, 98:739 | Cite as

A gravid lizard from the Cretaceous of China and the early history of squamate viviparity

  • Yuan Wang
  • Susan E. EvansEmail author
Original Paper


Although viviparity is most often associated with mammals, roughly one fifth of extant squamate reptiles give birth to live young. Phylogenetic analyses indicate that the trait evolved more than 100 times within Squamata, a frequency greater than that of all other vertebrate clades combined. However, there is debate as to the antiquity of the trait and, until now, the only direct fossil evidence of squamate viviparity was in Late Cretaceous mosasauroids, specialised marine lizards without modern equivalents. Here, we document viviparity in a specimen of a more generalised lizard, Yabeinosaurus, from the Early Cretaceous of China. The gravid female contains more than 15 young at a level of skeletal development corresponding to that of late embryos of living viviparous lizards. This specimen documents the first occurrence of viviparity in a fossil reptile that was largely terrestrial in life, and extends the temporal distribution of the trait in squamates by at least 30 Ma. As Yabeinosaurus occupies a relatively basal position within crown-group squamates, it suggests that the anatomical and physiological preconditions for viviparity arose early within Squamata.


Viviparity Squamata Reptilia Cretaceous China 



This work formed part of a joint Anglo-Chinese project funded by the Royal Society, London and the National Natural Science Foundation of China. Field work was also supported by grant 41072015 from the NNSF, China. Our thanks go to Jie Zhang (IVPP) for photographing the fossil and to Jack Conrad, Marcelo Sánchez-Villagra and an anonymous reviewer for comments on an earlier draft.

Supplementary material

114_2011_820_MOESM1_ESM.pdf (181 kb)
ESM 1 (PDF 181 kb)


