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

Abstract

Avian genomes are small and streamlined compared with those of other amniotes by virtue of having fewer repetitive elements and less non-coding DNA. 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 sizes. 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 feathers, pulmonary innovations, and parental care and nesting.

Genome size and wing parameters in passerine birds

“…This would place partially reduced genome sizes among other features such as bipedal locomotion, feathers and possibly endothermy that appeared prior to, but then became important in, the evolution of avian flight. However, just as feathers subsequently became specialized for flight in birds, the fact that the estimated mean genome size for theropod dinosaurs (Organ et al 2007) is notably larger than that for the average modern bird (Gregory 2008) implies that genome sizes continued to shrink along with specializations for flight.…”

“…New light has been recently shed on this issue by Organ et al (2007) who analysed the sizes of fossil osteocytes in dinosaurs and concluded that birds inherited already diminutive genomes from ancestral theropod dinosaurs (see also Ellegren 2007;Zimmer 2007). This would place partially reduced genome sizes among other features such as bipedal locomotion, feathers and possibly endothermy that appeared prior to, but then became important in, the evolution of avian flight.…”

The smallest avian genomes are found in hummingbirds

“…We hypothesize that hovering flight and reduced genome size evolved in concert early in the hummingbird lineage. Further genome size estimates for owlet-nightjars and swifts and cell size estimates for fossil Apodiformes will bear on this hypothesis (Mayr 2004;Organ et al 2007;Organ & Shedlock 2009), but remain unavailable at present.…”

“…Importantly, it has recently been shown that saurischian dinosaurs (from which birds are derived) had already undergone an initial reduction in genome size prior to the evolution of flight (Organ et al 2007), though their estimated genome sizes were larger than those of most modern birds. Moreover, genome sizes have been suggested to assort according to flight ability in extant birds, with strong fliers possessing the smallest genomes and flightless birds some of the largest (Hughes 1999;Gregory 2005).…”

Genome sizes through the ages

“…People have asked how and why genomes vary so extensively and whether it matters. The recent paper by Organ et al (2007) has extended a paleogenomics dimension to these questions. By using the size of fossil dinosaur bone cells as proxies for genome size, they have attempted to trace the evolution of genome size in reptiles over 200 million years.…”