549–561 (2015).

    Article  Google Scholar 

  9. 9

    Wright, A. M., Lyons, K. M., Brandley, M. C. & Hillis, D. M. Which came first: the lizard or the egg? Robustness in phylogenetic reconstruction of ancestral states. J. Exp. Zool. Part B 324, 504–516 (2015).

    Article  Google Scholar 

  10. 10

    Griffith, O. W. et al. Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: a case study examining the evolution of reproductive mode in squamate reptiles. J. Exp. Zool. Part B 324, 493–503 (2015).

    Article  Google Scholar 

  11. 11

    Cornetti, L., Ficetola, G. F., Hoban, S. & Vernesi, C. Genetic and ecological data reveal species boundaries between viviparous and oviparous lizard lineages. Heredity 115, 517–526 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12

    Murphy, B. & Thompson, M. A review of the evolution of viviparity in squamate reptiles: the past, present and future role of molecular biology and genomics. J. Comp. Physiol. B 181B, 575–594 (2011).

    Article  Google Scholar 

  13. 13

    Brigandt, I. & Love, A. C. Conceptualizing evolutionary novelty: moving beyond definitional debates. J. Exp. Zool. Part B 318, 417–427 (2012).

    Article  Google Scholar 

  14. 14

    Müller, G. B. & Wagner, G. P. Novelty in evolution: restructuring the concept. Annu. Rev. Ecol. Syst. 22, 229–256 (1991).

    Article  Google Scholar 

  15. 15

    Wagner, G. P. Evolutionary innovations and novelties: let us get down to business! Zool. Anz. 256, 75–81 (2015).

    Article  Google Scholar 

  16. 16

    Love, A. C. Evolutionary morphology, innovation, and the synthesis of evolutionary and developmental biology. Biol. Philos. 18, 309–345 (2003).

    Article  Google Scholar 

  17. 17

    Wagner, G. P. Homology, Genes and Evolutionary Innovation (Princeton Univ. Press, 2014).

    Book  Google Scholar 

  18. 18

    Arendt, D. et al. Evolution of sister cell types by individuation. Nat. Rev. Genet. 17, 744–757 (2016).

  19. 19

    Wagner, G. P., Pavlicev, M. & Cheverud, J. M. The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).

    CAS  Article  PubMed  Google Scholar 

  20. 20

    Eddy, S. R. The C-value paradox, junk DNA and ENCODE. Curr. Biol. 22, R898–R899 (2012).

    CAS  Article  PubMed  Google Scholar 

  21. 21

    Richter, D. J. & King, N. The genomic and cellular foundations of animal origins. Annu. Rev. Genet. 47, 509–537 (2013).

    Article  PubMed  Google Scholar 

  22. 22

    Erwin, D. H. Early origin of the bilaterian developmental toolkit. Phil. Trans. R. Soc. B 364, 2253–2261 (2009).

    CAS  Article  PubMed  Google Scholar 

  23. 23

    Chen, S., Krinsky, B. H. & Long, M. New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 14, 645–660 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24

    Blackburn, D. G. Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J. Exp. Zool. 282, 560–617 (1998).

    CAS  Article  PubMed  Google Scholar 

  25. 25

    Thompson, M. B. & Speake, B. K. A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. J. Comp. Physiol. 176B 179–189 (2006).

    Article  Google Scholar 

  26. 26

    Cruze, L., Hamlin, H. J., Kohno, S., McCoy, M. W. & Guillette Jr, L. J. Evidence of steroid hormone activity in the chorioallantoic membrane of a Turtle (Pseudemys nelsoni). Gen. Comp. Endocr. 186, 50–57 (2013).

    CAS  Article  PubMed  Google Scholar 

  27. 27

    Griffith, O. W., Brandley, M. C., Whittington, C. M., Belov, K. & Thompson, M. B. Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes. Gen. Comp. Endocrinol. http://dx.doi.org/10.1016/j.ygcen.2016.04.017 (2016).

