The "Big Bang" of Bird Evolution (Part 2)

A few highlights of the findings; a look at what's next
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Dec 10, 2014

(Continued from "Big Bang" of Bird Evolution.) 

Important Lessons

The new studies have shed light on several other questions about birds, including:

How did vocal learning evolve? Eight studies in the package examined the subject of vocal learning. According to new evidence in the two flagship papers, vocal learning evolved independently at least twice, and was associated with convergent evolution in many proteins. A Science study led by Andreas Pfenning, Alexander Hartemink, Jarvis and others at Duke, in collaboration with researchers at the Allen Institute for Brain Science in Seattle and the RIKEN Institute in Japan, found that the specialized song-learning brain circuitry of vocal learning birds (songbirds, parrots and hummingbirds) and human brain speech regions have convergent changes in the activity of more than 50 genes. Most of these genes are involved in forming neural connections. Osceola Whitney, Pfenning and Anne West, also of Duke, found in another Science study that singing is associated with the activation of 10 percent of the expressed genome, with diverse activation patterns in different song-learning regions of the brain, controlled by epigenetic regulation of the genome. Duke's Mukta Chakraborty and others found in a PLoS ONE study that parrots have a song system within a song system, with the surrounding song system unique to them. This might explain their greater ability to imitate human speech. In a BMC Genomics study, Morgan Wirthlin, Peter Lovell and Claudio Mello from Oregon Health & Science University found unique genes in the song-control brain regions of songbirds.

Grey-Crowned CraneGrey-crowned crane (Balearica regulorum) by Sanja Byelkin via Wikimedia Commons

The XYZW of sex chromosomes. Just as the sex of humans is determined by the X and Y chromosomes, the sex of birds is controlled by the Z and W chromosomes. The W makes birds female, just as the Y makes humans male. Most mammals share a similar evolutionary history of the Y chromosome, which now contains many degenerated genes that no longer function and only a few active genes related to ”maleness.” A Science study led by Qi Zhou and Doris Bachtrog from the University of California, Berkeley, and Zhang found that half of bird species still contain substantial numbers of active genes in their W chromosomes. This challenges the classic view that the W chromosome is a ”graveyard of genes” like the human Y.

This group also found that bird species are at drastically different states of sex chromosome evolution. For example, the ostrich and emu, which belong to one of the older branches of the bird family tree, have sex chromosomes resembling their ancestors. Yet some modern birds such as the chicken and zebra finch have sex chromosomes that contain few active genes. This opens a new set of questions on how the diversity of sex chromosomes may drive the diversity of sex differences in the outward appearance of various bird species. Peacocks and peahens are dramatically different; male and female crows are indistinguishable.

How did birds lose their teeth? In a Science study led by Robert Meredith from Montclair State University and Mark Springer from the University of California, Riverside, a comparison between the genomes of living bird species and those of vertebrate species that have teeth identified key mutations in the parts of the genome that code for enamel and dentin, the building blocks of teeth. The evidence suggests that five tooth-related genes were disabled within a short time period in the common ancestor of modern birds more than 100 million years ago.

What's the connection between birds and dinosaurs? Unlike mammals, birds (along with reptiles, fish and amphibians) have a large number of tiny microchromosomes. These smaller packages of gene-rich material are thought to have been present in their dinosaur ancestors. A study of genome karyotype structure in BMC Genomics analyzed whole genomes of the chicken, turkey, Peking duck, zebra finch and budgerigar. They found the chicken has the most similar overall chromosome pattern to an avian ancestor, which was thought to be a feathered dinosaur. This work was led by Darren Griffin and Michael Romanov from the University of Kent, and by Denis Larkin and Marta Farré from the Royal Veterinary College, University of London.

Another study in Science examined birds' closest living relatives, the crocodiles. This team, led by Richard Green and Benedict Paton from the University of California, Santa Cruz, David Ray from Texas Tech University and Ed Braun from the University of Florida, found that crocodiles have one of the slowest-evolving genomes. The researchers were able to infer the genome sequence of the common ancestor of birds and crocodilians (archosaurs) and therefore all dinosaurs, including those that went extinct 66 million years ago.

