Terrestrial Origin of Viviparity in Mesozoic Marine Reptiles Indicated by Early Triassic Embryonic Fossils

Viviparity in Mesozoic marine reptiles has traditionally been considered an aquatic adaptation. We report a new fossil specimen that strongly contradicts this traditional interpretation. The new specimen contains the oldest fossil embryos of Mesozoic marine reptile that are about 10 million years older than previous such records. The fossil belongs to Chaohusaurus (Reptilia, Ichthyopterygia), which is the oldest of Mesozoic marine reptiles (ca. 248 million years ago, Early Triassic). This exceptional specimen captures an articulated embryo in birth position, with its skull just emerged from the maternal pelvis. Its headfirst birth posture, which is unlikely to be a breech condition, strongly indicates a terrestrial origin of viviparity, in contrast to the traditional view. The tail-first birth posture in derived ichthyopterygians, convergent with the conditions in whales and sea cows, therefore is a secondary feature. The unequivocally marine origin of viviparity is so far not known among amniotes, a subset of vertebrate animals comprising mammals and reptiles, including birds. Therefore, obligate marine amniotes appear to have evolved almost exclusively from viviparous land ancestors. Viviparous land reptiles most likely appeared much earlier than currently thought, at least as early as the recovery phase from the end-Permian mass extinction.

The maternal specimen with three embryos.  Color coding indicates: black, maternal vertebral column, including neural and haemal spines; blue, maternal pelvis and hind flipper; green, maternal ribs and gastralia. Embryos 1 and 2 are in orange and yellow, respectively, whereas neonate 1 is in red. Scale bar is 1 cm. Abbreviations: i-v, metatarsals; 4, fourth distal tarsal; a, astragalus; c, calcaneum; cr, caudal rib; cv, caudal vertebra; d, dentary; fe, femur; fi, fibula; h, haemal spine; il, ilium; is, ischium; pb, pubis; pm, premaxilla; sr, sacral rib; sv, sacral vertebra; and ti, tibia. See fig. S2 for a high resolution image.  doi:10.1371/journal.pone.0088640.g002

The maternal specimen with three embryos.
Color coding indicates: black, maternal vertebral column, including neural and haemal spines; blue, maternal pelvis and hind flipper; green, maternal ribs and gastralia. Embryos 1 and 2 are in orange and yellow, respectively, whereas neonate 1 is in red. Scale bar is 1 cm. Abbreviations: i-v, metatarsals; 4, fourth distal tarsal; a, astragalus; c, calcaneum; cr, caudal rib; cv, caudal vertebra; d, dentary; fe, femur; fi, fibula; h, haemal spine; il, ilium; is, ischium; pb, pubis; pm, premaxilla; sr, sacral rib; sv, sacral vertebra; and ti, tibia. See fig. S2 for a high resolution image.
doi:10.1371/journal.pone.0088640.g002

 

Completeness of the two skeletons used in maternal body size estimation.  (A), AGM CHS-5, a nearly complete skeleton that is almost as large as AGM I-1. (B), AGM CH-628-22, a complete skeleton that preserves the tail tip. Large scale bars are 10 cm, and short bars 2 cm.  doi:10.1371/journal.pone.0088640.g003

Completeness of the two skeletons used in maternal body size estimation.
(A), AGM CHS-5, a nearly complete skeleton that is almost as large as AGM I-1. (B), AGM CH-628-22, a complete skeleton that preserves the tail tip. Large scale bars are 10 cm, and short bars 2 cm.
doi:10.1371/journal.pone.0088640.g003

 

Stylized reconstruction of adult and embryo of Chaohusaurus in comparison to a derived ichthyopterygian.  (A), adult based on AGM I-1 and CHS-5. Rectangle indicates the approximate range preserved in AGM I-1. Colored silhouettes of embryo are placed in approximate positions of embryos 1 and 2, with embryo 3 displaced to avoid overlap with embryo 2. The extent of the maternal tail tip, in gray, is based on AGM-CH-628-22. Scleral ring is based on AGM-CHS-3. (B), embryo based on embryo 2 and neonate 1 of AGM I-1. Elements in gray are missing. (C), the derived ichthyopterygian Stenopterygius with one embryo in birth position and three in body cavity, reconstructed based on SMNS 6293 (Staatliches Museum für Naturkunde, Stüttgart, Germany). Scale bars are 5 cm. See fig. S3 for a high resolution image.  doi:10.1371/journal.pone.0088640.g004

Stylized reconstruction of adult and embryo of Chaohusaurus in comparison to a derived ichthyopterygian.
(A), adult based on AGM I-1 and CHS-5. Rectangle indicates the approximate range preserved in AGM I-1. Colored silhouettes of embryo are placed in approximate positions of embryos 1 and 2, with embryo 3 displaced to avoid overlap with embryo 2. The extent of the maternal tail tip, in gray, is based on AGM-CH-628-22. Scleral ring is based on AGM-CHS-3. (B), embryo based on embryo 2 and neonate 1 of AGM I-1. Elements in gray are missing. (C), the derived ichthyopterygian Stenopterygius with one embryo in birth position and three in body cavity, reconstructed based on SMNS 6293 (Staatliches Museum für Naturkunde, Stüttgart, Germany). Scale bars are 5 cm. See fig. S3 for a high resolution image.
doi:10.1371/journal.pone.0088640.g004

 

Citation: Motani R, Jiang D-y, Tintori A, Rieppel O, Chen G-b (2014) Terrestrial Origin of Viviparity in Mesozoic Marine Reptiles Indicated by Early Triassic Embryonic Fossils. PLoS ONE 9(2): e88640. doi:10.1371/journal.pone.0088640

Editor: Peter Dodson, University of Pennsylvania, United States of America

 

 

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