1932

Abstract

Viviparity (live birth) represents a significant evolutionary innovation that has emerged in hundreds of lineages of invertebrate and vertebrate animals. The evolution of this trait from the ancestral state of egg laying has involved complex morphological, behavioral, physiological, and genetic changes, which enable internal development of embryos within the female reproductive tract. Comparable changes have also occurred in oviparous, brooding species that carry developing embryos in locations other than the female reproductive tract. This review explores the taxonomic distribution of vertebrate viviparity and brooding (collectively termed pregnancy), discusses the adaptations associated with internal incubation, and examines hypotheses surrounding the evolution of pregnancy in different lineages. Understanding the mechanisms that have led to the emergence of this trait can illuminate questions about the evolution of reproductive complexity and the processes that led to the emergence of evolutionary innovations that have shaped the remarkable diversity of Earth's fauna.

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2025-02-18
2025-06-24
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Literature Cited

  1. 1.
    Blackburn DG. 2015.. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. . J. Morphol. 276::96190
    [Crossref] [Google Scholar]
  2. 2.
    Ostrovsky AN, Lidgard S, Gordon DP, Schwaha T, Genikhovich G, Ereskovsky AV. 2016.. Matrotrophy and placentation in invertebrates: a new paradigm. . Biol. Rev. 91::673711
    [Crossref] [Google Scholar]
  3. 3.
    Lefèvre CM, Sharp JA, Nicholas KR. 2010.. Evolution of lactation: ancient origin and extreme adaptations of the lactation system. . Annu. Rev. Genom. Hum. Genet. 11::21938
    [Crossref] [Google Scholar]
  4. 4.
    Whittington CM, Van Dyke JU, Liang SQT, Edwards SV, Shine R, et al. 2022.. Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy. . Biol. Rev. 97::117992
    [Crossref] [Google Scholar]
  5. 5.
    Blackburn DG. 2000.. Classification of the reproductive patterns of amniotes. . Herpetol. Monogr. 14::37177
    [Crossref] [Google Scholar]
  6. 6.
    Blackburn DG. 1994.. Review: discrepant usage of the term “ovoviviparity” in the herpetological literature. . Herpetol. J. 4::6572
    [Google Scholar]
  7. 7.
    Wourms JP. 1981.. Viviparity: the maternal-fetal relationship in fishes. . Am. Zool. 21::473515
    [Crossref] [Google Scholar]
  8. 8.
    Whittington CM, Friesen CR. 2020.. The evolution and physiology of male pregnancy in syngnathid fishes. . Biol. Rev. 95::125272
    [Crossref] [Google Scholar]
  9. 9.
    Greven H. 2011.. In Hormones and Reproduction of Vertebrates, ed. DO Norris, KH Lopez , pp. 11741. London:: Academic
    [Google Scholar]
  10. 10.
    Wetzel J, Wourms JP, Friel J. 1997.. Comparative morphology of cotylephores in Platystacus and Solenostomus: modifications of the integument for egg attachment in skin-brooding fishes. . Environ. Biol. Fishes 50::1325
    [Crossref] [Google Scholar]
  11. 11.
    Cornetti L, Menegon M, Giovine G, Heulin B, Vernesi C. 2014.. Mitochondrial and nuclear DNA survey of Zootoca vivipara across the eastern Italian alps: evolutionary relationships, historical demography and conservation implications. . PLOS ONE 9::e85912
    [Crossref] [Google Scholar]
  12. 12.
    Qualls CP, Shine R. 1996.. Reconstructing ancestral reaction norms: an example using the evolution of reptilian viviparity. . Funct. Ecol. 10::68897
    [Crossref] [Google Scholar]
  13. 13.
    Smith SA, Shine R. 1997.. Intraspecific variation in reproductive mode within the scincid lizard Saiphos equalis. . Aust. J. Zool. 45::43545
    [Crossref] [Google Scholar]
  14. 14.
    Qualls CP, Shine R. 1998.. Lerista bougainvillii, a case study for the evolution of viviparity in reptiles. . J. Evol. Biol. 11::6378
    [Google Scholar]
  15. 15.
    Recknagel H, Carruthers M, Yurchenko AA, Nokhbatolfoghahai M, Kamenos NA, et al. 2021.. The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards. . Nat. Ecol. Evol. 5::154656
    [Crossref] [Google Scholar]
  16. 16.
    Stewart JR, Ecay TW, Heulin B. 2009.. Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara. . J. Exp. Biol. 212::252024
    [Crossref] [Google Scholar]
  17. 17.
    Griffith OW, Blackburn DG, Brandley MC, Van Dyke JU, Whittington CM, Thompson MB. 2015.. 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. B 324::493503
    [Crossref] [Google Scholar]
  18. 18.
