Ovarian follicles shed new light on dinosaur reproduction during the transition towards birds

Abstract

The reproductive systems of living archosaurs, crocodilians and birds are very different; the derived features present in birds are inferred to have evolved within the derived archosaur group, Dinosauria, which includes Aves (the common ancestor of Archaeopteryx + living birds) as a member of the derived theropod clade, Maniraptora. Compared to Aves, crocodilians have two ovaries, prolonged folliculogenesis (maturation of ovarian follicles), large clutches and small eggs [1]. Living birds, on the other hand, nearly all have a single functional ovary and oviduct (all other amniotes have two) and rapid folliculogenesis [2]. Living birds are the most diverse Linnean class of tetrapods on the planet and within this diversity there exists a spectrum of clutch sizes and egg sizes (relative to body size) [2]. However, egg size is greater than that in crocodilians, and clutches are typically much smaller [2]. The derived reproductive system present in living birds was acquired gradually during the evolution of dinosaurs and basal birds (Fig. 1), but the timing of these changes is poorly known given the preservational constraints of the fossil record. However, the recent report of the exceptional preservation of ovarian follicles in one specimen of the basal bird Jeholornis and two enantiornithines from the Early Cretaceous Jehol Biota helps elucidate important stages in the evolution of the modern avian reproductive system as it occurred among derived paravian dinosaurs [3]. Although the extraordinary preservation of such structures has been met with some skepticism [4], neither strong counter arguments nor plausible alternative interpretations for the preserved structures have arisen [5]. Interpretations of the structures as seeds in the stomach are inconsistent