Birdsong and human voice built from same genetic blueprint

A trio of recent studies led by researchers from The University of Texas at Austin is changing that.

The studies include high-resolution anatomical scans of syrinxes from hummingbirds and ostriches -- the world's smallest and largest bird species -- and the discovery that the syrinx and larynx, the vocal organ of reptiles and mammals, including humans, share the same developmental programming.

According to Julia Clarke, a professor at UT's Jackson School of Geosciences, this genetic connection between the vocal organs is an exciting new example of "deep homology," a term that describes how different tissues or organs can share a common genetic link.

"To me, this is as big as the flippers-to-limbs transition," said Clarke, who co-led or co-authored the studies. "In some ways, it's even bigger because the syrinx is not a modified organ with a new function but a completely new one with an ancient and common function."

The three studies are built on a foundation of collaborative and interdisciplinary syrinx research with physiologists and developmental biologists that Clarke has been leading for over a decade. The research got its start in 2013 when Clarke, a paleontologist, discovered a syrinx in a fossil of a duck-like bird that lived in what is now Antarctica during the Late Cretaceous. The specimen is the oldest syrinx to be discovered. But when she tried to compare the fossil syrinx to the syrinxes of modern birds, she found the scientific literature lacking. Many of the studies dated back to the 19^th century, before the advent of modern scientific imaging, or cited claims from those older studies made without double-checking them.

This set Clarke on a mission to modernize -- and maximize -- syrinx data collection.

"We had this new three-dimensional structure, but we had nothing to compare it to," said Clarke, describing CT imaging data of the fossil syrinx. "So, we started generating data that did not previously exist on syrinx structure across many different groups of birds."

Over the years, Clarke and members of her lab have developed new methods for dissecting, preserving and CT-scanning syrinxes that have helped reveal the syrinx in more detail. These enhanced views of the ostrich and hummingbird vocal organ have shown that bird behavior may be just as important as the syrinx when it comes to the repertoire of sounds these birds produce.

For example, in the study of the ostrich syrinx, the researchers found no significant differences in syrinx anatomy between adult male and female birds (previous studies focused only on male ostriches.) However, even though both sexes have the same vocal equipment, male ostriches tended to make a wider variety of sounds than female ostriches, with the sounds often associated with aggressive behaviors between rowdy males. On a visit to a Texas ostrich farm, the researchers recorded 11 types of calls, ranging from high frequency peeps and gurgles in baby ostriches to low frequency boos and booms in adult males. These included a few call types that had never been recorded before. The only sounds definitively recorded from adult female ostriches were hisses. What the females lacked in range, they made up for in attitude said Michael Chiappone, who became involved with the ostrich research as an undergraduate student at the Jackson School and is the lead author of the study.

"They were quite prolific hissers," said Chiappone, who is now a doctoral student at the University of Minnesota.

For the hummingbird study, the researchers compared the hummingbird syrinx to the syrinx of swifts and nightjars, two close relatives, and found that all three birds have similar vocal folds in their syrinx despite having different ways of learning their calls. Swifts and nightjars work with a limited repertoire of instinctive calls while hummingbirds are able to elaborate on calls by learning complex songs from each other, a trait called vocal learning.

According to Lucas Legendre, a Jackson School research associate who led the hummingbird research, the findings suggest that the common ancestor of all three birds also had a similar vocal fold structure -- and that it may have helped lay the groundwork for the evolution in vocal learning in hummingbirds.

"Having all of the [vocal fold] structures already present before vocal learning was acquired by hummingbirds probably made it easier for them to acquire vocal production learning," he said.

Before the study, it was uncertain if swifts even had vocal folds. As part of the research, Legendre created a 3D digital model of the swift vocal track that takes viewers down the windpipe to the syrinx and to the vocal folds that rest near the top of each branch of the syrinx. The model -- dubbed the "magical mystery voyage" by Clarke -- shows the advances in anatomical knowledge of syrinx that her lab is leading.

"This is a structure that wasn't known to exist outside of hummingbirds, but our CT scans revealed that swifts have these vocal folds in the same position," Clarke said. "This is the kind of voyage we needed to go on to get these answers."

At the same time Clarke and her team were developing methods to preserve and capture syrinx anatomy across bird species, they were collaborating with Clifford Tabin, a developmental biologist at Harvard University, on investigating the evolutionary origins of the syrinx by tracking the gene expression that accompanied vocal organ development in the embryos of birds, mammals and reptiles.

The research published in Current Biology is a culmination of that collaboration. The study details how scientists discovered the deep connection between the larynx and the syrinx tissues by observing that the same genes were controlling the development of the vocal organs in mice and chicken embryos, respectively, even though the organs arose from different embryological layers.

"They form under the influence of the same genetic pathways, ultimately giving the vocal tissue similar cellular structure and vibratory properties in birds and mammals," said Tabin, a co-lead on the study.

The study also analyzed syrinx development across bird species -- which involved observing gene expression in embryos from 14 different species, from penguins to budgies -- and found that the common ancestor of modern birds probably had a syrinx with two sound sources, or two independently functioning vocal folds. This trait is found in songbirds today, allowing many to create two distinct sounds at the same time. The research suggests that that the common ancestor of birds may have been making similarly diverse calls.

These results may shed light on the syrinx's origins but it's still unknown when the syrinx first developed and whether non-avian dinosaurs -- the ancestors of today's birds -- had the vocal organ, said Clarke. No one has yet found a fossil syrinx from a non-avian dinosaur.

According to Clarke, the best way to understand the possibilities for ancient dinosaur sounds is to continue studying vocalization as it exists today in birds, the dinosaurs that are still with us, and other reptile cousins.

"We can't start talking about sound production in dinosaurs until we truly understand the system in living species," she said.

This research was supported by the Gordon and Betty Moore Foundation, Howard Hughes Medical InstituteProfessors Program and the Jackson School of Geosciences. Chad Eliason, a senior research scientist at the Field Museum of Natural History and former postdoctoral scholar at the Jackson School, was also a major contributor to these syrinx projects and others.