    Blackburn DG. 1995.. Saltationist and punctuated equilibrium models for the evolution of viviparity and placentation. . J. Theor. Biol. 174::199216
    [Crossref] [Google Scholar]
  19. 19.
    Shine R, Thompson MB. 2006.. Did embryonic responses to incubation conditions drive the evolution of reproductive modes in squamate reptiles?. Herpetol. Monogr. 20::15971
    [Crossref] [Google Scholar]
  20. 20.
    Qualls CP. 1996.. Influence of the evolution of viviparity on eggshell morphology in the lizard Lerista bougainvillii. . J. Morphol. 228::11925
    [Crossref] [Google Scholar]
  21. 21.
    Wourms JP. 1991.. Reproduction and development of Sebastes in the context of the evolution of piscine viviparity. . Environ. Biol. Fishes 30::11126
    [Crossref] [Google Scholar]
  22. 22.
    Wourms JP, Lombardi J. 1992.. Reflections on the evolution of piscine viviparity. . Am. Zool. 32::27693
    [Crossref] [Google Scholar]
  23. 23.
    Wourms JP, Grove BD, Lombardi J. 1988.. The maternal-embryonic relationship in viviparous fishes. . In Fish Physiology, ed. WS Hoar, DJ Randall , pp. 1134. London:: Academic
    [Google Scholar]
  24. 24.
    Mossman HW. 1937.. Comparative Morphogenesis of the Fetal Membranes and Accessory Uterine Structures. Washington, DC:: Carnegie Inst. Contrib. Embryol.
    [Google Scholar]
  25. 25.
    Whittington CM, Buddle AL, Griffith OW, Carter AM. 2022.. Embryonic specializations for vertebrate placentation. . Philos. Trans. R. Soc. B 377::20210261
    [Crossref] [Google Scholar]
  26. 26.
    Carter AM. 2018.. Comparative placentation. . In Encyclopedia of Reproduction, ed. MK Skinner , pp. 12936. London:: Academic
    [Google Scholar]
  27. 27.
    Wooding P, Burton GJ. 2008.. Fish, amphibian, bird and reptile placentation. . In Comparative Placentation: Structures, Functions and Evolution, ed. P Wooding, G Burton , pp. 8397. Berlin:: Springer Berlin Heidelberg
    [Google Scholar]
  28. 28.
    Grosser O. 1907.. Vergleichende Anatomie und Entwicklungsgeschichte der Eihäute und der Placenta. Vienna:: Wilhelm Braumüller
    [Google Scholar]
  29. 29.
    Jiang B, He Y, Elsler A, Wang S, Keating JN, et al. 2023.. Extended embryo retention and viviparity in the first amniotes. . Nat. Ecol. Evol. 7::113140
    [Crossref] [Google Scholar]
  30. 30.
    dos Reis M, Inoue J, Hasegawa M, Asher RJ, Donoghue PC, Yang Z. 2012.. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. . Proc. R. Soc. B 279::3491500
    [Crossref] [Google Scholar]
  31. 31.
    Blackburn DG, Stewart J. 2011.. Viviparity and placentation in snakes. . In Reproductive Biology and Phylogeny of Snakes, ed. RD Aldridge, DM Sever , pp. 11981. Boca Raton, FL:: CRC Press
    [Google Scholar]
  32. 32.
    Stewart JR, Blackburn DG. 2014.. In Reproductive Biology and Phylogeny of Lizards and Tuatara, ed. JL Rheubert, DS Siegel, SE Trauth , pp. 448563. Boca Raton, FL:: CRC Press
    [Google Scholar]
  33. 33.
    Stewart JR. 2013.. Fetal nutrition in lecithotrophic squamate reptiles: toward a comprehensive model for evolution of viviparity and placentation. . J. Morphol. 274::82443
    [Crossref] [Google Scholar]
  34. 34.
    Blackburn DG. 2015.. Evolution of viviparity in squamate reptiles: reversibility reconsidered. . J. Exp. Zool. B 324::47386
    [Crossref] [Google Scholar]
  35. 35.
    Blackburn DG, Hughes DF. 2024.. Phylogenetic analysis of viviparity, matrotrophy, and other reproductive patterns in chondrichthyan fishes. . Biol. Rev. 99::131456
    [Crossref] [Google Scholar]
  36. 36.
    Buddle AL, Van Dyke JU, Thompson MB, Simpfendorfer CA, Whittington CM. 2019.. Evolution of placentotrophy: using viviparous sharks as a model to understand vertebrate placental evolution. . Mar. Freshw. Res. 70::90824
    [Crossref] [Google Scholar]
  37. 37.
    Renesto S, Stockar R. 2009.. Exceptional preservation of embryos in the actinopterygian Saurichthys from the Middle Triassic of Monte San Giorgio, Switzerland. . Swiss J. Geosci. 102::32330
    [Crossref] [Google Scholar]
  38. 38.
