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Bird and archosaur genome analysis in Science

Ben Creisler

The new issue of Science has a special section on a new study of avian
and crocodile genomes and relates to many vert-paleo topics.



Particular papers of interest:

Xing Xu, Zhonghe Zhou, Robert Dudley, Susan Mackem, Cheng-Ming Chuong,
Gregory M. Erickson, and David J. Varricchio (2014)
An integrative approach to understanding bird origins.
Science 346 (6215): 1253293
DOI: 10.1126/science.1253293

The origin of birds is one of the most enduring and dramatic
evolutionary debates. The hypothesis that the primarily small-sized
birds are nested within a theropod dinosaur group that includes the
gigantic Tyrannosaurus rex has been supported by strong fossil
evidence, but until recently, several important issues remained
unresolved, including the origins of feathers and flight, the
“temporal paradox” (the coelurosaurian theropods occur too late in the
fossil record to be ancestral to the Jurassic bird Archaeopteryx), and
supposed homological incongruities (e.g., the suggested homologies of
three fingers in tetanuran theropods are different from those of
living birds). Recent discoveries of spectacular dinosaur fossils from
China and elsewhere provide new information to address these issues,
and also prompt numerous studies in disciplines other than
paleontology that help explain how bird characteristics originated and

Evolutionary history of selected bird features inferred from
multidisciplinary data. Recent studies demonstrate that major bird
characteristics have evolved in a sequential way, and many of them
initiated transformation early in dinosaur evolution, with some
approaching modern conditions well before the origin of birds, whereas
others appear only near the origin of the crown group birds.

The discoveries of feathered dinosaur fossils from the Jurassic and
Cretaceous sediments of China and elsewhere document a diverse range
of feathers from monofilamentous feathers to highly complex flight
feathers, which show a general evolutionary trend of increasing
complexity leading to the cladogenesis of birds. The wide occurrence
of foot feathers in Mesozoic theropods (i.e., short filamentous forms
in relatively basal theropods and large vaned forms in derived
theropods, including early birds) clarifies feather-scale relations
and integumentary evolution pertinent to flight origins and also shows
that bird flight likely had evolved through a four-winged stage. With
numerous discoveries of well-preserved dinosaur fossils covering a
wide range of geological periods, the morphological, functional, and
temporal transition from ground-living to flight-capable theropod
dinosaurs is now one of the best-documented major evolutionary
transitions. Meanwhile, studies in disciplines other than paleontology
provide new insights into how bird characteristics originated and
evolved—such as feathers, flight, endothermic physiology, unique
strategies for reproduction and growth, and an unusual pulmonary
system. The iconic features of extant birds, for the most part,
evolved in a gradual and stepwise fashion throughout theropod
evolution. However, new data also highlight occasional bursts of
morphological novelty at certain stages particularly close to the
origin of birds and an unavoidable complex, mosaic evolutionary
distribution of major bird characteristics on the theropod tree.
Research into bird origins provides a model example of how an
integration of paleontological and neontological data can be used to
gain a comprehensive understanding of the complexity surrounding major
evolutionary transitions and to set new research directions.

A refined, more robust phylogeny will be imperative to move our
studies forward. A larger data set will help to increase the accuracy
of phylogenetic reconstructions, but better character formulation and
more accurate scorings are imperative at the current stage. In terms
of character evolution, an integrative approach combining
paleontological, neontological, developmental, temporal, and even
paleoenvironmental data is particularly desirable. Greater examination
of fossils pertaining to molecular information is also a potentially
fruitful avenue for future investigation. Evolutionary scenarios for
various aspects of the origin of birds have sometimes been constructed
from neontological data, but any historical reconstruction must
ultimately be tested using the fossil record. Consequently, dense
fossil sampling along the line to modern birds and better
understanding of transitional forms play key roles in such


Robert W. Meredith, Guojie Zhang, M. Thomas P. Gilbert, Erich D.
Jarvis, and Mark S. Springer (2014)
Evidence for a single loss of mineralized teeth in the common avian ancestor.
Science 346 (6215): 1254390
DOI: 10.1126/science.1254390

