The two surviving groups of Archosaurs, Crocodilians and Birds, show very different reproductive strategies. Crocodilians have paired ovaries and produce large clutches of small eggs, which mature slowly prior to being laid, and make a relatively small investment in parental care. Birds have only a single ovary, a modification not seen in any other Amniote (Reptile or Mammal) with eggs that mature rapidly prior to being laid, smaller clutch sizes and larger eggs, and make a higher level of investment in parental care (these traits are highly variable within Birds, but there is a clear separation between the situation in Birds and the situation in Crocodilians).
In a paper published in the journal Nature on 17 March 2013, a team of scientists led by Xiaoting Zheng of the Institute of Geology and Palaeontology at Linyi University and the Shandong Tianyu Museum of Nature, reported the presence of ovarian follicles (developing eggs) in a specimen of the Early Cretaceous Bird Jeholornis. This met with some scepticism from the palaeontological community but no alternative explanation for the structures has been suggested.
In a paper published in the National Science Review on 12 December 2013, Jingmai O’Connor of the Institute of Vertebrate Palaeontology and Paleoanthropology of the Chinese Academy of Sciences, Xiaoting Zheng of the Institute of Geology and Palaeontology at Linyi University and the Shandong Tianyu Museum of Nature, Xiaoli Wang and Yan Wang, also of the Geology and Palaeontology at Linyi University and Zhonghe Zhou, also of the Institute of Vertebrate Palaeontology and Paleoanthropology of the Chinese Academy of Sciences, describe the presence of ovarian follicles in five further birds from the Johol Biota, all Enantiornithines (an extinct group of toothed Birds that dominated the Cretaceous Avian Fauna, and which are more closely related to modern Birds than Jeholornis) from the Shandong Tianyu Museum of Nature and discuss the implications of these findings for our understanding of the evolution of egg development in early Birds.
New specimen of an unnamed Enantiornithine Bird from the Jehol Biota, preserving ovarian follicles, note the specimen is preserved in dorsal view and the follicles are preserved on the left side of the body, scale bar equals 20 mm. (B) Close-up of the follicles (enlarged from white box in A), scale bar equals 5 mm. O’Connor et al (2013).
Because of the large clutch sizes and slow development of eggs in Crocodilians, a female Crocodilian, prior to laying eggs, will contain a large number of ovarian follicles of identical size. A female Bird on the other hand, will contain a smaller number of follicles, and these will be of different sizes, due to the rapid development of eggs in modern Birds. This raises questions as to when this situation developed, in the earliest birds or earlier in the Dinosaur group from which Birds evolved, or even the earliest Dinosaurs.
The presence of ovarian follicles has been reported once previously in a non-Avian Dinosaur, in a specimen of Compsognathus longipes from the Late Jurassic of Germany. Compsognathus longipes is a Jurassic Coelurosaur placed outside (but closely related to) the Maniraptoriformes, the group of Dinosaurs from which Birds evolved, and therefore a useful species from which to make judgements about the evolution of egg development in Birds. Unfortunately the angle at which Compsognathus longipes is preserved does not allow the determination of the number of ovaries it had, however it is clear that it had a large number of follicles, and that they were similar in size, suggesting that they developed in a similar way to the eggs of modern Crocodilians.
In addition an Oviraptorosaurian Maniraptoran has previously been described from the Late Cretaceous of China, with two eggs between the pubes (i.e. in the process of being laid). This has been interpreted as evidence that the Dinosaur had two oviducts, and therefore two ovaries.
Jeholornis contains a large number of small ovarian follicles, all apparently at the same stage of development, however these follicles are all found on the left side of the body, the side where the sole ovary of modern Birds is found, suggesting that this early Bird had already lost its second ovary.
The new Entornithine specimens all appear to show a range of clutch sizes, but none appear to possess ovarian follicles at different stages of development, suggesting that this arose in the Neornithine Birds (the group that includes all living Birds), after its split from the Entornithine Birds.
From this O’Connor et al. develop the following theory on the evolution of egg development in early Birds: The Coelurosaur and Maniraptoriformes, and therefore most likely all Dinosaurs, had paired ovaries and produced large numbers of small eggs, which matured slowly inside the mother in a way similar to that seen in modern Crocodilians. The early Bird, Jeholornis, which is only slightly more advanced than Archaeopteryx, and which is thought to have been a week flier with a slow metabolism, had already lost one ovary, presumably an adaptation to weight-reduction associated with flying, but otherwise shows a similar pattern of egg development. The more derived Entornithine Birds, a successful and diverse Cretaceous group, show a variety of reproductive strategies, as reflected in clutch sizes, but still have not developed the hierarchical development of eggs seen in modern Birds, which enables the female to hold eggs at different stages of development. Finally the Neornithine Birds show hierarchical development of eggs, a feature thought to be closely associated with having a high metabolism.
Preserved data regarding ovarian anatomy mapped over a simplified cladogram of Theropoda, with a focus on Maniraptora, the derived clade that includes Aves. Crocodylia are placed as the outgroup, and this clade and crown group birds define an extant phylogenetic bracket for interpreting the reproductive traits of Mesozoic birds and other extinct Theropods. O’Connor et al (2013).
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