    Wake MH. 1985.. Oviduct structure and function in non-mammalian vertebrates. . Forschritte Zool. 30::42735
    [Google Scholar]
  39. 39.
    Wourms JP, Atz JW, Stribling MD. 1991.. Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae. . Environ. Biol. Fishes 32::22548
    [Crossref] [Google Scholar]
  40. 40.
    Heemstra PC, Greenwood PH. 1992.. New observations on the visceral anatomy of the late-term fetuses of the living coelacanth fish and the oophagy controversy. . Proc. R. Soc. Lond. B 249::4955
    [Crossref] [Google Scholar]
  41. 41.
    Long JA, Trinajstic K, Young GC, Senden T. 2008.. Live birth in the Devonian period. . Nature 453::65052
    [Crossref] [Google Scholar]
  42. 42.
    Grogan ED, Lund R. 2011.. Superfoetative viviparity in a Carboniferous chondrichthyan and reproduction in early gnathostomes. . Zool. J. Linn. Soc. 161::58794
    [Crossref] [Google Scholar]
  43. 43.
    Blackburn DG, Sidor CA. 2014.. Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles. . Int. J. Dev. Biol. 58::93548
    [Crossref] [Google Scholar]
  44. 44.
    Meier R, Kotrba M, Ferrar P. 1999.. Ovoviviparity and viviparity in the Diptera. . Biol. Rev. 74::199258
    [Crossref] [Google Scholar]
  45. 45.
    Shine R. 2014.. Evolution of an evolutionary hypothesis: a history of changing ideas about the adaptive significance of viviparity in reptiles. . J. Herpetol. 48::14761
    [Crossref] [Google Scholar]
  46. 46.
    Tinkle DW, Gibbons JW. 1977.. The distribution and evolution of viviparity in reptiles. Misc. Publ., Mus. Zool., Univ. Mich., Ann Arbor:
    [Google Scholar]
  47. 47.
    Shine R, Bull JJ. 1979.. The evolution of live-bearing in lizards and snakes. . Am. Nat. 113::90523
    [Crossref] [Google Scholar]
  48. 48.
    Meiri S, Feldman A, Schwarz R, Shine R. 2020.. Viviparity does not affect the numbers and sizes of reptile offspring. . J. Anim. Ecol. 89::36069
    [Crossref] [Google Scholar]
  49. 49.
    Meiri S, Brown JH, Sibly RM. 2012.. The ecology of lizard reproductive output. . Glob. Ecol. Biogeogr. 21::592602
    [Crossref] [Google Scholar]
  50. 50.
    Recknagel H, Elmer KR. 2019.. Differential reproductive investment in co-occurring oviparous and viviparous common lizards (Zootoca vivipara) and implications for life-history trade-offs with viviparity. . Oecologia 190::8598
    [Crossref] [Google Scholar]
  51. 51.
    Hulthén K, Hill JS, Jenkins MR, Langerhans RB. 2021.. Predation and resource availability interact to drive life-history evolution in an adaptive radiation of livebearing fish. . Front. Ecol. Evol. 9::619277
    [Crossref] [Google Scholar]
  52. 52.
    Zimin A, Zimin SV, Shine R, Avila L, Bauer A, et al. 2022.. A global analysis of viviparity in squamates highlights its prevalence in cold climates. . Glob. Ecol. Biogeogr. 31::243752
    [Crossref] [Google Scholar]
  53. 53.
    Liedtke HC, Müller H, Hafner J, Penner J, Gower DJ, et al. 2017.. Terrestrial reproduction as an adaptation to steep terrain in African toads. . Proc. R. Soc. B 284::20162598
    [Crossref] [Google Scholar]
  54. 54.
    Watson CM, Cox CL. 2021.. Elevation, oxygen, and the origins of viviparity. . J. Exp. Zool. B 336::45769
    [Crossref] [Google Scholar]
  55. 55.
    Pincheira-Donoso D, Tregenza T, Witt MJ, Hodgson DJ. 2013.. The evolution of viviparity opens opportunities for lizard radiation but drives it into a climatic cul-de-sac. . Glob. Ecol. Biogeogr. 22::85767
    [Crossref] [Google Scholar]
  56. 56.
    Shine R. 2002.. Reconstructing an adaptationist scenario: What selective forces favor the evolution of viviparity in montane reptiles?. Am. Nat. 160::58293
    [Crossref] [Google Scholar]
  57. 57.
    Wang Z, Lu HL, Ma L, Ji X. 2014.. Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. . Oecologia 174::63949
    [Crossref] [Google Scholar]
  58. 58.
