Comparative genomics reveals insights into avian genome evolution and adaptation - PubMed (original) (raw)

. 2014 Dec 12;346(6215):1311-20.

doi: 10.1126/science.1251385. Epub 2014 Dec 11.

Cai Li 2, Qiye Li 2, Bo Li 3, Denis M Larkin 4, Chul Lee 5, Jay F Storz 6, Agostinho Antunes 7, Matthew J Greenwold 8, Robert W Meredith 9, Anders Ödeen 10, Jie Cui 11, Qi Zhou 12, Luohao Xu 13, Hailin Pan 3, Zongji Wang 14, Lijun Jin 3, Pei Zhang 3, Haofu Hu 3, Wei Yang 3, Jiang Hu 3, Jin Xiao 3, Zhikai Yang 3, Yang Liu 3, Qiaolin Xie 3, Hao Yu 3, Jinmin Lian 3, Ping Wen 3, Fang Zhang 3, Hui Li 3, Yongli Zeng 3, Zijun Xiong 3, Shiping Liu 14, Long Zhou 3, Zhiyong Huang 3, Na An 3, Jie Wang 15, Qiumei Zheng 3, Yingqi Xiong 3, Guangbiao Wang 3, Bo Wang 3, Jingjing Wang 3, Yu Fan 16, Rute R da Fonseca 17, Alonzo Alfaro-Núñez 17, Mikkel Schubert 17, Ludovic Orlando 17, Tobias Mourier 17, Jason T Howard 18, Ganeshkumar Ganapathy 18, Andreas Pfenning 18, Osceola Whitney 18, Miriam V Rivas 18, Erina Hara 18, Julia Smith 18, Marta Farré 4, Jitendra Narayan 19, Gancho Slavov 19, Michael N Romanov 20, Rui Borges 7, João Paulo Machado 21, Imran Khan 7, Mark S Springer 22, John Gatesy 22, Federico G Hoffmann 23, Juan C Opazo 24, Olle Håstad 25, Roger H Sawyer 8, Heebal Kim 26, Kyu-Won Kim 27, Hyeon Jeong Kim 28, Seoae Cho 28, Ning Li 29, Yinhua Huang 30, Michael W Bruford 31, Xiangjiang Zhan 32, Andrew Dixon 33, Mads F Bertelsen 34, Elizabeth Derryberry 35, Wesley Warren 36, Richard K Wilson 36, Shengbin Li 37, David A Ray 38, Richard E Green 39, Stephen J O'Brien 40, Darren Griffin 20, Warren E Johnson 41, David Haussler 39, Oliver A Ryder 42, Eske Willerslev 17, Gary R Graves 43, Per Alström 44, Jon Fjeldså 45, David P Mindell 46, Scott V Edwards 47, Edward L Braun 48, Carsten Rahbek 49, David W Burt 50, Peter Houde 51, Yong Zhang 3, Huanming Yang 52, Jian Wang 3; Avian Genome Consortium; Erich D Jarvis 53, M Thomas P Gilbert 54, Jun Wang 55

Collaborators, Affiliations

Comparative genomics reveals insights into avian genome evolution and adaptation

Guojie Zhang et al. Science. 2014.

Abstract

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.

Copyright © 2014, American Association for the Advancement of Science.

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Figures

Fig. 1

Fig. 1. Avian family tree and genomes sequenced

The phylogenomic relationships of the 48 avian genomes from (5), with Sanger-sequenced (black), high-coverage (dark red), and low-coverage (light red) genomes denoted.