  28. 28

    Linville, B. et al. Placental calcium provision in a lizard with prolonged oviductal egg retention. J. Comp. Physiol. B 180B 221–227 (2010).

    Article  Google Scholar 

  29. 29

    Herbert, J. F., Murphy, C. R. & Thompson, M. B. Calcium ATPase localization in the uterus of two species of Pseudemoia (Lacertilia: Scincidae) with complex placentae. Herpetol. Conserv. Biol. 5, 290–296 (2010).

    Google Scholar 

  30. 30

    Stewart, J. R., Ecay, T. W., Heulin, B., Fregoso, S. P. & Linville, B. J. Developmental expression of calcium transport proteins in extraembryonic membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae). J. Exp. Biol. 214, 2999–3004 (2011).

    CAS  Article  PubMed  Google Scholar 

  31. 31

    Blank, D., Wolf, L., Ackermann, M. & Silander, O. K. The predictability of molecular evolution during functional innovation. Proc. Natl Acad. Sci. USA 111, 3044–3049 (2014).

    CAS  Article  PubMed  Google Scholar 

  32. 32

    Dennis, A. B., Dunning, L. T., Sinclair, B. J. & Buckley, T. R. Parallel molecular routes to cold adaptation in eight genera of New Zealand stick insects. Sci. Rep. 5, 13965 (2015).

  33. 33

    Rawn, S. M. & Cross, J. C. The evolution, regulation, and function of placenta-specific genes. Annu. Rev. Cell Dev. Biol. 24, 159–181 (2008).

    CAS  Article  PubMed  Google Scholar 

  34. 34

    Schep, R. et al. Control of Hoxd gene transcription in the mammary bud by hijacking a preexisting regulatory landscape. Proc. Natl Acad. Sci. USA 113, E7720–E7729 (2016).

    CAS  Article  PubMed  Google Scholar 

  35. 35

    Lynch, V. J. et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 10, 551–561 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36

    Griffith, O. W., Brandley, M. C., Belov, K. & Thompson, M. B. Reptile pregnancy is underpinned by complex changes in uterine gene expression: a comparative analysis of the uterine transcriptome in viviparous and oviparous lizards. Genome Biol. Evol. 8, 3226–3239 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37

    Kin, K. et al. The transcriptomic evolution of mammalian pregnancy: gene expression innovations in endometrial stromal fibroblasts. Genome Biol. Evol. 8, 2459–2473 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38

    Wittkopp, P. J. & Kalay, G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13, 59–69 (2012).

    CAS  Article  Google Scholar 

  39. 39

    Carter, A. M. Evolution of placental function in mammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol. Rev. 92, 1543–1576 (2012).

    CAS  Article  PubMed  Google Scholar 

  40. 40

    Lowdon, R. F., Jang, H. S. & Wang, T. Evolution of epigenetic regulation in vertebrate genomes. Trends Genet. 32, 269–283 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41

    Feschotte, C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397–405 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42

    Emera, D. et al. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29, 239–247 (2012).

    CAS  Article  PubMed  Google Scholar 

  43. 43

    Chuong, E. B., Rumi, M. A. K., Soares, M. J. & Baker, J. C. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 45, 325–329 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44

    Lynch, V. J., Leclerc, R. D., May, G. & Wagner, G. P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43, 1154–1158 (2011).

    CAS  Article  PubMed  Google Scholar 

  45. 45

    Kordis, D. Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet. Genome Res. 127, 94–111 (2009).

    CAS  Article  PubMed  Google Scholar 

  46. 46

    Gilbert, C., Hernandez, S. S., Flores-Benabib, J., Smith, E. N. & Feschotte, C. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol. Biol. Evol. 29, 503–515 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    Whittington, C. M., Griffith, O. W., Qi, W., Thompson, M. B. & Wilson, A. B. Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. Mol. Biol. Evol. 32, 3114–3131 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48

    Fried, C., Prohaska, S. J. & Stadler, P. F. Exclusion of repetitive DNA elements from gnathostome Hox clusters. J. Exp. Zool. Part B 302B 165–173 (2004).

