International team maps "Big Bang" of bird speciation
The story of how modern species of birds emerged and evolved after the mass extinction event that wiped out the dinosaurs and much of everything else 66 million years ago is now coming to light, thanks to an ambitious international Avian Phylogenomics Project that has been underway for four years.
The first findings of this project were reported nearly simultaneously today in 23 papers: 8 in a special issue in Science and 15 accompanying papers in Genome Biology, GigaScience, and other journals.
Birds experienced a rapid burst of evolution in the wake of the extinction, producing the richly diverse class of vertebrates we know today. However, the relationship of modern birds has confused biologists for centuries, and the molecular mechanisms that gave rise to the great biodiversity in birds are barely known.
To resolve these fundamental questions, a consortium led by Guojie Zhang of the National Genebank at BGI and the University of Copenhagen, Erich Jarvis of Duke University and the Howard Hughes Medical Institute, and M. Thomas P. Gilbert of the Natural History Museum of Denmark has sequenced, assembled, and compared full genomes of 48 bird species, including the crow, duck, falcon, parakeet, crane, ibis, woodpecker, eagle, and others. These species represent all major branches of modern birds.
"Although birds have been studied for centuries, the unresolved phylogeny has been an obstacle for a long time to our understanding of molecular mechanisms for the biodiversity in birds," Zhang said. "BGI’s strong support and four years of hard work by the entire community have enabled us to answer numerous fundamental questions to a unprecedented scale."
"Although an increasing number of vertebrate genomes are being released, to date no single study has deliberately targeted the full diversity of any major vertebrate group," Gilbert said. “This is precisely what our consortium set out to do from the start. Only with this scale of sampling can scientists truly begin to fully explore the genomic diversity within a full vertebrate class."
Jarvis said, "This is an exciting moment. Lots of fundamental questions now can be resolved with more genomic data from a broader sampling."
This first round of analyses is already suggesting some remarkable new ideas about bird evolution.
The first flagship paper published in Science presents the well-resolved new avian phylogenetic tree basis on the whole-genome data. The second flagship paper in Science describes the big picture of the evolution patterns of avian genomes.
Six other papers published together in this special issue of Science describe how vocal learning may have evolved (and their similarities with the human brain's speech regions), how the sex chromosomes of birds came to be, how birds lost their teeth, how crocodile genomes evolved, and a new method for phylogenic analysis with large-scale genomics data.
The Avian Phylogenomics Consortium has so far involved more than 200 scientists from 80 institutions in 20 countries, including BGI in China, Copenhagen University, Duke University, the Smithsonian Museum, the Chinese Academy of Sciences, and Louisiana State University.
A Clearer Picture of the Bird Family Tree
Past attempts to reconstruct the avian family tree using partial DNA sequencing or anatomical and behavioral traits have been fraught with complexity and contradiction, because some species of birds are too closely related to tell which preceded the other in evolutionary history.
To resolve the debate on the timing and relationships of modern birds, one of the flagship papers, by Jarvis, Siavash Mirarab, and the consortium authors used whole-genome DNA sequences to infer the bird species tree.
Jarvis indicated that past attempts have used 10 to 20 genes to try to infer the species relationships, but the whole-genome approach leads to a somewhat different inferred phylogeny (family tree).
"We've figured out that protein-coding genes are not sufficient for inferring the species tree. You need non-coding sequence, including the intergenic regions," Jarvis said.
This new tree resolves the early branches of Neoaves (new birds) and supports conclusions of some relationships that have been long debated. For example, the findings support two independent origins of waterbirds and indicates that a common ancestor of core landbirds, which includes songbirds, parrots, woodpeckers, owls, eagles, and falcons, was an apex predator related to the giant terror birds that once roamed the Americas.
The researchers date the radiation of Neoaves at around the time of the mass extinction event 66 million years ago that killed off all other dinosaurs. This contradicts the idea that Neoaves blossomed 10 to 80 million years earlier, as some recent studies suggested.
Based on this new genomic data, only four lineages survived the mass extinction, and these gave rise to more than 10,000 Neoaves species, comprising 95% of all bird species living with us today.
The freed-up ecological niches caused by extinction were thought to allow rapid species radiation in less than 15 million years, which explains much of modern bird biodiversity.
Increasingly sophisticated and more affordable genomic sequencing technologies and the advent of computational tools for reconstructing and comparing whole genomes have allowed the consortium to resolve these controversies with better clarity than ever before, the researchers say.