    Ma L, Buckley LB, Huey RB, Du W-G. 2018.. A global test of the cold-climate hypothesis for the evolution of viviparity of squamate reptiles. . Glob. Ecol. Biogeogr. 27::67989
    [Crossref] [Google Scholar]
  59. 59.
    Kearney MR, Porter WP. 2017.. NicheMapR—an R package for biophysical modelling: the microclimate model. . Ecography 40::66474
    [Crossref] [Google Scholar]
  60. 60.
    Brooks GC, Kindsvater HK. 2022.. Early development drives variation in amphibian vulnerability to global change. . Front. Ecol. Evol. 10::813414
    [Crossref] [Google Scholar]
  61. 61.
    Velo-Anton G, Zamudio KR, Cordero-Rivera A. 2012.. Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra). . Heredity 108::41018
    [Crossref] [Google Scholar]
  62. 62.
    Horreo JL, Jiménez-Valverde A, Fitze PS. 2021.. Climatic niche differences among Zootoca vivipara clades with different parity modes: implications for the evolution and maintenance of viviparity. . Front. Zool. 18::32
    [Crossref] [Google Scholar]
  63. 63.
    Feldman A, Bauer AM, Castro-Herrera F, Chirio L, Das I, et al. 2015.. The geography of snake reproductive mode: a global analysis of the evolution of snake viviparity. . Glob. Ecol. Biogeogr. 24::143342
    [Crossref] [Google Scholar]
  64. 64.
    Shine R. 2002.. An empirical test of the ‘predictability’ hypothesis for the evolution of viviparity in reptiles. . J. Evol. Biol. 15::55360
    [Crossref] [Google Scholar]
  65. 65.
    Hirshfield MF, Tinkle DW. 1975.. Natural selection and the evolution of reproductive effort. . PNAS 72::222731
    [Crossref] [Google Scholar]
  66. 66.
    Shine R. 1995.. A new hypothesis for the evolution of viviparity in reptiles. . Am. Nat. 145::80923
    [Crossref] [Google Scholar]
  67. 67.
    Foucart T, Heulin B, Lourdais O. 2018.. Small changes, big benefits: testing the significance of maternal thermoregulation in a lizard with extended egg retention. . Biol. J. Linn. Soc. 125::28091
    [Crossref] [Google Scholar]
  68. 68.
    Gao JF, Qu YF, Luo LG, Ji X. 2010.. Evolution of reptilian viviparity: a test of the maternal manipulation hypothesis in a temperate snake, Gloydius brevicaudus (Viperidae). . Zool. Sci. 27::24855
    [Crossref] [Google Scholar]
  69. 69.
    Webb JK, Shine R, Christian KA. 2006.. The adaptive significance of reptilian viviparity in the tropics: testing the maternal manipulation hypothesis. . Evolution 60::11522
    [Google Scholar]
  70. 70.
    Li H, Qu YF, Hu RB, Ji X. 2009.. Evolution of viviparity in cold-climate lizards: testing the maternal manipulation hypothesis. . Evol. Ecol. 23::77790
    [Crossref] [Google Scholar]
  71. 71.
    Ji X, Lin CX, Lin LH, Qiu QB, Du Y. 2007.. Evolution of viviparity in warm-climate lizards: an experimental test of the maternal manipulation hypothesis. . J. Evol. Biol. 20::103745
    [Crossref] [Google Scholar]
  72. 72.
    Pettersen AK, Feiner N, Noble DWA, While GM, Uller T, Cornwallis CK. 2023.. Maternal behavioral thermoregulation facilitated evolutionary transitions from egg laying to live birth. . Evol. Lett. 7::35160
    [Crossref] [Google Scholar]
  73. 73.
    Shine R. 2004.. Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures?. Evolution 58::180918
    [Google Scholar]
  74. 74.
    Schwarzkopf L, Andrews RM. 2012.. Are moms manipulative or just selfish? Evaluating the “maternal manipulation hypothesis” and implications for life-history studies of reptiles. . Herpetologica 68::14759
    [Crossref] [Google Scholar]
  75. 75.
    Schwarzkopf L, Andrews RM. 2012.. “ Selfish mothers” use “maternal manipulation” to maximize lifetime reproductive success. . Herpetologica 68::30811
    [Crossref] [Google Scholar]
  76. 76.
    Dayananda B, Ibargüengoytía N, Whiting MJ, Webb JK. 2017.. Effects of pregnancy on body temperature and locomotor performance of velvet geckos. . J. Therm. Biol. 65::6468
    [Crossref] [Google Scholar]
  77. 77.
    Shine R. 2012.. Manipulative mothers and selective forces: the effects of reproduction on thermoregulation in reptiles. . Herpetologica 68::28998
    [Crossref] [Google Scholar]
  78. 78.