    CAS  Article  Google Scholar 

  49. 49

    Di-Poï, N. et al. Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464, 99–103 (2010).

    Article  CAS  PubMed  Google Scholar 

  50. 50

    Long, M., VanKuren, N. W., Chen, S. & Vibranovski, M. D. New gene evolution: little did we know. Annu. Rev. Genet. 47, 307–333 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51

    Knox, K. & Baker, J. C. Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res. 18, 695–705 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52

    Zhang, J. Z. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292–298 (2003).

    Article  Google Scholar 

  53. 53

    Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).

    CAS  Article  PubMed  Google Scholar 

  54. 54

    Varanou, A. et al. The importance of cysteine cathepsin proteases for placental development. J. Mol. Med. 84, 305–317 (2006).

    CAS  Article  PubMed  Google Scholar 

  55. 55

    Puente, X. S. & López-Otín, C. A genomic analysis of rat proteases and protease inhibitors. Genome Res. 14, 609–622 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56

    Ramsey, E. M. The Placenta Human and Animal (Praeger, 1982).

    Google Scholar 

  57. 57

    Gundling, W. E. & Wildman, D. E. A review of inter- and intraspecific variation in the eutherian placenta. Phil. Trans. R. Soc. B 370, 20140072 (2015).

  58. 58

    Blackburn, D. G., Avanzati, A. M. & Paulesu, L. Classics revisited. History of reptile placentology: Studiati's early account of placentation in a viviparous lizard. Placenta 36, 1207–1211 (2015).

    Article  PubMed  Google Scholar 

  59. 59

    Carter, A. M. & Enders, A. C. Placentation in mammals: definitive placenta, yolk sac and paraplacenta. Theriogenology 86, 278–287 (2016).

    CAS  Article  PubMed  Google Scholar 

  60. 60

    Stölting, K. N. & Wilson, A. B. Male pregnancy in seahorses and pipefish: beyond the mammalian model. BioEssays 29, 884–896 (2007).

    Article  PubMed  Google Scholar 

  61. 61

    Ripley, J. L. Osmoregulatory role of the paternal brood pouch for two Syngnathus species. Comp. Biochem. Physiol. Part A 154, 98–104 (2009).

    Article  CAS  Google Scholar 

  62. 62

    Carcupino, M., Baldacci, A., Mazzini, M. & Franzoi, P. Functional significance of the male brood pouch in the reproductive strategies of pipefishes and seahorses: a morphological and ultrastructural comparative study on three anatomically different pouches. J. Fish Biol. 61, 1465–1480 (2002).

    Article  Google Scholar 

  63. 63

    Fiedler, K. Hormonale auslösung der geburtsbewegungen beim seepferdchen (Hippocampus, Syngnathidae, Teleostei). Z. Tierpsychol. 27, 679–686 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Shubin, N., Tabin, C. & Carroll, S. Deep homology and the origins of evolutionary novelty. Nature 457, 818–823 (2009).

    CAS  Article  PubMed  Google Scholar 

  65. 65

    Wagner, G. P. & Lynch, V. J. Evolutionary novelties. Curr. Biol. 20, R48–R52 (2010).

    CAS  Article  PubMed  Google Scholar 

  66. 66

    Arendt, D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868–882 (2008).

    CAS  Article  PubMed  Google Scholar 

  67. 67

    Wagner, G. P. What is “homology thinking” and what is it for? J. Exp. Zool. Part B 326, 3–8 (2015).

    Article  Google Scholar 

  68. 68

    Liang, C., the, F. C., Forrest, A. R. R. & Wagner, G. P. The statistical geometry of transcriptome divergence in cell-type evolution and cancer. Nat. Commun. 6, 6066 (2015).

  69. 69

    Chavan, A. R., Bhullar, B. A. & Wagner, G. P. What was the ancestral function of decidual stromal cells? A model for the evolution of eutherian pregnancy. Placenta 40, 40–51 (2016).