The absence of teeth or edentulism has evolved on multiple occasions
within vertebrates, including birds, turtles, and a few groups of
mammals (anteaters, baleen whales, and pangolins). There are also
mammals with enamelless teeth (aardvarks, sloths, and armadillos). All
toothless/enamelless vertebrates are descended from ancestors with
enamel-capped teeth. In the case of birds, it is theropod dinosaurs.
Instead of teeth, modern birds use a horny beak (rhamphotheca) and
part of their digestive tract (muscular gizzard) to grind up and
process food. The fossil record of early birds is fragmentary, and it
is unclear whether tooth loss evolved in the common ancestor of all
modern birds or convergently in two or more independent lineages.

The absence of teeth or edentulism has evolved on multiple occasions
within vertebrates, including birds, turtles, and a few groups of
mammals (anteaters, baleen whales, and pangolins). There are also
mammals with enamelless teeth (aardvarks, sloths, and armadillos). All
toothless/enamelless vertebrates are descended from ancestors with
enamel-capped teeth. In the case of birds, it is theropod dinosaurs.
Instead of teeth, modern birds use a horny beak (rhamphotheca) and
part of their digestive tract (muscular gizzard) to grind up and
process food. The fossil record of early birds is fragmentary, and it
is unclear whether tooth loss evolved in the common ancestor of all
modern birds or convergently in two or more independent lineages.

Observed shared inactivating mutations in tooth formation. Related
genes were mapped onto a time tree depicting evolutionary
relationships and times of divergence between modern birds, the
closely related extinct taxon Ichthyornis, and the American alligator.
The hypothesized loss of mineralized teeth on the modern bird branch
at 116 million years ago (Ma) is based on frameshift mutation rates.
Observed shared inactivating mutations in tooth formation. Related
genes were mapped onto a time tree depicting evolutionary
relationships and times of divergence between modern birds, the
closely related extinct taxon Ichthyornis, and the American alligator.
The hypothesized loss of mineralized teeth on the modern bird branch
at 116 million years ago (Ma) is based on frameshift mutation rates.

Tooth formation in vertebrates is a complicated process that involves
many different genes. Of these genes, six are essential for the proper
formation of dentin (DSPP) and enamel (AMTN, AMBN, ENAM, AMELX, and
MMP20). We examined these six genes in the genomes of 48 bird species,
which represent nearly all living bird orders, as well as the American
alligator, a representative of Crocodylia (the closest living
relatives of birds), for the presence of inactivating mutations that
are shared by all 48 birds. The presence of such shared mutations in
dentin and enamel-related genes would suggest a single loss of
mineralized teeth in the common ancestor of all living birds. We also
queried the genomes of additional toothless/enamelless vertebrates,
including three turtles and four mammals, for inactivating mutations
in these genes. For comparison, we looked at the genomes of mammalian
taxa with enamel-capped teeth.

All edentulous vertebrate genomes that were examined are characterized
by inactivating mutations in DSPP, AMBN, AMELX, AMTN, ENAM, and MMP20,
rendering these genes nonfunctional. The dentin-related gene DSPP is
functional in vertebrates with enamelless teeth (sloth, aardvark, and
armadillo). All six genes are functional in the American alligator and
mammalian taxa with enamel-capped teeth. More important, 48 bird
species share inactivating mutations in both dentin-related (DSPP) and
enamel-related genes (ENAM, AMELX, AMTN, and MMP20), indicating that
the genetic machinery necessary for tooth formation was lost in the
common ancestor of all modern birds. Furthermore, the frameshift
mutation rate in birds suggests that the outer enamel covering of
teeth was lost about 116 million years ago.

We postulate, on the basis of fossil and molecular evidence, a
two-step scenario whereby tooth loss and beak development evolved
together in the common ancestor of all modern birds. In the first
stage, tooth loss and partial beak development commenced on the
anterior portion of both the upper and lower jaws. The second stage
involved concurrent progression of tooth loss and beak development
from the anterior portion of both jaws to the back of the rostrum. We
propose that this progression ultimately resulted in a complete horny
beak that effectively replaced the teeth and may have contributed to
the diversification of living birds.

