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

Abstract

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.

Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles

“…Such documentation of viviparity likewise extends from the Early Jurassic (McGowan, 1979;Deeming et al, 1993;Dal Sasso and Pinna, 1996;Lomax and Massare, 2012;Maxwell, 2012) and Late Jurassic (O'Keefe et al, 2009) into the Cretaceous (Kear et al, 2003;Maxwell and Caldwell, 2003;Kear and Zammit, 2014). Viviparity was recently discovered in the basal ichthyopterygian Chaohusaurus (Motani et al, 2014). This finding extends the record of ichthyopterygian viviparity back another 10 million years.…”

“…Easily recognizable from their dolphin-like body shape, they ranged from small (< 1m long), snub-nosed forms through enormous, long snouted types that reached as much as 20m in body length (Ellis, 2003;Motani, 2005). Ichthyosaurs are combined with basal forms of the Early Triassic in the clade Ichthyopterygia (Motani et al, 2014).…”

Integrating developmental biology and the fossil record of reptiles

“…The fossil record does not give an answer to this problem because fossilized placentae are not yet known in extinct reptiles (although one example exists in the Devonian placoderm fish), even in well-preserved fossils due to the absence of relevant soft tissues (e.g. Motani et al, 2014; see a more thorough review in Blackburn and Sidor 2015).…”

“…Our knowledge about evolution of their development increased in recent years thanks to the remarkable findings of embryos inside female skeletons (e.g. Ji et al, 2010;Motani et al, 2014) or within mineralized eggshells (e.g. Chiappe et al, 2004;Kundrát et al, 2008;Araújo et al, 2013), sometimes even with preserved organic remains (Reisz et al, 2013), and development of new research techniques which allow us to investigate embryonic fossils which were previously inaccessible, like embryos in ovo (e.g.…”

“…Fossilized embryos, juveniles and adults can test hypotheses concerning the antiquity of developmental processes (e.g. Motani et al, 2014) and origin of morphological traits observed in living animals (e.g. Lyson et al, 2013).…”