Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds
摘要: 古颚类鸟类包括平胸目和䳍形目，对它们的研究有助于我们对鸟类早期演化的了解。我们通过对古颚类15个物种全基因组序列的分析来重构其种群演化历史。除了分布在澳大利亚，新西兰和南美洲最南端的物种，我们发现，自上个冰川期开始以来，大多数古鄂类物种的种群数量都减少了。基因组转座元件不同程度的收缩和扩增塑造了古颚类的基因组结构，相对于平胸目，䳍形目的转座子有更高的丢失速率。大约3000万年前，AviRTE重复序列可能发生了从热带寄生虫向小穴䳍和波斑穴䳍祖先的水平转移。我们对基因家族的分析确定了与免疫和繁殖相关基因的快速变化，但是没有发现平胸目飞行趋同退化的基因家族变化。我们还发现线粒体基因在䳍形目中的进化速率高于平胸目，前者的W染色体退化地更严重。该结果可以通过W染色体和线粒体因为遗传连锁受到希尔·罗伯森干涉效应的影响来解释。综上，我们重建了古颚类种群，基因和转座元件的演化历史。线粒体和W染色体共同演化的发现突出了ZW性染色体物种与XY性染色体物种之间基因组进化的关键差异。Abstract: Palaeognathae includes ratite and tinamou species that are important for understanding early avian evolution. Here, we analyzed the whole-genome sequences of 15 paleognathous species to infer their demographic histories, which are presently unknown. We found that most species showed a reduction of population size since the beginning of the last glacial period, except for those species distributed in Australasia and in the far south of South America. Different degrees of contraction and expansion of transposable elements (TE) have shaped the paleognathous genome architecture, with a higher transposon removal rate in tinamous than in ratites. One repeat family, AviRTE, likely underwent horizontal transfer from tropical parasites to the ancestor of little and undulated tinamous about 30 million years ago. Our analysis of gene families identified rapid turnover of immune and reproduction-related genes but found no evidence of gene family changes underlying the convergent evolution of flightlessness among ratites. We also found that mitochondrial genes have experienced a faster evolutionary rate in tinamous than in ratites, with the former also showing more degenerated W chromosomes. This result can be explained by the Hill-Robertson interference affecting genetically linked W chromosomes and mitochondria. Overall, we reconstructed the evolutionary history of the Palaeognathae populations, genes, and TEs. Our findings of co-evolution between mitochondria and W chromosomes highlight the key difference in genome evolution between species with ZW sex chromosomes and those with XY sex chromosomes.
Figure 1. Continental distributions of paleognathous species investigated in this study
Species range information of studied paleognaths (ratites and tinamous) was retrieved from MAP OF LIFE (https://mol.org/). All bird icons were ordered from https://www.hbw.com/. Points indicate their rough distribution range.
Figure 2. Dynamic changes in effective population size
Red curve of each species is the population size dynamics inferred from PSMC analyses, with pink curves indicating variation in population size derived from 100 bootstraps. Gray shaded areas indicate last glacial period (LGP). We also aligned species range information (https://mol.org/) to each panel.
Figure 3. Temporal evolution of transposable elements of paleognaths
Patterns of eight out of 15 studied Palaeognathae species are shown here. The remaining species, whose patterns were very similar to the eight species, are included in Supplementary Figures S1, S3. A, B: Inferred bursts of certain subfamilies of DNA transposons (in black-framed color squares) and CR1 LINEs (in squares without black frames) are labelled at corresponding phylogenetic nodes. Histograms show distributions of sequence divergence between each subfamily vs. their consensus sequences. We dated the expansion of certain repeat subfamilies based on their sequence divergence patterns in phylogeny by parsimony. We also dated two horizontal transfers of AviRTE retroposon, one of which has been reported previously (Suh et al., 2016), indicated here in red.
Figure 4. Gene family evolution across Palaeognathae tree
A: Numbers designate number of gene families that have expanded (green) or contracted (red) since split from common ancestor. Most recent common ancestor (MCRA) has 14 999 gene families. Phylogenetic tree based on genome-wide alignments of non-coding sequences, adapted from Wang et al. (2019). B, C: GO-term enrichment analysis of contracted gene families in ostriches (B) and expanded gene families in ancestor of tinamous (C). Bubble color indicates log10 (P-value) (legend in upper left-hand corner). Size of bubble indicates frequency of the GO term in the underlying GOA database (larger ones denote more general terms). Scatterplots were drawn by REVIGO (http://revigo.irb.hr/).