Richard E. Green, Edward L. Braun, Joel Armstrong, Dent Earl, Ngan
Nguyen, Glenn Hickey, Michael W. Vandewege, John A. St. John, Salvador
Capella-Gutiérrez, Todd A. Castoe, Colin Kern, Matthew K. Fujita, Juan
C. Opazo, Jerzy Jurka, Kenji K. Kojima, Juan Caballero, Robert M.
Hubley, Arian F. Smit, Roy N. Platt, Christine A. Lavoie, Meganathan
P. Ramakodi, John W. Finger Jr., Alexander Suh, Sally R. Isberg, Lee
Miles, Amanda Y. Chong, Weerachai Jaratlerdsiri, Jaime Gongora,
Christopher Moran, Andrés Iriarte, John McCormack, Shane C. Burgess,
Scott V. Edwards, Eric Lyons, Christina Williams, Matthew Breen, Jason
T. Howard, Cathy R. Gresham, Daniel G. Peterson, Jürgen Schmitz, David
D. Pollock, David Haussler, Eric W. Triplett, Guojie Zhang, Naoki
Irie, Erich D. Jarvis, Christopher A. Brochu, Carl J. Schmidt, Fiona
M. McCarthy, Brant C. Faircloth, Federico G. Hoffmann, Travis C.
Glenn, Toni Gabaldón, Benedict Paten, and David A. Ray (2014)

Three crocodilian genomes reveal ancestral patterns of evolution among
Science 346 (6215): 1254449
DOI: 10.1126/science.1254449

Crocodilians and birds are the two extant clades of archosaurs, a
group that includes the extinct dinosaurs and pterosaurs. Fossils
suggest that living crocodilians (alligators, crocodiles, and
gharials) have a most recent common ancestor 80 to 100 million years
ago. Extant crocodilians are notable for their distinct morphology,
limited intraspecific variation, and slow karyotype evolution. Despite
their unique biology and phylogenetic position, little is known about
genome evolution within crocodilians.

Evolutionary rates of tetrapods inferred from DNA sequences anchored
by ultraconserved elements. Evolutionary rates among reptiles vary,
with especially low rates among extant crocodilians but high rates
among squamates. We have reconstructed the genomes of the common
ancestor of birds and of all archosaurs (shown in gray silhouette,
although the morphology of these species is uncertain).

Genome sequences for the American alligator, saltwater crocodile, and
Indian gharial—representatives of all three extant crocodilian
families—were obtained to facilitate better understanding of the
unique biology of this group and provide a context for studying avian
genome evolution. Sequence data from these three crocodilians and
birds also allow reconstruction of the ancestral archosaurian genome.

We sequenced shotgun genomic libraries from each species and used a
variety of assembly strategies to obtain draft genomes for these three
crocodilians. The assembled scaffold N50 was highest for the alligator
(508 kilobases). Using a panel of reptile genome sequences, we
generated phylogenies that confirm the sister relationship between
crocodiles and gharials, the relationship with birds as members of
extant Archosauria, and the outgroup status of turtles relative to
birds and crocodilians.

We also estimated evolutionary rates along branches of the tetrapod
phylogeny using two approaches: ultraconserved element–anchored
sequences and fourfold degenerate sites within stringently filtered
orthologous gene alignments. Both analyses indicate that the rates of
base substitution along the crocodilian and turtle lineages are
extremely low. Supporting observations were made for transposable
element content and for gene family evolution. Analysis of
whole-genome alignments across a panel of reptiles and mammals showed
that the rate of accumulation of micro-insertions and microdeletions
is proportionally lower in crocodilians, consistent with a single
underlying cause of a reduced rate of evolutionary change rather than
intrinsic differences in base repair machinery. We hypothesize that
this single cause may be a consistently longer generation time over
the evolutionary history of Crocodylia.

Low heterozygosity was observed in each genome, consistent with
previous analyses, including the Chinese alligator. Pairwise
sequential Markov chain analysis of regional heterozygosity indicates
that during glacial cycles of the Pleistocene, each species suffered
reductions in effective population size. The reduction was especially
strong for the American alligator, whose current range extends
farthest into regions of temperate climates.