    Saldívar-Lemus Y, Macías Garcia C. 2022.. Conflict and the evolution of viviparity in vertebrates. . Behav. Ecol. Sociobiol. 76::68
    [Crossref] [Google Scholar]
  79. 79.
    Crespi B, Semeniuk C. 2004.. Parent-offspring conflict in the evolution of vertebrate reproductive mode. . Am. Nat. 163::63553
    [Crossref] [Google Scholar]
  80. 80.
    Gillespie JM, McClintock JB. 2007.. Brooding in echinoderms: How can modern experimental techniques add to our historical perspective?. J. Exp. Mar. Biol. Ecol. 342::191201
    [Crossref] [Google Scholar]
  81. 81.
    Ringler E, Rojas B, Stynoski JL, Schulte LM. 2023.. What amphibians can teach us about the evolution of parental care. . Annu. Rev. Ecol. Evol. Syst. 54::4362
    [Crossref] [Google Scholar]
  82. 82.
    Zamudio KR, Bell RC, Nali RC, Haddad CFB, Prado CPA. 2016.. Polyandry, predation, and the evolution of frog reproductive modes. . Am. Nat. 188::S41S61
    [Crossref] [Google Scholar]
  83. 83.
    Lange L, Bégué L, Brischoux F, Lourdais O. 2021.. The costs of being a good dad: egg-carrying and clutch size impair locomotor performance in male midwife toads (Alytes obstetricans). . Biol. J. Linn. Soc. 132::27082
    [Crossref] [Google Scholar]
  84. 84.
    Lange L, Brischoux F, Lourdais O. 2022.. Benefits of paternal thermoregulation: Male midwife toads select warmer temperature to shorten embryonic development. . Behav. Ecol. Sociobiol. 76::27082
    [Crossref] [Google Scholar]
  85. 85.
    Schulte LM, Ringler E, Rojas B, Stynoski JL. 2020.. Developments in amphibian parental care research: history, present advances, and future perspectives. . Herpetol. Monogr. 34::7197
    [Crossref] [Google Scholar]
  86. 86.
    Ma L, Sun BJ, Li SR, Hao X, Bi JH, Du WG. 2018.. The vulnerability of developing embryos to simulated climate warming differs between sympatric desert lizards. . J. Exp. Zool. A 329::25261
    [Crossref] [Google Scholar]
  87. 87.
    Wake MH. 1993.. Evolution of oviductal gestation in amphibians. . J. Exp. Zool. 266::394413
    [Crossref] [Google Scholar]
  88. 88.
    Fishelson L, Gon O, Holdengreber V, Delarea Y. 2006.. Comparative morphology and cytology of the male sperm-transmission organs in viviparous species of clinid fishes (Clinidae: Teleostei, Perciformes). . J. Morphol. 267::140614
    [Crossref] [Google Scholar]
  89. 89.
    Rosen DE, Gordon M. 1953.. Functional anatomy and evolution of male genitalia in poeciliid fishes. . Zoologica 38::147
    [Google Scholar]
  90. 90.
    Lampert KP, Blassmann K, Hissmann K, Schauer J, Shunula P, et al. 2013.. Single-male paternity in coelacanths. . Nat. Commun. 4::2488
    [Crossref] [Google Scholar]
  91. 91.
    Packard GC, Tracy CR, Roth JJ. 1977.. The physiological ecology of reptilian eggs and embryos and the evolution of viviparity within the class Reptilia. . Biol. Rev. 52::71105
    [Crossref] [Google Scholar]
  92. 92.
    Oppenheimer JR. 1970.. Mouthbreeding in fishes. . Anim. Behav. 18::493503
    [Crossref] [Google Scholar]
  93. 93.
    Krogh A. 1919.. The rate of diffusion of gases through animal tissues, with some remarks on the coefficient of invasion. . J. Physiol. 52::391408
    [Crossref] [Google Scholar]
  94. 94.
    Andrews RM, Mathies T. 2000.. Natural history of reptilian development: constraints on the evolution of viviparity. . BioScience 50::22738
    [Crossref] [Google Scholar]
  95. 95.
    Buddle AL, Van Dyke JU, Thompson MB, Simpfendorfer CA, Murphy CR, et al. 2022.. Structure and permeability of the egg capsule of the placental Australian sharpnose shark, Rhizoprionodon taylori. . J. Comp. Physiol. B 192::26373
    [Crossref] [Google Scholar]
  96. 96.
    Stewart JR, Mathieson AN, Ecay TW, Herbert JF, Parker SL, Thompson MB. 2010.. Uterine and eggshell structure and histochemistry in a lizard with prolonged uterine egg retention (Lacertilia, Scincidae, Saiphos). . J. Morphol. 271::134251
    [Crossref] [Google Scholar]
  97. 97.