A Genomic Perspective of Avian Evolution and Biodiversity
Birds are the most species-rich tetrapod vertebrates and spread out across the world. They have been traditionally used as models for evolutionary and ecological studies since Darwin.
The flagship paper led by Guojie Zhang, Cai Li, and others offers many new insights from a whole-genome perspective about the blueprints of their evolution and the resulting biodiversity.
For all their biological intricacies, birds are surprisingly light on DNA. Compared to other reptile genomes, avian genomes contain fewer of the repeating sequences and have lost thousands of genes in the early evolution after they split with other reptiles.
Zhang said, "Many of these genes have essential functions in humans, such as in the reproduction system, skeleton, and lungs. The loss of these key genes may have significant effect in evolution of many distinct phenotypes of birds. This is an exciting finding, because it is quite different from what people normally think that evolution innovation is normally contributed by origin of new genetic material. Sometimes, less is more."
The studies revealed that birds' genomic structure, from whole chromosome level to gene order, has been highly conserved among species over 100 million years. The evolutionary rate of nucleotide sequence across all bird species is also slower compared with that of mammals. Nevertheless, some genomic regions display relatively faster evolution in some lineages of species that show similar lifestyles or phenotypes.
This convergent evolution pattern may be the underlying mechanisms for how distant bird species evolved similar phenotypes independently. The analyses performed on particular gene families begins to better explain how birds evolved a lighter skeleton, distinct lung system, dietary specialties, colorful feathers, color vision, and sex-related traits.
The new studies have shed new light on several questions about birds.
How did vocal learning evolve?
Eight of the studies examined the vocal learning to understand how some birds, such as parrots, have the rare ability to learn and mimic speech.
Evidence reported in the two flagship papers indicates vocal learning evolved independently at least twice and was associated with convergence of many proteins. A study led by Andreas Pfenning, Jarvis, and others in collaboration with the Allen Institute for Brain Science found convergent changes in the activity of more than 50 genes responsible for brain circuitry related to specialized song learning in songbirds, parrots, and hummingbirds and also to human speech. Most of these genes are involved in forming neural connections.
Chakraborty and others found that parrots have a unique song system within a song system, potentially explaining their greater ability to imitate human speech.
Osceola Whitney, Pfenning, and others found that singing is associated with the activation of 10% of the expressed genome, with diverse brain patterns controlled by epigenetic regulation of the genome.
Morgan Wirthlin, Peter Lovell, Claudio Mello and others found unique genes in song control brain regions of songbirds. "I got into the Avian Phylogenomics Project because of my interest in birds as a model for vocal learning and speech production in humans," Jarvis said. "It has opened up some amazing new vistas on the evolution of brains, and not only allowed us to more precisely identify the analogous song and speech brain regions in birds and humans, but broadly similar cell types between birds and mammals."
The XYZW of sex chromosomes
Humans have XY sex chromosomes, and the sex of a human baby is determined by the presence or absence of Y in males. Birds by contrast have ZW chromosomes, where the sex of chick is determined by the presence or absence of W in females.
Most mammals share the same origin and similar evolution status of their Y chromosomes, which have degenerated to the point of having very few genes related to the 'maleness.'
A led by Qi Zhou and Doris Bachtrog at University of California, Berkeley, and Guojie Zhang and reported in Science found half of bird species still contain substantial numbers of active genes in their W chromosomes. This challenged the classic view that old Y or W chromosomes are usually a 'graveyard of genes' similar to the human Y chromosome.
Different bird species demonstrate drastically different states of sex chromosome evolution. For example, sex chromosomes of ostrich and emu, a group basal with all other birds, resemble their ancestor autosomes. In contrast, sex chromosomes of modern birds such as chicken and zebra finch are at the terminal stages and thus contain few active genes.
This finding opens new questions, such as how this great diversity in sex chromosomes correlates with the wide spectrum of phenotypic differences between sexes of birds, such as the differences between the peacock and the peahen.
How did birds lose their teeth?
A study led by Robert Meredith from Montclair State University and Robert Springer from University of California, Riverside, and reported in Science compared the genomes of living bird species with those of vertebrate species that have teeth. It identified key mutations in the parts of the genome that code for enamel and dentin. The evidence suggests these genes were disabled in the bird line more than 100 million years ago.
What is the connection between birds and dinosaurs?
Unlike mammals, birds (along with reptiles, fish, and amphibians) have not only chromosomes but also microchromosomes. These smaller packages of gene-rich material are thought to have been present in dinosaurs.