We used crocodilian, avian, and outgroup genomes to reconstruct 584
megabases of the archosaurian common ancestor genome and the genomes
of key ancestral nodes. The estimated accuracy of the archosaurian
genome reconstruction is 91% and is higher for conserved regions such
as genes. The reconstructed genome can be improved by adding more
crocodilian and avian genome assemblies and may provide a unique
window to the genomes of extinct organisms such as dinosaurs and


Guojie Zhang, Cai Li, Qiye Li, Bo Li, Denis M. Larkin, Chul Lee, Jay
F. Storz, Agostinho Antunes, Matthew J. Greenwold, Robert W. Meredith,
Anders Ödeen, Jie Cui, Qi Zhou, Luohao Xu, Hailin Pan, Zongji Wang,
Lijun Jin, Pei Zhang, Haofu Hu, Wei Yang, Jiang Hu, Jin Xiao, Zhikai
Yang, Yang Liu, Qiaolin Xie, Hao Yu, Jinmin Lian, Ping Wen, Fang
Zhang, Hui Li, Yongli Zeng, Zijun Xiong, Shiping Liu, Long Zhou,
Zhiyong Huang, Na An, Jie Wang, Qiumei Zheng, Yingqi Xiong, Guangbiao
Wang, Bo Wang, Jingjing Wang, Yu Fan, Rute R. da Fonseca, Alonzo
Alfaro-Núñez, Mikkel Schubert, Ludovic Orlando, Tobias Mourier, Jason
T. Howard, Ganeshkumar Ganapathy, Andreas Pfenning, Osceola Whitney,
Miriam V. Rivas, Erina Hara, Julia Smith, Marta Farré, Jitendra
Narayan, Gancho Slavov, Michael N Romanov, Rui Borges, João Paulo
Machado, Imran Khan, Mark S. Springer, John Gatesy, Federico G.
Hoffmann, Juan C. Opazo, Olle Håstad, Roger H. Sawyer, Heebal Kim,
Kyu-Won Kim, Hyeon Jeong Kim, Seoae Cho, Ning Li, Yinhua Huang,
Michael W. Bruford, Xiangjiang Zhan, Andrew Dixon, Mads F. Bertelsen,
Elizabeth Derryberry, Wesley Warren, Richard K Wilson, Shengbin Li,
David A. Ray, Richard E. Green, Stephen J. O’Brien, Darren Griffin,
Warren E. Johnson, David Haussler, Oliver A. Ryder, Eske Willerslev,
Gary R. Graves, Per Alström, Jon Fjeldså, David P. Mindell, Scott V.
Edwards, Edward L. Braun, Carsten Rahbek, David W. Burt, Peter Houde,
Yong Zhang, Huanming Yang, Jian Wang, Avian Genome Consortium, Erich
D. Jarvis, M. Thomas P. Gilbert, and Jun Wang (2014)

Comparative genomics reveals insights into avian genome evolution and
Science 346 (6215): 1311-1320
DOI: 10.1126/science.1251385

Birds are the most species-rich class of tetrapod vertebrates and have
wide relevance across many research fields. We explored bird
macroevolution using full genomes from 48 avian species representing
all major extant clades. The avian genome is principally characterized
by its constrained size, which predominantly arose because of
lineage-specific erosion of repetitive elements, large segmental
deletions, and gene loss. Avian genomes furthermore show a remarkably
high degree of evolutionary stasis at the levels of nucleotide
sequence, gene synteny, and chromosomal structure. Despite this
pattern of conservation, we detected many non-neutral evolutionary
changes in protein-coding genes and noncoding regions. These analyses
reveal that pan-avian genomic diversity covaries with adaptations to
different lifestyles and convergent evolution of traits.