    Buddle AL, Otway NM, Van Dyke JU, Thompson MB, Murphy CR, et al. 2020.. Structural changes to the uterus of the dwarf ornate wobbegong shark (Orectolobus ornatus) during pregnancy. . J. Morphol. 281::42837
    [Crossref] [Google Scholar]
  98. 98.
    Parker SL, Manconi F, Murphy CR, Thompson MB. 2010.. Uterine and placental angiogenesis in the Australian skinks, Ctenotus taeniolatus, and Saiphos equalis. . Anat. Record 293::82938
    [Crossref] [Google Scholar]
  99. 99.
    Jollie WP, Jollie LG. 1964.. The fine structure of the ovarian follicle of the ovoviviparous poeciliid fish, Lebistes reticulatus. II. Formation of follicular pseudoplacenta. . J. Morphol. 114::50325
    [Crossref] [Google Scholar]
  100. 100.
    Grigg GC, Harlow P. 1981.. A fetal-maternal shift of blood oxygen affinity in an Australian viviparous lizard, Sphenomorphus quoyii (Reptilia, Scincidae). . J. Comp. Physiol. 142::49599
    [Crossref] [Google Scholar]
  101. 101.
    Ingermann RL, Terwilliger RC. 1981.. Oxygen affinities of maternal and fetal hemoglobins of the viviparous seaperch, Embiotoca lateralis. . J. Comp. Physiol. 142::52331
    [Crossref] [Google Scholar]
  102. 102.
    Wake MH. 1977.. Fetal maintenance and its evolutionary significance in the Amphibia: Gymnophiona. . J. Herpetol. 11::37986
    [Crossref] [Google Scholar]
  103. 103.
    Lombardi J, Wourms JP. 1985.. The trophotaenial placenta of a viviparous goodeid fish. II. Ultrastructure of trophotaeniae, the embryonic component. . J. Morphol. 184::293309
    [Crossref] [Google Scholar]
  104. 104.
    Ellis MT, Otway NM. 2011.. Uterine fluid composition of the dwarf ornate wobbegong shark (Orectolobus ornatus) during gestation. . Mar. Freshw. Res. 62::57682
    [Crossref] [Google Scholar]
  105. 105.
    Tomita T, Cotton C, Toda M. 2015.. Ultrasound and physical models shed light on the respiratory system of embryonic dogfishes. . Zoology 119::3641
    [Crossref] [Google Scholar]
  106. 106.
    Tomita T, Murakumo K, Ueda K, Ashida H, Furuyama R. 2018.. Locomotion is not a privilege after birth: ultrasound images of viviparous shark embryos swimming from one uterus to the other. . Ethology 125::12226
    [Crossref] [Google Scholar]
  107. 107.
    Male V. 2020.. Medawar and the immunological paradox of pregnancy: in context. . Oxford Open Immunol. 2::iqaa006
    [Crossref] [Google Scholar]
  108. 108.
    Paulesu L. 2013.. Materno-fetal immunotolerance: an evolutionary view. . J. Siena Acad. Sci. 5::1122
    [Crossref] [Google Scholar]
  109. 109.
    Stadtmauer DJ, Wagner GP. 2020.. Cooperative inflammation: the recruitment of inflammatory signaling in marsupial and eutherian pregnancy. . J. Reprod. Immunol. 137::102626
    [Crossref] [Google Scholar]
  110. 110.
    Chavan AR, Griffith OW, Stadtmauer D, Maziarz J, Pavlicev M, et al. 2020.. Evolution of embryo implantation was enabled by the origin of decidual stromal cells in eutherian mammals. . Mol. Biol. Evol. 38::106074
    [Crossref] [Google Scholar]
  111. 111.
    Moffett A, Shreeve N. 2023.. Local immune recognition of trophoblast in early human pregnancy: controversies and questions. . Nat. Rev. Immunol. 23::22235
    [Crossref] [Google Scholar]
  112. 112.
    Brandley MC, Young RL, Warren DL, Thompson MB, Wagner GP. 2012.. Uterine gene expression in the live-bearing lizard, Chalcides ocellatus, reveals convergence of squamate reptile and mammalian pregnancy mechanisms. . Genome Biol. Evol. 4::394411
    [Crossref] [Google Scholar]
  113. 113.
    Foster CSP, Thompson MB, Van Dyke JU, Brandley MC, Whittington CM. 2020.. Emergence of an evolutionary innovation: gene expression differences associated with the transition between oviparity and viviparity. . Mol. Ecol. 29::131527
    [Crossref] [Google Scholar]
  114. 114.
    Gao W, Sun Y-B, Zhou W-W, Xiong Z-J, Chen L, et al. 2019.. Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity. . PNAS 116::364655
    [Crossref] [Google Scholar]
  115. 115.
