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, 346 (6215), 1320-31

Whole-genome Analyses Resolve Early Branches in the Tree of Life of Modern Birds

Erich D Jarvis  1 Siavash Mirarab  2 Andre J Aberer  3 Bo Li  4 Peter Houde  5 Cai Li  6 Simon Y W Ho  7 Brant C Faircloth  8 Benoit Nabholz  9 Jason T Howard  10 Alexander Suh  11 Claudia C Weber  11 Rute R da Fonseca  12 Jianwen Li  13 Fang Zhang  13 Hui Li  13 Long Zhou  13 Nitish Narula  14 Liang Liu  15 Ganesh Ganapathy  10 Bastien Boussau  16 Md Shamsuzzoha Bayzid  2 Volodymyr Zavidovych  10 Sankar Subramanian  17 Toni Gabaldón  18 Salvador Capella-Gutiérrez  19 Jaime Huerta-Cepas  19 Bhanu Rekepalli  20 Kasper Munch  21 Mikkel Schierup  21 Bent Lindow  12 Wesley C Warren  22 David Ray  23 Richard E Green  24 Michael W Bruford  25 Xiangjiang Zhan  26 Andrew Dixon  27 Shengbin Li  28 Ning Li  29 Yinhua Huang  29 Elizabeth P Derryberry  30 Mads Frost Bertelsen  31 Frederick H Sheldon  32 Robb T Brumfield  32 Claudio V Mello  33 Peter V Lovell  34 Morgan Wirthlin  34 Maria Paula Cruz Schneider  35 Francisco Prosdocimi  36 José Alfredo Samaniego  12 Amhed Missael Vargas Velazquez  12 Alonzo Alfaro-Núñez  12 Paula F Campos  12 Bent Petersen  37 Thomas Sicheritz-Ponten  37 An Pas  38 Tom Bailey  39 Paul Scofield  40 Michael Bunce  41 David M Lambert  17 Qi Zhou  42 Polina Perelman  43 Amy C Driskell  44 Beth Shapiro  24 Zijun Xiong  13 Yongli Zeng  13 Shiping Liu  13 Zhenyu Li  13 Binghang Liu  13 Kui Wu  13 Jin Xiao  13 Xiong Yinqi  13 Qiuemei Zheng  13 Yong Zhang  13 Huanming Yang  45 Jian Wang  45 Linnea Smeds  11 Frank E Rheindt  46 Michael Braun  47 Jon Fjeldsa  48 Ludovic Orlando  12 F Keith Barker  49 Knud Andreas Jønsson  50 Warren Johnson  51 Klaus-Peter Koepfli  52 Stephen O'Brien  53 David Haussler  54 Oliver A Ryder  55 Carsten Rahbek  56 Eske Willerslev  12 Gary R Graves  57 Travis C Glenn  58 John McCormack  59 Dave Burt  60 Hans Ellegren  11 Per Alström  61 Scott V Edwards  62 Alexandros Stamatakis  63 David P Mindell  64 Joel Cracraft  65 Edward L Braun  66 Tandy Warnow  67 Wang Jun  68 M Thomas P Gilbert  69 Guojie Zhang  70

Whole-genome Analyses Resolve Early Branches in the Tree of Life of Modern Birds

Erich D Jarvis et al. Science.


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.

Conflict of interest statement

R.E.G. declares that he is President of Dovetail Genomics, with no conflicts of interest.