    Article  PubMed  Google Scholar 

  70. 70

    Kin, K., Nnamani, Mauris C., Lynch, Vincent J., Michaelides, E. & Wagner, Günter P. Cell-type phylogenetics and the origin of endometrial stromal cells. Cell Rep. 10, 1398–1409 (2015).

    CAS  Article  PubMed  Google Scholar 

  71. 71

    Kin, K., Maziarz, J. & Wagner, G. P. Immunohistological study of the endometrial stromal fibroblasts in the opossum, Monodelphis domestica: evidence for homology with eutherian stromal fibroblasts. Biol. Reprod. 90, 111 (2014).

  72. 72

    Vasquez, Y. M. et al. FOXO1 is required for binding of PR on IRF4, novel transcriptional regulator of endometrial stromal decidualization. Mol. Endocrinol. 29, 421–433 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. 73

    Nnamani, Mauris C. et al. A derived allosteric switch underlies the evolution of conditional cooperativity between HOXA11 and FOXO1. Cell Rep. 15, 2097–2108 (2016).

    CAS  Article  PubMed  Google Scholar 

  74. 74

    Small, C. M., Harlin-Cognato, A. D. & Jones, A. G. Functional similarity and molecular divergence of a novel reproductive transcriptome in two male-pregnant Syngnathus pipefish species. Ecol. Evol. 3, 4092–4108 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  75. 75

    Sonderegger, S., Pollheimer, J. & Knöfler, M. Wnt signalling in implantation, decidualisation and placental differentiation — review. Placenta 31, 839–847 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. 76

    Hill, J. A. Maternal–embryonic cross-talk. Ann. NY Acad. Sci. 943, 17–25 (2001).

    CAS  Article  PubMed  Google Scholar 

  77. 77

    Guzeloglu-Kayisli, O., Kayisli, U. A. & Taylor, H. S. The role of growth factors and cytokines during implantation: endocrine and paracrine interactions. Semin. Reprod. Med. 27, 062–079 (2009).

    CAS  Article  Google Scholar 

  78. 78

    Fritz, R. R., Jain, C. & Armant, R. Cell signaling in trophoblast-uterine communication. Int. J. Dev. Biol. 58, 261–271 (2014).

    CAS  Article  PubMed  Google Scholar 

  79. 79

    Murphy, B. F., Parker, S. L., Murphy, C. R. & Thompson, M. B. Placentation in the eastern water skink (Eulamprus quoyii): a placentome-like structure in a lecithotrophic lizard. J. Anat. 218, 678–689 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  80. 80

    Mor, G., Cardenas, I., Abrahams, V. & Guller, S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann. NY Acad. Sci. 1221, 80–87 (2011).

    CAS  Article  PubMed  Google Scholar 

  81. 81

    Brandley, M. C., Young, R. L., Warren, D. L., Thompson, M. B. & Wagner, G. P. Uterine gene expression in the live-bearing lizard, Chalcides ocellatus, reveals convergence of squamate reptile and mammalian pregnancy mechanisms. Genome Biol. Evol. 4, 394–411 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 82

    Schlosser, G. in International Review of Cell and Molecular Biology Vol. 283 (ed. Kwang, J. ) 129–234 (Academic, 2010).

    Google Scholar 

  83. 83

    Gilbert, S. F. & Barresi, M. J. F. Developmental Biology 10th edn (Sinaur Associates, 2016).

    Google Scholar 

  84. 84

    Chen, C.-F. et al. Development, regeneration, and evolution of feathers. Annu. Rev. Anim. Biosci. 3, 169–195 (2015).

    Article  PubMed  Google Scholar 

  85. 85

    Marcotte, M., Sharma, R. & Bouchard, M. Gene regulatory network of renal primordium development. Pediatr. Nephrol. 29, 637–644 (2014).