    Graham SP, Earley RL, Guyer C, Mendonça MT. 2011.. Innate immune performance and steroid hormone profiles of pregnant versus nonpregnant cottonmouth snakes (Agkistrodon piscivorus). . Gen. Comp. Endocrinol. 174::34853
    [Crossref] [Google Scholar]
  116. 116.
    Foster CSP, Van Dyke JU, Thompson MB, Smith NMA, Simpfendorfer CA, et al. 2022.. Different genes are recruited during convergent evolution of pregnancy and the placenta. . Mol. Biol. Evol. 39::msac077
    [Crossref] [Google Scholar]
  117. 117.
    Haines AN, Flajnik MF, Wourms JP. 2006.. Histology and immunology of the placenta in the Atlantic sharpnose shark, Rhizoprionodon terraenovae. . Placenta 27::111423
    [Crossref] [Google Scholar]
  118. 118.
    Cateni C, Paulesu L, Bigliardi E, Hamlett WC. 2003.. The interleukin 1 (IL-1) system in the uteroplacental complex of a cartilaginous fish, the smoothhound shark, Mustelus canis. . Reprod. Biol. Endocrinol. 1::25
    [Crossref] [Google Scholar]
  119. 119.
    Jantra S, Bigliardi E, Brizzi R, Ietta F, Bechi N, Paulesu L. 2007.. Interleukin 1 in oviductal tissues of viviparous, oviparous, and ovuliparous species of amphibians. . Biol. Reprod. 76::100915
    [Crossref] [Google Scholar]
  120. 120.
    Exbrayat J, Pujol P, Hraoui-Bloquet S. 1995.. First observations on the immunological materno-foetal relationships in Typhlonectes compressicaudus, a viviparous Gymnophionan Amphibia. . Sci. Herpetol. 1995::27173
    [Google Scholar]
  121. 121.
    Gilmore RG Jr., Putz O, Dodrill JW. 2011.. Oophagy, intrauterine cannibalism and reproductive strategy in lamnoid sharks. . In Reproductive Biology and Phylogeny of Chondrichthyes, ed. WC Hamlett , pp. 44572. Boca Raton, FL:: CRC Press
    [Google Scholar]
  122. 122.
    Thompson MB, Stewart JR, Speake BK. 2000.. Comparison of nutrient transport across the placenta of lizards differing in placental complexity. . Comp. Biochem. Physiol. A 127::46979
    [Crossref] [Google Scholar]
  123. 123.
    Knight FM, Lombardi J, Wourms JP, Burns JR. 1985.. Follicular placenta and embryonic growth of the viviparous four-eyed fish (Anableps). . J. Morphol. 185::13142
    [Crossref] [Google Scholar]
  124. 124.
    Gilchrist JDF. 1905.. The development of South African fishes. Part II. . Mar. Investig. S. Afr. 3::13167
    [Google Scholar]
  125. 125.
    Meisner AD, Burns JR. 1997.. Viviparity in the halfbeak genera Dermogenys and Nomorhamphus (Teleostei: Hemiramphidae). . J. Morphol. 234::295317
    [Crossref] [Google Scholar]
  126. 126.
    Buckley D, Alcobendas M, García-París M, Wake MH. 2007.. Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. . Evol. Dev. 9::10515
    [Crossref] [Google Scholar]
  127. 127.
    Exbrayat J-M, Hraoui-Bloquet S. 2006.. Viviparity in Typhlonectes compressicauda. . In Reproductive Biology and Phylogeny of Gymnophiona (Caecilians), ed. J-M Exbrayat , pp. 32558. Boca Raton, FL:: CRC Press
    [Google Scholar]
  128. 128.
    Reznick DN, Mateos M, Springer MS. 2002.. Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. . Science 298::101820
    [Crossref] [Google Scholar]
  129. 129.
    Skalkos Z, Van Dyke JU, Whittington CM. 2023.. Distinguishing between embryonic provisioning strategies in teleost fishes using a threshold value for parentotrophy. . Biomolecules 13::166
    [Crossref] [Google Scholar]
  130. 130.
    Frazer HA, Ellis M, Huveneers C. 2012.. Can a threshold value be used to classify chondrichthyan reproductive modes: systematic review and validation using an oviparous species. . PLOS ONE 7::e50196
    [Crossref] [Google Scholar]
  131. 131.
    Wetzel J, Wourms J. 1995.. Adaptations for reproduction and development in the skin-brooding ghost pipefishes. , Solenostomus. Environ. Biol. Fishes 44::36384
    [Crossref] [Google Scholar]
  132. 132.
    Berra TM, Humphrey JD. 2002.. Gross anatomy and histology of the hook and skin of forehead brooding male nurseryfish, Kurtus gulliveri, from northern Australia. . Environ. Biol. Fishes 65::26370
    [Crossref] [Google Scholar]
  133. 133.
