A joint study by researchers from the UK and China, including the University of Bristol, sheds light on how birds shifted toward this more crouched posture.
The research team was led by Professor John R Hutchinson at the Royal Veterinary College (UK) and Professor Baoyu Jiang at Nanjing University in China. The study has been published in the online journal Nature Communications.
The team studied the lower leg of the early Cretaceous (about 125 million years old) bird Confuciusornis that had been fossilised in volcanic ash and lake sediments in China.
Dr Jiang said: "We found that this fossil had amazingly well preserved soft tissues around the ankle joint, including cartilages and ligaments.
"These soft tissues were not just preserved as an ashen replacement of the former tissue, as sometimes happens. Rather, the cellular and fibrous structure of the tissues was preserved at a microscopic level."
Going beyond microscopic analysis, X-ray synchrotron and multiple spectroscopic imaging methods showed that the detailed anatomical preservation extended to the molecular level, with some of the original chemistry of the bird's tissues remaining.
In particular, the team found evidence of fragments of the collagen proteins that made up the leg ligaments, which matched the preservation at the microscopic tissue level of detail. Their findings concur with an expanding body of evidence that, under special conditions, some biological molecules including even amino acids or partial proteins, can persist over millions of years in the fossil record.
Professor Roy Wogelius, from the University of Manchester, one of the collaborators on the project, added: "The preservation in this fossil was exceptional and allowed us to resolve subtle but important chemical and structural details within this critical early species of bird."
The researchers then reconsidered this evidence in light of the whole anatomy of the Confuciusornis leg, and that of its cousins from earlier dinosaurs to extinct and even modern birds.
Professor Hutchinson said: "Once we were confident that some of the remnants of the soft tissues around the ankle joint still remained around the ankle, we could reconstruct parts of the ankle beyond just the bones.
"The new information we gained about the anatomy of the cartilages and tendons show that this early bird had an ankle whose form fit an intermediate function between that of early dinosaurs and modern birds.
"Overall this reinforced other lines of evidence that the more crouched, zigzag limb posture of birds evolved gradually from early dinosaurs to birds, with even these early birds having limbs that were built and worked differently from those of living birds, but were approaching the modern condition."
This many-layered study was enabled by international collaboration between many scientists from fields as diverse as palaeontology and ornithology, biomechanics, geology and geochemistry, medical imaging and physics.
Professor Michael Benton from the School of Earth Sciences at the University of Bristol, said: "Our study exemplifies how a combination of sophisticated technologies with fast-paced discoveries of spectacular fossils is revealing new insights into how major changes in anatomy, physiology and behaviour evolved in animals."
The research was funded by the National Science Foundation of China, Leverhulme Trust and Natural Environment Research Council (UK).