Do differences in gene trees versus species trees matter? In the phylogenomics flagship study by Jarvis and others, the consortium found that no gene tree has a history exactly the same as the species tree, partly due to a process called incomplete lineage sorting. Another Science study, led by Tandy Warnow at the University of Texas and the University of Illinois, and her student Siavash Mirarab, developed a new computational approach called “statistical binning.” They used this approach to show it does not matter much that the gene trees differ from the species tree because they were able to infer the first coalescent-based, genome-scale species tree, combining gene trees with similar histories to accurately infer a species tree.

Do bird genomes carry fewer virus sequences than other species? Mammalian genomes harbor a diverse set of genomic “fossils” of past viral infections called “endogenous viral elements" (EVEs). A study published in Genome Biology led by Jie Cui of Duke-NUS Graduate Medical School in Singapore, Edward Holmes of the University of Sydney and Zhang, found that bird species had 6-13 times fewer EVE infections in their past than mammals. This finding is consistent with the fact that birds have smaller genomes than mammals. It also suggests birds may either be less susceptible to viral invasions or better able to purge viral genes.

Crested IbisCrested Ibis (Nipponia nippon) by Nicolas Huet le Jeune (1770-1830) via Wikimedia Commons

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. The Zhang team's flagship paper in Science, and a companion study in BMC Evolutionary Biology by Matthew Greenwold and Roger Sawyer from the University of South Carolina, found that genes involved in feather coloration evolved more quickly than other genes in eight of 46 bird lineages. Waterbirds have the lowest number of beta keratin feather genes, landbirds have more than twice as many, and in domesticated pet and agricultural bird species, there are eight times more of these genes.

What happens to species facing extinction or recovering from near-extinction? Birds are like the proverbial canaries in the coal mine because of their sensitivity to environmental changes that cause extinction. In a Genome Biology study led by Shengbin Li, Cheng Cheng and Jun Yu from Xi'an Jiaotong University, Huanming Yang from BGI and Jarvis, 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 there is lower diversity of immune system genes in endangered species. In the recovering crested ibis population, genes involved in brain function and metabolism have been preferentially selected. The researchers found more genomic diversity in the recovering population than was expected, giving greater hope for species conservation.

Adélie Penguin (Pygoscelis adeliae) by Liam Quinn via Wikimedia Commons

How did penguins adapt to the hostile Antarctic environment? Penguins live in the coldest place on Earth and have specialized wings and skin that allow them to swim under water. Two Antarctic penguin genomes, Adélie and Emperor, were sequenced by the consortium. In a GigaScience paper led by Zhang and David Lambert from Griffith University, changes in genes related to feathers, wings, eyes and metabolism give insights into how these birds adapted to the cold and hostile environment. The analysis also reveals historical population changes in response to climate change and glaciation, and estimates that the ancestral penguin species first appeared about 60 million years ago.


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 University of Copenhagen for DNA separation. Most of the genome sequencing and critical initial analyses of the genomes have then been conducted by BGI.

The Avian phylogenomics Consortium is now creating a database that will be made publicly available in the future 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. To encourage other researchers to dig through 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. The GigaScience data releases were done via Twitter, which led to much discussion on social media and doubled the number of GigaScience database users.

Under the leadership of Dave Burt, the National Avian Research Facility at the Roslin Institute and Edinburgh University, UK, has created genome browser databases based on the ENSEMBL model for 48 species.

This project received its main financial support from BGI and the China National GeneBank, as well as from the U.S. National Institutes of Health, the U.S. National Science Foundation, the Howard Hughes Medical Institute, the Lundbeck Foundation and the Danish National Research Foundation, and support from the many other sources of funding for the consortium’s individual scientists.

Other leadership in the Avian Phylogenomics Project include, but are not limited to, Tandy Warnow of the University of Illinois; Stephen O’ Brien, David Haussler and Oliver Ryder of the Genome 10K consortium; 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 Studies and Karlsruhe Institute of Technology; Jon Fjeldsa and Carsten Rahbek of the University of Copenhagen; Scott Edwards of Harvard University; David Burt of the Roslin Institute of Edinburgh University; Gary Graves of the Smithsonian Institution; Robb Brumfield of Louisiana State University; Agostinho Antunes of the Universidade do Porto in Portugal; Darren Griffin of the University of Kent; Dennis Larkin from the Royal Veterinary College, University of London; Qi Zhou of the University of California, Berkeley; and Wang Jun of BGI.