    Lombardi J. 1998.. Comparative Vertebrate Reproduction. New York:: Springer Sci. Bus. Media
    [Google Scholar]
  134. 134.
    Skalkos ZMG, Van Dyke JU, Whittington CM. 2020.. Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis. . J. Comp. Physiol. B 190::54756
    [Crossref] [Google Scholar]
  135. 135.
    Dudley JS, Hannaford P, Dowland SN, Lindsay LA, Thompson MB, et al. 2021.. Structural changes to the brood pouch of male pregnant seahorses (Hippocampus abdominalis) facilitate exchange between father and embryos. . Placenta 114::11523
    [Crossref] [Google Scholar]
  136. 136.
    Skalkos Z, Van Dyke J, Dowland S, Whittington C. 2024.. Paternal protein provisioning to embryos during male seahorse pregnancy. . Reproduction 167::e230420
    [Crossref] [Google Scholar]
  137. 137.
    del Pino EM. 2018.. The extraordinary biology and development of marsupial frogs (Hemiphractidae) in comparison with fish, mammals, birds, amphibians and other animals. . Mech. Dev. 154::211
    [Crossref] [Google Scholar]
  138. 138.
    Warne RW, Catenazzi A. 2016.. Pouch brooding marsupial frogs transfer nutrients to developing embryos. . Biol. Lett. 12::20160673
    [Crossref] [Google Scholar]
  139. 139.
    Goicoechea O, Garrido O, Jorquera B. 1986.. Evidence for a trophic paternal-larval relationship in the frog Rhinoderma darwinii. . J. Herpetol. 20::16878
    [Crossref] [Google Scholar]
  140. 140.
    van Kruistum H, Nijland R, Reznick DN, Groenen MAM, Megens H-J, Pollux BJA. 2021.. Parallel genomic changes drive repeated evolution of placentas in live-bearing fish. . Mol. Biol. Evol. 38::262738
    [Crossref] [Google Scholar]
  141. 141.
    Guernsey MW, van Kruistum H, Reznick DN, Pollux BJA, Baker JC. 2020.. Molecular signatures of placentation and secretion uncovered in Poeciliopsis maternal follicles. . Mol. Biol. Evol. 37::267990
    [Crossref] [Google Scholar]
  142. 142.
    Whittington CM, Griffith OW, Qi W, Thompson MB, Wilson AB. 2015.. Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. . Mol. Biol. Evol. 32::311431
    [Google Scholar]
  143. 143.
    Parker J, Dubin A, Schneider R, Wagner KS, Jentoft S, et al. 2022.. Immunological tolerance in the evolution of male pregnancy. . Mol. Ecol. 32::81940
    [Crossref] [Google Scholar]
  144. 144.
    Yusuf LH, Saldívar Lemus Y, Thorpe P, Macías Garcia C, Ritchie MG. 2023.. Genomic signatures associated with transitions to viviparity in Cyprinodontiformes. . Mol. Biol. Evol. 40::msad208
    [Crossref] [Google Scholar]
  145. 145.
    Eastment RV, Wong BBM, McGee MD. 2024.. Convergent genomic signatures associated with vertebrate viviparity. . BMC Biol. 22::34
    [Crossref] [Google Scholar]
  146. 146.
    Mika K, Whittington CM, McAllan BM, Lynch VJ. 2022.. Gene expression phylogenies and ancestral transcriptome reconstruction resolves major transitions in the origins of pregnancy. . eLife 11::e74297
    [Crossref] [Google Scholar]
  147. 147.
    Arutyunyan A, Roberts K, Troulé K, Wong FCK, Sheridan MA, et al. 2023.. Spatial multiomics map of trophoblast development in early pregnancy. . Nature 616::14351
    [Crossref] [Google Scholar]
  148. 148.
    Hemberger M, Dean W. 2023.. The placenta: epigenetic insights into trophoblast developmental models of a generation-bridging organ with long-lasting impact on lifelong health. . Physiol. Rev. 103::252360
    [Crossref] [Google Scholar]
  149. 149.
    Laundon D, Gostling NJ, Sengers BG, Chavatte-Palmer P, Lewis RM. 2023.. Placental evolution from a three-dimensional and multiscale structural perspective. . Evolution 78::1325
    [Crossref] [Google Scholar]
  150. 150.
    Dudley JS, Paul JW, Teh V, Mackenzie TE, Butler TA, et al. 2022.. Seahorse brood pouch morphology and control of male parturition in Hippocampus abdominalis. . Placenta 127::8894
    [Crossref] [Google Scholar]
  151. 151.
    Whittington CM. 2021.. Evolution of lizard viviparity. . Nat. Ecol. Evol. 5::147677
    [Crossref] [Google Scholar]
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