Fig. 2

Fig. 2. Genome reduction and conservation in birds

(A) Comparison of average size of introns, exons, and intergenic regions within avian, reptilian, and mammalian genomes. (B) Synteny plot and large segmental deletions between green anole chromosome 2 and multiple chicken chromosomes. Colored bars and lines indicate homologous blocks between two species; black bars indicate location of large avian-specific segmental deletions, which are enriched at the breakpoints of interchromosome rearrangements. (Bottom) An example of a large segmental deletion in birds (represented by ostrich genes). Homologous genes annotated in each species are shown in small boxes. The color spectrum represents the percent identity of homologous genes with the green anole. (C) Distribution of gene synteny percentages identified for phylogenetically independent species pairs of various divergence ages. Dots indicate the percentage of genes remaining in a syntenic block in pairwise comparisons between two avian or mammalian species. Box plots indicate that the overall distributions of the synteny percentages in birds and mammals are different (P value was calculated by using Wilcoxon rank sum test with phylogenetically independent species pairs). (D) Chromosomal organization of the α- and β-globin gene clusters in representative avian and mammalian taxa. These genes encode the α- and β-type subunits of tetrameric (α2β) hemoglobin isoforms that are expressed at different ontogenetic stages. In; the case of the α-like globin genes, birds and mammals share orthologous copies of the α_D_- and α_A_-globin genes. Likewise, the avian π-globin and the mammalian ζ-globin genes are 1:1 orthologs. In contrast, the genes in the avian and mammalian β-globin gene clusters are derived from independent duplications of one or more β-like globin genes that were inherited from the common ancestor of tetrapod vertebrates (90, 91).

Fig. 3

Fig. 3. Evolutionary rate and selection constraints

(A) Substitution rate in each lineage was estimated by the comparison of fourfold degenerate (4d) sites in coding regions, in units of substitutions per site per million years. Waterbirds and landbirds are defined in (5). (B) Correlation between average substitution rates and number of species within different avian orders. Divergence times were estimates from (5).The fit line was derived from least square regression analysis, and the confidence interval was estimated by “stat_smooth” in R. The units of the x axis are numbers of substitutions per site per million years. The correlation figure with phylogenetically independent contrasts is provided in the supplementary materials. (C) Density map for comparison of conservation levels between pan-avian and pan-mammalian genomes, on the basis of the homologous genomic regions between birds and mammals. Conservation levels were quantified by means of PhastCons basewise conservation scores. (D) HCEs found in both mammalian and avian genomes (smaller pie piece) and those that are avian-specific (larger pie piece). (E) MID1 contains abundant avian-specific HCEs in the upstream and downstream regulatory regions. Many regulatory motif elements are identified in these avian-specific HCEs. Cons., conservation level.

Fig. 4

Fig. 4. Selection constraints on genes

(A) Box plot for the distribution of d_N_/d_S_ values of genes on avian macrochromosomes, microchromosomes, and the Z chromosome. P values were calculated with Wilcoxon rank sum tests. (B) GO categories in Neoaves, Galloanserae, and Palaeognathae showing clade-specific rapid evolutionary rates. Red bars, P value of significance; blue bars, number of genes in each GO.

Fig. 5

Fig. 5. Convergent molecular changes among vocal learning birds

(A) Songbird brain diagram showing the specialized forebrain song-learning nuclei (yellow) that controls the production (HVC and RA) and acquisition (LMAN and Area X) of learned song (55). Gray arrows indicate connections between brain regions; red and blue (thick) arrows indicate relative numbers of genes with increased or decreased specialized expression in zebra finch song nuclei and with convergent accelerated coding sequences (left numbers of 66 total) or convergent amino acid substitutions (right numbers of 6). Genes expressed in more than one song nucleus are counted multiple times. RA, robust nucleus of the arcopallium; LMAN, lateral magnocellular nucleus of the anterior nidopallium; Area X, Area X of the striatum; and HVC, a letter-based name. (B) Classification of vocal learner-specific accelerated elements, compared with the background alignment of 15 avian species.

Fig. 6

Fig. 6. Genetic changes associated with ecological adaptations

(A) Copy numbers of α- and β-keratins in humans, reptiles, and birds, including in aquatic birds, land birds, and domesticated birds. Definitions of aquatic and landbirds are provided in (5). (B) Pseudogenization events of the diet-related genes AGT and GULO along the avian phylogeny. (C) Density distribution of d_N_/d_S_ values of the OPN1sw1 gene for mammals (median, 0.21) and birds (median, 0.16). (D) d_N_/d_S_ values of two plumage color–related genes (GSTA2 and SLC24A4) show negative correlation with the color discriminability values (log transformation applied). The correlation figures with phylogenetically independent contrasts are provided in the supplementary materials.

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