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What the ovaries of dinosaurs can tell us

By Dr. Jingmai O’Connor

Understanding the internal organs of extinct animals over 100 million years old used to belong in the realm of impossibility. However, during recent decades exceptional discoveries from all over the world have revealed elusive details such as fossilized feathers, skin, and muscle. The Upper Jurassic/Lower Cretaceous Chaomidianzi Formation of Liaoning province in northeastern China has done a great deal to contribute to this wealth of biological information on extinct organisms. Here, exceptionally well-preserved specimens are the norm; feathers are preserved in numerous specimens revealing morphologies that no longer exist today, even allowing scientists to determine the color of extinct dinosaurs. Internal organs and structures such as the crop and gizzard are inferred through preservation of their contents, revealing the diet of dinosaurs and birds over 120 million year old.

More recently, an even more unlikely discovery was made: several specimens of Early Cretaceous birds preserving ovarian follicles (the largest single cells in the body, essentially egg yolks in the ovary before they are ovulated into the oviduct, joined with albumen, and shelled) preserved in place within the abdominal cavity of the body. One specimen is referred to Jeholornis, a long boney-tailed bird only more derived than Archaeopteryx, and two specimens belong to Enantiornithes, the most diverse clade of Mesozoic birds and sister group to Ornithuromorpha, the clade that includes living birds (Neornithes). Together, these three specimens sample a fairly large spectrum of basal birds, revealing early evolutionary trends in reproductive behavior within the clade. After the initial identification of three specimens, my colleagues and I searched the enormous collections of the Shandong Tianyu Museum of Nature for additional specimens, turning up several more enantiornithine specimens preserving follicles. The Collection is heavily biased towards this clade, which apparently dominated the Cretaceous both in diversity and numbers.

The now dozen or so specimens of enantiornithine preserving ovarian follicles reveal a diversity of reproductive strategies. In Neornithes there exists an incredible spectrum: from birds born nearly independent and soon able to fly (super precocial), to those born blind, naked, and entirely dependent (altricial). In living birds, the more that is invested in the individual offspring, the fewer offspring there are in a clutch, and egg size is typically larger. Prior to ovulation, the number of mature ovarian follicles is a good indicator of clutch size — allowing clutch size to be estimated in these Jehol birds. The same trade off is observed in enantiornithines, and smaller egg to body size ratios are associated with larger clutches. Although the spectrum of egg to body size ratios observed in enantiornithines does not come close to that of Neornithes, this is not surprising given the limited ecological diversity observed among Jehol enantiornithines, which are interpreted as arboreal.

Although overlooked in the initial report of the Jehol specimens, the holotype of Compsognathus longipes also was described to preserve ovarian follicles. Although not entirely preserved within the body, descriptions of this specimen are consistent with observations from Jehol specimens and we concur with the author’s interpretation that these circular structures are ovarian follicles. Compsognathus is a primitive maniraptoran and thus reveals the condition outside Paraves (birds and their close relatives). This taxon is also larger than Jeholornis, the long-tailed bird, which is in turn much larger than all Early Cretaceous enantiornithines preserving ovarian follicles. However, despite the disparity in overall body size, follicle size is comparable in all specimens, consistent with S. J. Gould’s theory of egg size conservation — the idea that body size is more easily subject to evolutionary change than the size of the egg itself. This is also observed in ratites, the living group of large flightless birds, in which the large egg of the kiwi bird is the result of the body evolving smaller size while the egg stayed the same size as in other larger ratites (e.g. the ostrich and other even larger extinct relative such as Dinornis).

While egg size is apparently more difficult to change due to biological restrictions, body size is reduced in the theropod lineage that leads to Aves, which apparently facilitated the evolution of flight. As body size decreases around the egg size, the egg becomes increasingly larger and more massive relative to the body. At the same time, a trend in flying organisms is to reduce the weight of the body. Birds are unique among amniotes in that they typically only have one functional ovary and oviduct, the left. The loss of the right ovary, the larger of the two in crocodilians, is inferred to have evolved in order to reduce weight during flight. Imagine a gravid female bird with swollen ovaries and an ovum in each oviduct in the process of being shelled. Her body is considerably heavier than normal, impeding her ability to take off quickly and maneuver in flight.

Given that Early Cretaceous birds were relatively poor fliers compared to living birds, this added weight would have posed a considerable disadvantage. These limitations due to flight may have resulted in the eventual loss of the right ovary. The closest non-avian dinosaur relatives to birds preserve evidence for two functional ovaries and oviducts; one specimen of oviraptorosaur preserves an egg in each oviduct. However, every specimen of Jehol bird preserving ovarian follicles clearly preserves the cluster on the left side of the body, indicating the right ovary has been lost. The long boney-tailed Jeholornis is one of the most basal fossil birds indicating that the loss of the right ovary occurred at the dinosaur-bird transition, providing strong support for the hypothesis that birds lost an ovary in response to the physical restrictions of flight.

Dr. Jingmai O’Connor is associate professor at the Institute of Vertebrate Palaeontology and Paleoanthropology, Chinese Academy of Sciences. Dr. O’Connor is a co-author of the paper ‘Ovarian follicles shed new light on dinosaur reproduction during the transition towards birds‘, which is published in the National Science Review.

Under the auspices of the Chinese Academy of Sciences, National Science Review is a new journal aimed at reviewing cutting-edge developments across science and technology in China and around the world. The journal focuses on topics of interest to the international science community, including multi-national collaborations, global issues in scientific and technological development, and their impact on society in general.

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Image credit: Fossil specimen (DNHM D2945/6) of the Early Cretaceous bird Hongshanornis longicresta. By Chiappe et al. CC-BY-3.0 via Wikimedia Commons

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