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Origin of avian genome size and structure in non-avian dinosaurs

Nature volume 446, pages 180–184 (2007)Cite this article

Abstract

Avian genomes are small and streamlined compared with those of other amniotes by virtue of having fewer repetitive elements and less non-coding DNA1,2. This condition has been suggested to represent a key adaptation for flight in birds, by reducing the metabolic costs associated with having large genome and cell sizes3,4. However, the evolution of genome architecture in birds, or any other lineage, is difficult to study because genomic information is often absent for long-extinct relatives. Here we use a novel bayesian comparative method to show that bone-cell size correlates well with genome size in extant vertebrates, and hence use this relationship to estimate the genome sizes of 31 species of extinct dinosaur, including several species of extinct birds. Our results indicate that the small genomes typically associated with avian flight evolved in the saurischian dinosaur lineage between 230 and 250 million years ago, long before this lineage gave rise to the first birds. By comparison, ornithischian dinosaurs are inferred to have had much larger genomes, which were probably typical for ancestral Dinosauria. Using comparative genomic data, we estimate that genome-wide interspersed mobile elements, a class of repetitive DNA, comprised 5–12% of the total genome size in the saurischian dinosaur lineage, but was 7–19% of total genome size in ornithischian dinosaurs, suggesting that repetitive elements became less active in the saurischian lineage. These genomic characteristics should be added to the list of attributes previously considered avian but now thought to have arisen in non-avian dinosaurs, such as feathers5, pulmonary innovations6, and parental care and nesting7.

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Figure 1: Primary histological data, distribution of average osteocyte-cell size in extinct dinosaur species, and regression lines derived from data on extant animals used to infer genome size and interspersed repetitive elements.
Figure 2: Haploid genome size (mean of posterior predictive distribution) mapped onto a phylogeny shows a reduction within saurischian dinosaurs, the lineage to which birds belong.
Figure 3: Bar graph of interspersed repetitive elements in a range of extant vertebrate species and extinct dinosaur species inferred from genome size reconstructions and the correlation between repetitive element composition and genome size.

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Acknowledgements

We thank the Museum of Comparative Zoology at Harvard University and the Gabriel Laboratory for Cellular and Molecular Paleontology at the Museum of the Rockies for access to histology sections. We also thank D. Smith at the Imaging Center in the Department of Cellular and Molecular Biology, Harvard University for facilitating microscopy, A. Crompton and J. Horner for offering materials, laboratory space, and discussions on palaeohistology, and D. Jablonski and T. Garland for discussions. We are grateful for comments from B. Jennings, N. Hobbs and M. Laurin, which have improved this manuscript. This research was supported by an NIH Postdoctoral Fellowship granted to C.L.O., an NSF grant to S.V.E. and a NERC grant to M.P.

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Authors and Affiliations

  1. Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA,

    Chris L. Organ, Andrew M. Shedlock & Scott V. Edwards

  2. School of Biological Sciences, University of Reading, Reading, RG6 6AJ, UK,

    Andrew Meade & Mark Pagel

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Correspondence to Chris L. Organ.

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Organ, C., Shedlock, A., Meade, A. et al. Origin of avian genome size and structure in non-avian dinosaurs. Nature 446, 180–184 (2007). https://doi.org/10.1038/nature05621

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