An international team of researchers has sequenced the genomes of 45 avian species and created the most reliable tree of life for birds to date. Their new avian family tree helps to clarify how modern birds — the most species-rich class of four-limbed vertebrates on the planet — emerged rapidly from a mass extinction event that wiped out the dinosaurs about 66 million years ago.
It also reveals how some of the earliest branches on the bird tree of life diverged, answering many long-standing questions about the common ancestor of birds, crocodilians, and dinosaurs. The findings shed new light on the evolution of avian sex chromosomes, vocal learning in both birds and humans, and the process that led to birds losing their teeth.
The massive comparative genomics project took more than four years to complete and involved hundreds of scientists from about 80 institutions in 20 different countries. The collaboration culminated in multiple studies, eight of which are published in the 12 December issue of Science. Others are published in journals such as Genome Biology and GigaScience.
The research was led by Guojie Zhang from BGI in Shenzhen, China, and the University of Copenhagen in Denmark; Erich Jarvis from the Howard Hughes Medical Institute and Duke University in Durham, North Carolina; and Thomas Gilbert from the Natural History Museum of Denmark and Curtin University in Australia. With the expertise of colleagues from around the world, they were able to sequence at least one genome from every major modern bird lineage.
Zhang and his colleagues described their analysis of 48 avian genomes, including the 45 new sequences that they contributed (crow, duck, pigeon, falcon, woodpecker, eagle, ostrich, and many more) along with three genomes that were already available (chicken, turkey, and zebra finch). Their findings help to explain why bird genomes, in general, are about 70% smaller than those of mammals.
Bird specimens from the National Museum of Natural History in Washington, D.C. illustrate some of the diverse avian species whose genomes were sequenced for the project. | AAAS/ Carla Schaffer
"One major reason that bird genomes are so small is because they don't have much repetitive DNA," explained Zhang during a webcast teleconference. "Another reason is that bird genomes have experienced massive gene loss in their ancestral stages. At least 1,600 genes have been lost in all bird genomes. Many of these genes actually have essential functions in humans, including some related to reproduction, skeleton formation, and lung systems."
"The loss of these key genes may have a significant effect on the evolution of many distinct phenotypes of birds," he continued. "Like their loss of teeth and dysfunction of one of their ovaries."
The analysis also revealed that the earliest common ancestor of land birds, which include parrots and songbirds as well as hawks and eagles, was a predator at the top of its food chain.
In a separate report, Jarvis and colleagues showed that protein-coding genes are not enough to get accurate phylogenetic trees. They suggested that researchers must include non-coding sequences of DNA as well as regions between the genes to provide a more accurate picture.
"In the past, people have been using one, two — up to 10 or 20 genes — to try to infer [bird] species relationships over the last 100 million years or so," said Jarvis. "Our theory has been: If you take the whole genome, you would have a more accurate species tree than just one or two genes [could provide] alone."
Their approach required more than 300 years of CPU time on several supercomputers, but they suggest that it could enable other groups of researchers to reconstruct similar, high-quality species trees for other challenging datasets in the future.
Ed Green from the University of California in Santa Cruz, California, and colleagues described the first sequencing of three crocodilian genomes — the American alligator, the saltwater crocodile, and the Indian gharial — which represent birds' closest living relatives. They revealed that the genomes of such crocodilians are evolving at an exceptionally slow pace.
The Indian gharial is one of the closest living relatives of birds. | Christopher Brochu
"The molecular evolution of birds is much faster than it is in crocs, turtles, and other reptilian lineages," said Green. "So this avian lineage seems to be faster than other reptiles, but not faster than mammals."
Some of the other Science reports explore long-standing mysteries of bird biology. Qi Zhou from the University of California in Berkeley, California, and colleagues, for example, used the new avian genome sequences to explain how sex chromosomes have evolved in birds. Unlike the human Y chromosome, the avian W chromosome still has many active genes, and sex chromosomes of various bird species are currently at different stages of evolution, they write.
Andreas Pfenning from Duke University with support from the Howard Hughes Medical Institute, along with his colleagues, exploited the sequences to study the molecular specializations between brain circuits that are important for singing in vocal-learning birds and speech in humans. Osceola Whitney, also from Duke University, and his colleagues determined that a whopping 10% of a bird's genome is regulated by singing, with highly diverse patterns across singing brain regions mediated by differences in gene expression.
Robert Meredith from Montclair State University in Montclair, New Jersey, and colleagues suggests that the mutations that eliminated enamel and dentin from the teeth of modern birds, an event which eventually led to toothless beaks-began about 116 million years ago.
Taken together, these reports support the theory of a "big bang" for bird evolution, with many species emerging rapidly during the 10 to 15 million years that followed the dinosaurs' extinction at the Cretaceous-Paleogene Boundary. They're poised to provide a model for other comparative genomics projects for the foreseeable future.