“The [fossilised] embryos are mostly in articulation and their distribution on each side indicates that female Keichousaurus hui had a pair of oviducts as in ichthyosaurs and many extant lizards.” Y. Cheng et al. (2003) Nature vol. 432, p.383

Oviparity and viviparity

Forms of vertebrate reproduction can be divided into either ‘oviparous’ (egg-laying) or ‘viviparous’ (live-bearing), as first described by Aristotle in his Historia Animalium. In egg-laying species, the developing embryo obtains nutrients from a store of yolk (termed ‘lecithotrophy’), whereas viviparity is a broad term encompassing varied divergence from simple egg retention in the female oviduct to elaboration of complex placental structures between fetal and maternal tissues. During viviparous gestation, embryos may acquire nutrients by digestion of ovum yolk (‘lecithotrophy’), intake of nutrients transferred from the mother (‘matrotrophy’), or – in certain viviparous amphibians and fish only – by consuming sibling ova or embryos in utero. Current evidence suggests that genetic and phenotypic changes essential to acquiring viviparity strongly (but not absolutely) resist reversal to oviparity. Accordingly, in this case of evolution, not only is the direction of the “tape of life” very much determined, but it is very difficult to rewind.

Viviparity in reptiles and other vertebrates

Viviparity has evolved more than 120 times in vertebrates, and surprisingly almost all of the transitions from oviparity to viviparity have occurred in the reptiles – the remaining occurrences being restricted to a few fish (sharks and rays), amphibians (certain salamanders and caecilians) and the well-known eutherian mammals, which are characterised by highly specialised placental structures for fetal nutrition. Over 85% of reptile species are oviparous, and yet viviparity has evolved convergently over 100 times. Most of these independent events have occurred in squamates (lizards, snakes and amphisbaenians), but the fossil record of ichthyosaurs, sauropterygians (best known, perhaps, for the plesiosaurs) and mosasaurs clearly indicates that live birth also evolved in several disparate lineages of Mesozoic marine reptiles. Here we focus on the sauropterygians…

Viviparity in sauropterygians

Sauropterygians were long-necked aquatic predators that first appeared after the Permo-Triassic extinction event around 245 Ma (million years ago). The first sauropterygians were small (less than 1m long), semi-aquatic ‘pachypleurosaurs’, which evolved into several-metre long nothosaurs and then during the Jurassic period, diversified into taxa with powerful fore- and hind-limb flippers for locomotion and bodies from a few metres to >10m in length. Jurassic taxa persisted until the Cretaceous-Tertiary extinction event 65 Ma, and included pliosaurs, ‘superpredators’ with shorter necks (e.g. Pliosaurus, Liopleurodon), pistosaurs and the well-known, long-necked plesiosaurs (e.g. Elasmosaurus). Viviparity is proposed to have been the reproductive mode of all sauropterygians, on the basis of a derived open sea habitat and possession of a mobile pelvis joint (between the illium and sacrum) that would support (or be a preadaptation for) live birth. However, definitive fossil evidence for viviparity was lacking until 2004, when Yen-nien Cheng and colleagues reported two pregnant female specimens of a pachypleurosaur called Keichousaurus hui, found in late Middle Triassic rocks in SW China. These Keichousarus females were just under 30cm in length, and their exceptional state of preservation revealed paired oviducts (similar to ichthyosaurs) containing four or six embryos, paired either side of the female vertebral column. As pachypleurosaurs were early, primitive sauropterygians, it is reasonable to assume from the Keichousaurus finding that later lineages (e.g. nothosaurs, plesiosaurs) were indeed also viviparous, although it is not impossible that some continued to return to land to lay eggs in a manner reminiscent of sea turtles.

Sauropterygians and other marine reptiles (together called the Euryapsida) are most closely related to the Lepidosauria, a group comprising the squamates (lizards, snakes, amphisbaenians) and rhynchocephalians or ‘tuataras’ (rather curious lizards endemic to New Zealand). The ancestors of euryapsids and lepidosaurs diverged from one another more than 250 million years ago, and separate lineages subsequently evolved viviparous gestation as a mode of reproduction on multiple independent occasions. Although the sauropterygians represent only one independent lineage in which the transition from oviparity to vivparity occurred, the additional existence of viviparity in other marine reptile groups and many squamate lineages highlights the striking nature of reptilian viviparity as a powerful example of convergent evolution.