Fig. 1
Fig. 1. Genome-scale phylogeny of birds
The dated TENT inferred with ExaML. Branch colors denote well-supported clades in this and other analyses. All BS values are 100% except where noted. Names on branches denote orders (-iformes) and English group terms (in parentheses); drawings are of the specific species sequenced (names in table S1 and fig. S1). Order names are according to (36, 37) (SM6). To the right are superorder (-imorphae) and higher unranked names. In some groups, more than one species was sequenced, and these branches have been collapsed (noncollapsed version in fig. S1). Text color denotes groups of species with broadly shared traits, whether by homology or convergence.The arrow indicates the K-Pg boundary at 66 Ma, with the Cretaceous period shaded at left. The gray dashed line represents the approximate end time ( Ma) by which nearly all neoavian orders diverged. Horizontal gray bars on each node indicate the 95% credible interval of divergence time in millions of years.
Fig. 2
Fig. 2. Metatable analysis of species trees
Results for different genomic partitions, methods, and data types are consistent with or contradict clades in our TENT ExaML, TENT MP-EST* and exon-only trees and previous studies of morphology (15), DNA-DNA hybridization (24), mitochondrial genes (14), and nuclear genes (17). Letters (A to DD and a to e) denote clade nodes highlighted in Fig. 3, A and B, of the ExaML and MP-EST* TENT trees. Each column represents a species tree; each row represents a potential clade. Blue-green signifies the monophyly of a clade, and shades show the level of its BS (0 to 100%). Red, rejection of a clade; white, missing data. We used a 95% cut-off (instead of a standard 75%) for strong rejection due to higher support values with genome-scale data. The threshold for the mitochondrial study was set to 99% due to Bayesian posterior probabilities yielding higher values than BS. An expanded metatable showing partitioned ExaML, unbinned MP-EST, and additional codon tree analyses is shown in fig. S2.
Fig. 3
Fig. 3. Evidence of ILS
(A) Cladogram of ExaML TENT avian species tree, annotated for nodes from Fig. 2 (letters), for branches with less than 100% BS without and with (parentheses) third codon positions, for strong (>75% BS) intron gene tree incongruence and congruence, and for indel congruence on all branches (except the root). Thin branch lines represent those not present in the MP-EST* TENT of (B). (Inset) ExaML branch lengths in substitution units (expanded view in fig. S7). Color coding of branches and species is as in Fig. 1. (B) Cladogram of MP-EST* TENT species tree, annotated similarly as in the ExaML TENT in (A). Thin branch lines represent those not present in the ExaML TENT of (A). (C) Percent of intron gene trees rejecting (≥75% BS) branches in the ExaML TENT species tree relative to branch lengths. Letters denote nodes in (A) that either have less than 100% support or are different from the MP-EST* TENT in (B). (D) Percent of intron gene trees supporting (≥75% BS) branches in the ExaML TENT species tree relative to branch lengths. (E) Indel hemiplasy [the inverse of percent of retention index (RI) = 1.0 indels that support the branch; see SM9] correlated with ExaML TENT branch length (log transformed). r2, correlation coefficient. (F) Indel hemiplasy correlated with ExaML and MP-EST TENT internal branch divergence times in millions of years (log transformed). Plotting with internal branch times was necessary to compare both trees (SM9). (G) TE hemiplasy with owls among the core landbirds. Line color, shared TE tree topology; line thickness, relative proportion of TEs that support a specific topology (total numbers shown in the owl node). Circles at end of lines indicate loss of the TE allele in that species after ILS, as the sequence assembly contains an empty TE insertion site (SM10). Only topologies with two or more TEs are shown. (H) TE hemiplasy with songbirds among the core landbirds.
Fig. 4
Fig. 4. Species trees inferred from concatenation of different genomic partitions
(A) Intron tree. (B) UCE tree. (C) Exon c12 tree. (D) Exon c123 tree. The tree with the highest likelihood for each ExaML analysis is shown. Color coding of branches and species is as in Fig. 1 and fig. S1. Thick branches denote those present in the ExaML TENT. Numbers give the percent of BS.
Fig. 5
Fig. 5. Comparisons of total support among species trees and gene trees
(A) Average BS across all branches of species trees from varying input data as in Fig. 2, ordered left to right from lowest to highest values. (B) Numbers of incompatible branches (out of 45 internal), at different support thresholds, with the ExaML TENT tree, ordered left to right from most to least compatible (expanded analysis in fig. S6). (C) Analyses of intron, exon, and UCE gene tree congruence and incongruence with nodes in the ExaML TENT, MP-EST* TENT, and other species trees. Names and letters for clades are as in Figs. 2 and 3. “Missing” denotes the case in which an ortholog is not present for any taxa or is present for only one taxon, and hence monophyly cannot be determined. “Partially missing” indicates the case in which some taxa are missing but at least two of the taxa are present, and thus we can still categorize it as either monophyletic or not. For further details, see SM7.
Fig. 6
Fig. 6. Life history incongruence in protein-coding trees
(A) Species tree inferred from low-base composition variance exons (n = 830 genes) graphed with branch length, third codon position GC (GC3) content (heatmap), and log of body mass (numbers on branches). (B) Species tree inferred from high-base composition variance exons (n = 830 genes), graphed similarly as in (A). The %GC3 scale is higher and ~10 times wider for the high-variance genes, and the branch lengths are ~3 times longer [black scales at the bottom of (A) and (B)]. Color coding of species’ names is as in Fig. 1. Cladograms of trees in (A) and (B) are in figs. S16, A and B. (C and D) Correlations of branch length with GC content (C) and body mass (D) of the low-variance and high-variance exons. Correlations were still significant after independent contrast analyses for phylogenetic relationships (SM11). (E and F) Relative chromosome positions of the low-variance (E) and high-variance (F) exons normalized between 0 and 1 for all chicken chromosomes and separated into 100 bins (bars). The height of each bar represents the number of genes in that specific relative location. The two distributions in (E) and (F) are significantly different (P < 2.2 × 10−16, Wilcoxon rank sum test on grouped values). For further details, see SM11.

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