  1. Bell GL, Sheldon MA, Lamb JP, Martin JF (1996) The first direct evidence of live birth in Mosasauridae (Squamata): exceptional preservation in the Cretaceous Pierre Shale of South Dakota. J Vertebr Paleontol Suppl 16:21A–22BGoogle Scholar
  2. Blackburn DG (2000) Reptilian viviparity: past research, future directions, and appropriate models. Comp Biochem Physiol A 127:391–409. doi: 10.1016/S1095-6433[00]00272-5 Google Scholar
  3. Blackburn DG (2006) Squamate reptiles as model organisms for the evolution of viviparity. Herpetol Monogr 20:131–146CrossRefGoogle Scholar
  4. Caldwell MW, Lee MSY (2001) Live birth in Cretaceous marine lizards (mosasauroids). Proc R Soc B 268:2397–2401. doi: 10.1098/rspb.2001.1796 PubMedCrossRefGoogle Scholar
  5. Cheng YN, Wu XC, Ji Q (2004) Triassic marine reptiles gave birth to live young. Nat 432:383–386. doi: 10.1038/nature03050 CrossRefGoogle Scholar
  6. Conrad JL (2008) Phylogeny and systematics of Squamata (Reptilia) based on morphology. Bull Am Mus Nat Hist 310:1–182. doi: 10.1206/310.1 CrossRefGoogle Scholar
  7. Davis AR, Corl A, Surget-Groba Y, Sinervo B (2011) Convergent evolution of kin-based sociality in a lizard. Proc R Soc B 278:1507–1514. doi: 10.1098/rspb.2010.1703 PubMedCrossRefGoogle Scholar
  8. Delfino M, Sánchez-Villagra MR (2010) A survey of the rock record of reptilian ontogeny. Semin Cell Dev Biol 21:432–440. doi: 10.1016/j.semcdb.2009.11.007 PubMedCrossRefGoogle Scholar
  9. Dufaure JP, Hubert J (1961) Table de developpement du lizard vivipara:Lacerta (Zootoca) vivipara Jacquin. Arch Anat Microsc Morphol Exp 50:309–328Google Scholar
  10. Endo R, Shikama T (1942) Mesozoic reptilian fauna in the Jehol mountainland, Manchoukuo. Bull CentNat Mus Manchoukuo 3:1–19Google Scholar
  11. Evans SE, Wang Y, Li C (2005) The Early Cretaceous lizard genus Yabeinosaurus from China: resolving an enigma. J Syst Palaeontol 3:319–335. doi: 10.1017/S1477201905001641 CrossRefGoogle Scholar
  12. He H, Wang X, Zhou Z, Wang F, Boven A, Shi G, Zhu R (2004) Timing of the Jiufotang Formation (Jehol Group) in Liaoning, northeastern China and its implications. Geophys Res Lett 31:L12605. doi: 10.1029/2004GL019790 CrossRefGoogle Scholar
  13. Hugi J, Mitgutsch C, Sánchez-Villagra MR (2010) Chondrogenic and ossification patterns and sequences in White’s skink Liopholis whitii (Scincidae, Reptilia). Zoosyst Evol 86:21–32. doi: 10.1002/zoos.200900011 CrossRefGoogle Scholar
  14. Ji S, Lu LW, Bo HC (2001) New material of Yabeinosaurus tenuis (Lacertilia). Land and Resources 2001(3):41–43, In ChineseGoogle Scholar
  15. Ji Q, Wu XC, Cheng YN (2010) Cretaceous choristoderan reptiles gave birth to live young. Naturwiss 97:423–428. doi: 10.1007/s00114-010-0654-2 PubMedCrossRefGoogle Scholar
  16. Lee MSY, Shine R (1998) Reptilian viviparity and Dollo’s Law. Evol 52:1441–1450CrossRefGoogle Scholar
  17. Maisano JA (2001) A survey of state of ossification in neonatal squamates. Herpetol Monogr 15:135–157CrossRefGoogle Scholar
  18. Mattison C (1992) Lizards of the world. Blandford, LondonGoogle Scholar
  19. Maxwell EE, Caldwell MW (2003) First record of live birth in Cretaceous ichthyosaurs: closing an 80 million year gap. Proc R Soc Lond B 270(Suppl 1):S104–S107. doi: 10.1098/rsbl.2003.0029 CrossRefGoogle Scholar
  20. Organ CL, Janes DE, Meade A, Pagel M (2009) Genotypic sex determination enabled adaptive radiations of extinct marine reptiles. Nat 461:389–392. doi: 10.1038/nature08350 CrossRefGoogle Scholar
  21. Renesto S, Lombardo C, Tintori A, Danini G (2003) Nothosaurid embryos from the Middle Triassic of Northern Italy: an insight into the viviparity of nothosaurs? J Vertebr Paleontol 23:957–960. doi: 10.1671/1840-21 CrossRefGoogle Scholar
  22. Rieppel O (1992) Studies on skeleton formation in reptiles. III. Patterns of ossification in the skeleton of Lacerta vivipara Jacquin (Reptilia, Squamata). Fieldiana (Zool) 68:1–25Google Scholar
  23. Rieppel O (1994) Studies on skeleton formation in reptiles. Patterns of ossification in the skeleton of Lacerta agilis exigua Eichwald (Reptilia, Squamata). J Herpetol 28:145–153CrossRefGoogle Scholar
  24. Robert KA, Thompson MB (2010) Viviparity and temperature dependent sex determination. Sex Develop 4:119–128. doi: 10.1159/000260373 CrossRefGoogle Scholar
  25. Schulte JA II, Moreno-Roark F (2010) Live birth among iguanian lizards predates Pliocene–Pleistocene glaciations. Biol Lett 6:216–218. doi: 10.1098/rsbl.2009.0707 PubMedCrossRefGoogle Scholar
  26. Shine R (1985) The evolution of viviparity in reptiles: an ecological analysis. In: Gans C, Billet F (eds) Biology of the Reptilia, vol. 15. Wiley, New York, pp 605–694Google Scholar
  27. Swisher CC III, Wang YQ, Wang XL, Xu X, Wang Y (1999) Cretaceous age for the feathered dinosaurs of Liaoning, China. Nat 400:58–61CrossRefGoogle Scholar
  28. Wang XL, Zhou ZH (2003) Mesozoic Pompei. In: Chang MM, Cheng PJ, Wang YQ, Wang Y (eds) The Jehol Biota. Shanghai Scientific and Technical, China, pp 19–35Google Scholar
  29. Wang XL, Miao D, Zhang YG (2005) Cannibalism in a semi-aquatic reptile from the Early Cretaceous of China. Chin Sci Bull 50:282–284. doi: 10.1007/bf02897540 CrossRefGoogle Scholar
  30. Wapstra E, Olsson M, Shine R, Edwards A, Swain R, Joss JMP (2004) Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc R Soc B Suppl 271:S230–S252. doi: 10.1098/rsbl.2003.0152 CrossRefGoogle Scholar
  31. Zhou Z (2006) Evolutionary radiation of the Jehol Biota: chronological and ecological perspectives. Geol J 41:377–393CrossRefGoogle Scholar
  32. Zhou Z, Zhang F, Li Z (2010) A new Lower Cretaceous bird from China and tooth reduction in early avian evolution. Proc R Soc B 277:219–227. doi: 10.1098/rspb.2009.0885 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and PaleoanthropologyChinese Academy of SciencesBeijingChina
  2. 2.Department of Cell and Developmental BiologyUniversity College LondonLondonUK

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