    Article  PubMed  Google Scholar 

  86. 86

    Le Guen, L., Marchal, S., Faure, S. & de Santa Barbara, P. Mesenchymal–epithelial interactions during digestive tract development and epithelial stem cell regeneration. Cell Mol. Life Sci. 72, 3883–3896 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. 87

    Grove, B. D. & Wourms, J. P. The follicular placenta of the viviparous fish, Heterandria formosa. I. Ultrastructure and development of the embryonic absorptive surface. J. Morphol. 209, 265–284 (1991).

    Article  PubMed  Google Scholar 

  88. 88

    Dunn, C. W., Giribet, G., Edgecombe, G. D. & Hejnol, A. Animal phylogeny and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 45, 371–395 (2014).

    Article  Google Scholar 

  89. 89

    Budd, G. E. Early animal evolution and the origins of nervous systems. Phil. Trans. R Soc. B 370, 20150037 (2015).

    Article  Google Scholar 

  90. 90

    Telford, M. J., Budd, G. E. & Philippe, H. Phylogenomic insights into animal evolution. Curr. Biol. 25, R876–R887 (2015).

    CAS  Article  PubMed  Google Scholar 

  91. 91

    Jondelius, U., Ruiz-Trillo, I., Baguñà, J. & Riutort, M. The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool. Scripta. 31, 201–215 (2002).

    Article  Google Scholar 

  92. 92

    Turner, C. L. Pseudoamnion, pseudochorion, and follicular pseudoplacenta in poeciliid fishes. J. Morphol. 67, 59–89 (1940).

    Article  Google Scholar 

  93. 93

    Griffith, O. W., Brandley, M. C., Belov, K. & Thompson, M. B. Allelic expression of mammalian imprinted genes in a matrotrophic lizard, Pseudemoia entrecasteauxii. Dev. Genes Evol. 226, 79–85 (2016).

    CAS  Article  PubMed  Google Scholar 

  94. 94

    Li, H., Elphick, M. & Shine, R. Potential targets for selection during the evolution of viviparity in cold-climate reptiles. Oecologiahttp://dx.doi.org/10.1007/s00442-00016-03752-00449 (2016).

  95. 95

    Wourms, J. P. & Lombardi, J. Reflections on the evolution of piscine viviparity. Am. Zoologist 32, 276 (1992).

  96. 96

    Van Dyke, J. U., Griffith, O. W. & Thompson, M. B. High food abundance permits the evolution of placentotrophy: evidence from a placental lizard, Pseudemoia entrecasteauxii. Am. Nat. 184, 198–210 (2014).

    Article  PubMed  Google Scholar 

  97. 97

    Trexler, J. C. & DeAngelis, D. L. Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy. Am. Nat. 162, 574–585 (2003).

    Article  PubMed  Google Scholar 

  98. 98

    Crespi, B. & Semeniuk, C. Parent–offspring conflict in the evolution of vertebrate reproductive mode. Am. Nat. 163, 635–653 (2004).

    Article  PubMed  Google Scholar 

  99. 99

    Haig, D. Placental hormones, genomic imprinting, and maternal—fetal communication. J. Evol. Biol. 9, 357–380 (1996).

    CAS  Article  Google Scholar 

  100. 100

    Garratt, M., Gaillard, J.-M., Brooks, R. C. & Lemaître, J.-F. Diversification of the eutherian placenta is associated with changes in the pace of life. Proc. Natl Acad. Sci. USA 110, 7760–7765 (2013).

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the Gaylord Donnelley Postdoctoral Environmental Fellowship to O.W.G. and a John Templeton Foundation Grant to G.P.W. (no. 54860). The authors thank T. Stewart, E. Erckenbrack, A. Chavan, C. Laing and F. Stabile for useful comments on drafts of this manuscript and M. Thompson for his encouragement to write it.

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O.W.G. wrote the manuscript. O.W.G. and G.P.W. developed ideas for, edited and approved the final version of the paper.

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Correspondence to Oliver W. Griffith.

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Griffith, O., Wagner, G. The placenta as a model for understanding the origin and evolution of vertebrate organs. Nat Ecol Evol 1, 0072 (2017). https://doi.org/10.1038/s41559-017-0072

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