Figure 5. Correlated evolution of mitochondrial genes and W chromosomes among paleognathous species
A: Correlation between evolutionary rates of mitochondrial genes and length ratios of sexually differentiated regions (SDR) over entire chrZ. Each data point represents one paleognathous species. Pearson correlation coefficients (r) are shown for comparison. B: Synonymous substitution rates (dS) of mitochondrial genes (13 genes). Colors refer to ratites (blue), tinamous with moderately degenerated chrW (yellow), and tinamous with highly degenerated chrW (red). C: Branch-specific basal metabolic rates (BMR). Branches are colored according to BMR values obtained through ancestral character estimation using phytools (http://github.com/liamrevell/phytools) package as well as dependent package ape. Red indicates low BMR value and blue indicates high BMR values.
 Abascal F, Corvelo A, Cruz F, Villanueva-Cañas JL, Vlasova A, Marcet-Houben M, et al. 2016. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered iberian lynx. Genome Biology, 17: 251. doi: 10.1186/s13059-016-1090-1  Altimiras J, Lindgren I, Giraldo-Deck LM, Matthei A, Garitano-Zavala Á. 2017. Aerobic performance in tinamous is limited by their small heart. A novel hypothesis in the evolution of avian flight. Scientific Reports, 7(1): 15964.  Angst D, Buffetaut E. 2017. Paleobiology of Giant Flightless Birds. Oxford: Elsevier.  Barrón MG, Fiston-Lavier AS, Petrov DA, González J. 2014. Population genomics of transposable elements in Drosophila. Annual Review of Genetics, 48: 561−581. doi: 10.1146/annurev-genet-120213-092359  Beißbarth T, Speed TP. 2004. GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics, 20(9): 1464−1465. doi: 10.1093/bioinformatics/bth088  Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. 2001. Controlling the false discovery rate in behavior genetics research. Behavioural Brain Research, 125(1-2): 279−284. doi: 10.1016/S0166-4328(01)00297-2  Berlin S, Tomaras D, Charlesworth B. 2007. Low mitochondrial variability in birds may indicate hill–robertson effects on the w chromosome. Heredity, 99(4): 389−396. doi: 10.1038/sj.hdy.6801014  Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, et al. 2013. MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69(2): 313−319. doi: 10.1016/j.ympev.2012.08.023  Bishop CM. 1997. Heart mass and the maximum cardiac output of birds and mammals: Implications for estimating the maximum aerobic power input of flying animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 352(1352): 447−456. doi: 10.1098/rstb.1997.0032  Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 355(1403): 1563−1572. doi: 10.1098/rstb.2000.0717  Churakov G, Grundmann N, Kuritzin A, Brosius J, Makałowski W, Schmitz J. 2010. A novel web-based tint application and the chronology of the primate alu retroposon activity. BMC Evolutionary Biology, 10: 376. doi: 10.1186/1471-2148-10-376  De Bie T, Cristianini N, Demuth JP, Hahn MW. 2006. CAFE: a computational tool for the study of gene family evolution. Bioinformatics, 22(10): 1269−1271. doi: 10.1093/bioinformatics/btl097  Demuth JP, De Bie T, Stajich JE, Cristianini N, Hahn MW. 2006. The evolution of mammalian gene families. PLoS One, 1(1): e85. doi: 10.1371/journal.pone.0000085  DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics, 43(5): 491−498. doi: 10.1038/ng.806  Hahn MW, Han MV, Han SG. 2007. Gene family evolution across 12 Drosophila genomes. PLoS Genetics, 3(11): e197. doi: 10.1371/journal.pgen.0030197  Handford P, Mares MA. 1985. The mating systems of ratites and tinamous: an evolutionary perspective. Biological Journal of the Linnean Society, 25(1): 77−104. doi: 10.1111/j.1095-8312.1985.tb00387.x  Houde P. 1986. Ostrich ancestors found in the northern hemisphere suggest new hypothesis of ratite origins. Nature, 324(6097): 563−565. doi: 10.1038/324563a0  Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. 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  Kapusta A, Suh A, Feschotte C. 2017. Dynamics of genome size evolution in birds and mammals. Proceedings of the National Academy of Sciences of the United States of America, 114(8): E1460−E1469. doi: 10.1073/pnas.1616702114  Kent WJ. 2002. BLAT—the BLAST-like alignment tool. Genome Research, 12(4): 656−664. doi: 10.1101/gr.229202  Le Duc D, Renaud G, Krishnan A, Almén MS, Huynen L, Prohaska SJ, et al. 2015. Kiwi genome provides insights into evolution of a nocturnal lifestyle. Genome Biology, 16(1): 147. doi: 10.1186/s13059-015-0711-4  Li H, Coghlan A, Ruan J, Coin LJ, Hériché JK, Osmotherly L, et al. 2006. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Research, 34(S1): D572−D580.  Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature, 475(7357): 493−496. doi: 10.1038/nature10231  Löytynoja A, Goldman N. 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proceedings of the National Academy of Sciences of the United States of America, 102(30): 10557−10562. doi: 10.1073/pnas.0409137102  Lynch M. 2007. The Origins of Genome Architecture. Sunderland, MA: Sinauer Associates.  Nadachowska-Brzyska K, Li C, Smeds L, Zhang GJ, Ellegren H. 2015. Temporal dynamics of avian populations during pleistocene revealed by whole-genome sequences. Current Biology, 25(10): 1375−1380. doi: 10.1016/j.cub.2015.03.047  O’Connor RE, Farré M, Joseph S, Damas J, Kiazim L, Jennings R, et al. 2018. Chromosome-level assembly reveals extensive rearrangement in saker falcon and budgerigar, but not ostrich, genomes. Genome Biology, 19(1): 171. doi: 10.1186/s13059-018-1550-x  Ogawa A, Murata K, Mizuno S. 1998. The location of Z-and W-linked marker genes and sequence on the homomorphic sex chromosomes of the ostrich and the emu. Proceedings of the National Academy of Sciences of the United States of America, 95(8): 4415−4418. doi: 10.1073/pnas.95.8.4415  Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in r language. Bioinformatics, 20(2): 289−290. doi: 10.1093/bioinformatics/btg412  Pigozzi MI. 1999. Origin and evolution of the sex chromosomes in birds. Biocell, 23(2): 79−95.  Pigozzi MI, Solari AJ. 1999. The ZW pairs of two paleognath birds from two orders show transitional stages of sex chromosome differentiation. Chromosome Research, 7(7): 541−551. doi: 10.1023/A:1009241528994  Sackton TB, Grayson P, Cloutier A, Hu ZR, Liu JS, Wheeler NE, et al. 2019. Convergent regulatory evolution and loss of flight in paleognathous birds. Science, 364(6435): 74−78. doi: 10.1126/science.aat7244  Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG. 2007. Dynamic evolution of the innate immune system in Drosophila. Nature Genetics, 39(12): 1461−1468. doi: 10.1038/ng.2007.60  Shetty S, Griffin DK, Graves JAM. 1999. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Research, 7(4): 289−295. doi: 10.1023/A:1009278914829  Smeds L, Warmuth V, Bolivar P, Uebbing S, Burri R, Suh A, et al. 2015. Evolutionary analysis of the female-specific avian w chromosome. Nature Communications, 6: 7330. doi: 10.1038/ncomms8330  Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, Brosius J, et al. 2011. Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nature Communications, 2: 443. doi: 10.1038/ncomms1448  Suh A, Witt CC, Menger J, Sadanandan KR, Podsiadlowski L, Gerth M, et al. 2016. Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes. Nature Communications, 7: 11396. doi: 10.1038/ncomms11396  Takagi N, Itoh M, Sasaki M. 1972. Chromosome studies in four species of Ratitae (Aves). Chromosoma, 36(3): 281−291.  Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56(4): 564−577. doi: 10.1080/10635150701472164  Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y. 2007. Comparison of the z and w sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma, 116(2): 159−173. doi: 10.1007/s00412-006-0088-y  Wang ZJ, Zhang JL, Xu XM, Witt C, Deng Y, Chen GJ, et al. 2019. Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds. bioRxiv. doi: 10.1101/750109.  Wright NA, Gregory TR, Witt CC. 2014. Metabolic ‘engines’ of flight drive genome size reduction in birds. Proceedings of the Royal Society B: Biological Sciences, 281(1779): 20132780. doi: 10.1098/rspb.2013.2780  Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8): 1586−1591. doi: 10.1093/molbev/msm088  Young JJ, Grayson P, Edwards SV, Tabin CJ. 2019. Attenuated fgf signaling underlies the forelimb heterochrony in the emu Dromaius novaehollandiae. Current Biology, 29(21): 3681−3691.e5. doi: 10.1016/j.cub.2019.09.014  Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, et al. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215): 1311−1320. doi: 10.1126/science.1251385  Zhou Q, Zhang JL, Bachtrog D, An N, Huang QF, Jarvis ED, et al. 2014. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science, 346(6215): 1246338. doi: 10.1126/science.1246338
ZR-2020-175 Supplementary materials.zip