In the most comprehensive study to date of overall bird genome structure, Michael Romanov and Darren Griffin from University of Kent, Dennis Larkin from University of London, and others in BMC Genomics analyzed whole genomes of the chicken, turkey, Peking duck, zebra finch, and budgerigar. They found that the chicken is the most similar to an avian ancestor thought to be a feathered dinosaur.
A study led by Ed Green and Benedict Paten from University of California, Santa Cruz, David Ray from Texas Tech University, and others and reported in Science examined birds' closest living relative: crocodiles. They found that crocodiles have one of the slowest evolving genomes. In addition, the team was able to reconstruct the genome of the dinosaur that would have been the common ancestor of both birds and crocodiles.
Do differences in gene trees versus species tree matter?
In the phylogenomics flagship study, the consortium found that no gene tree has a history that is exactly the same as the species tree, partly due to a process called incomplete lineage sorting. However, a study led by Mirarab, Tandy Warnow from University of Texas, Austin, and others and reported in Science used new computational approaches to combine gene trees with similar histories to accurately infer a species tree.
Do bird genomes carry some viruses as much as other species?
A study led by Jie Cui and Edward Holmes from The University of Sydney, Zhang, and others and reported in Genome Biology showed evidence that throughout their history, birds have either been less susceptible to viral invasions or have been able to purge them more effectively.
When did colorful feathers evolve?
Elaborate, colorful feathers are thought to be evolutionarily advantageous, giving a male bird an edge over his competitors when it comes to mating.
In their flagship study, which was further analyzed by Matthew Greenwold and Roger Sawyer from the University of South Carolina, the consortium found that in eight of 46 bird lineages, the genes involved in feather coloration evolved more quickly than other genes. Landbirds have more than twice the number of beta keratin feather genes than do waterbirds, and domesticated pet and agricultural bird species have more than eight times the number of beta keratin feather genes.
What happens during species extinction and recovery?
Birds are like the proverbial canaries in the coal mine because of their sensitivity to environmental changes that cause extinction. In a study led by Shengbin Li, Cheng Cheng, and Jun Yu from Xi'an Jiaotong University, Jarvis and others and reported in Genome Biology, researchers analyzed the genomes of species that have recently gone nearly extinct, including the crested ibis in Asia and the bald eagle in the Americas.
They found genes that break down environmental toxins have a higher rate of mutations in these species and that endangered species have lower immune gene diversity.
In crested ibis populations that have been recovered by human assistance, genes involved in brain function and metabolism are evolving more rapidly. The researchers also found more genomic diversity in the recovering population than was expected, giving greater hope for species conservation.
The Start of Something Bigger
This sweeping genome-level comparison of an entire class of life is being powered by frozen bird tissue samples collected over the past 30 years by museums and other institutions around the world. Samples are sent as fingernail-sized chunks of frozen flesh mostly to Duke University and Copenhagen University for separation of the DNA.
Most of the genome sequencing and critical initial analyses of the genomes have then been conducted by the BGI in China.
The avian genome consortium is now creating a database that will be made publicly available for scientists to study the genetic basis of complex avian traits.
Setting up the pipeline for the large-scale study of whole genomes—collecting and organizing tissue samples, extracting the DNA, analyzing its quality, sequencing and managing torrents of new data—has been a massive undertaking. But the scientists say their work should help inform other major efforts for the comprehensive sequencing of vertebrate classes currently underway as part of an all-vertebrates Genome 10K Project.
To encourage other researchers to dig out this 'big data' and discover new patterns that were not seen in small-scale data before, the avian genome consortium has released the full dataset to the public in GigaScience, and in NCBI, ENSEMBL, and CoGe databases.
This project received the main financial support from BGI, China National GeneBank, and the US National Institutes of Health, the US National Science Foundation, the Howard Hughes Medical Institute, the Danish Government, the Lundbeck Foundation, and the many other sources funding the consortium’s individual scientists.
Other leadership in the Avian Phylogenomics Project include, but are not limited to, Stephen O’ Brien, David Haussler, and Oliver Ryder of the Genome 10K Project, Peter Houde of New Mexico State University, Edward Braun of the University of Florida, Joel Cracraft of the American Museum of Natural History, David Mindell of the University of California, San Francisco, Alexandros Stamatakis of the Heidelberg Institute for Theoretical Physics, Jon Fjeldsa and Carsten Rahbek of the University of Copenhagen, Scott Edwards of Harvard University, Dave Burt of the Roslin Institute, Gary Graves of the Smithsonian Institution, Robb Brumfield of Louisiana State University, and Wang Jun of BGI.