Erich D. Jarvis, Siavash Mirarab, Andre J. Aberer, Bo Li, Peter Houde,
Cai Li, Simon Y. W. Ho, Brant C. Faircloth, Benoit Nabholz, Jason T.
Howard, Alexander Suh, Claudia C. Weber, Rute R. da Fonseca, Jianwen
Li, Fang Zhang, Hui Li, Long Zhou, Nitish Narula, Liang Liu, Ganesh
Ganapathy, Bastien Boussau, Md. Shamsuzzoha Bayzid, Volodymyr
Zavidovych, Sankar Subramanian, Toni Gabaldón, Salvador
Capella-Gutiérrez, Jaime Huerta-Cepas, Bhanu Rekepalli, Kasper Munch,
Mikkel Schierup, Bent Lindow, Wesley C. Warren, David Ray, Richard E.
Green, Michael W. Bruford, Xiangjiang Zhan, Andrew Dixon, Shengbin Li,
Ning Li, Yinhua Huang, Elizabeth P. Derryberry, Mads Frost Bertelsen,
Frederick H. Sheldon, Robb T. Brumfield, Claudio V. Mello, Peter V.
Lovell, Morgan Wirthlin, Maria Paula Cruz Schneider, Francisco
Prosdocimi, José Alfredo Samaniego, Amhed Missael Vargas Velazquez,
Alonzo Alfaro-Núñez, Paula F. Campos, Bent Petersen, Thomas
Sicheritz-Ponten, An Pas, Tom Bailey, Paul Scofield, Michael Bunce,
David M. Lambert, Qi Zhou, Polina Perelman, Amy C. Driskell, Beth
Shapiro, Zijun Xiong, Yongli Zeng, Shiping Liu, Zhenyu Li, Binghang
Liu, Kui Wu, Jin Xiao, Xiong Yinqi, Qiuemei Zheng, Yong Zhang,
Huanming Yang, Jian Wang, Linnea Smeds, Frank E. Rheindt, Michael
Braun, Jon Fjeldsa, Ludovic Orlando, F. Keith Barker, Knud Andreas
Jønsson, Warren Johnson, Klaus-Peter Koepfli, Stephen O’Brien, David
Haussler, Oliver A. Ryder, Carsten Rahbek, Eske Willerslev, Gary R.
Graves, Travis C. Glenn, John McCormack, Dave Burt, Hans Ellegren, Per
Alström, Scott V. Edwards, Alexandros Stamatakis, David P. Mindell,
Joel Cracraft, Edward L. Braun, Tandy Warnow, Wang Jun, M. Thomas P.
Gilbert, and Guojie Zhang (2014)

Whole-genome analyses resolve early branches in the tree of life of
modern birds.
Science 346 (6215): 1320-1331
DOI: 10.1126/science.1253451

To better determine the history of modern birds, we performed a
genome-scale phylogenetic analysis of 48 species representing all
orders of Neoaves using phylogenomic methods created to handle
genome-scale data. We recovered a highly resolved tree that confirms
previously controversial sister or close relationships. We identified
the first divergence in Neoaves, two groups we named Passerea and
Columbea, representing independent lineages of diverse and
convergently evolved land and water bird species. Among Passerea, we
infer the common ancestor of core landbirds to have been an apex
predator and confirm independent gains of vocal learning. Among
Columbea, we identify pigeons and flamingoes as belonging to sister
clades. Even with whole genomes, some of the earliest branches in
Neoaves proved challenging to resolve, which was best explained by
massive protein-coding sequence convergence and high levels of
incomplete lineage sorting that occurred during a rapid radiation
after the Cretaceous-Paleogene mass extinction event about 66 million
years ago.


Elizabeth Pennisi (2014)
Bird genomes give new perches to old friends.
Comparing genomes clarifies family relations and pinpoints genes for
song learning.
Science 346 (6215): 1275-1276
DOI: 10.1126/science.346.6215.1275

The placement of a strange South American bird called the hoatzin in
the avian family tree is one of the many findings revealed this week
from a massive international project analyzing the sequenced genomes
of 48 bird species representing nearly every order of bird. The
effort, involving 200 people from 80 labs and weeks of supercomputer
time, has yielded the most definitive avian family tree yet. It has
also pinpointed gene networks underlying the traits that make birds
birds, such as feathers and beaks instead of teeth. In one provocative
finding, a team has identified the gene network that underlies complex
singing in birds—and found that the same network operates in humans,
where it is presumably crucial to language. Already, 200 more bird
genomes have been sequenced, with more waiting in the wings.


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