Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds

Zong-Ji Wang; Guang-Ji Chen; Guo-Jie Zhang; Qi Zhou

doi:10.24272/j.issn.2095-8137.2020.175

Volume 42 Issue 1

Jan. 2021

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Zong-Ji Wang, Guang-Ji Chen, Guo-Jie Zhang, Qi Zhou. Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds. Zoological Research, 2021, 42(1): 51-61. doi: 10.24272/j.issn.2095-8137.2020.175

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Zong-Ji Wang, Guang-Ji Chen, Guo-Jie Zhang, Qi Zhou. Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds. Zoological Research, 2021, 42(1): 51-61. doi: 10.24272/j.issn.2095-8137.2020.175

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Dynamic evolution of transposable elements, demographic history, and gene content of paleognathous birds

doi: 10.24272/j.issn.2095-8137.2020.175

Zong-Ji Wang^{1, 2, 3, 4},
Guang-Ji Chen⁴,
Guo-Jie Zhang^{4, 5, 6, 7
,
,},
Qi Zhou^{2, 3, 8
,
,}

1.
Institute of Animal Sex and Development, Zhejiang Wanli University, Ningbo, Zhejiang 315100, China
2.
MOE Laboratory of Biosystems Homeostasis & Protection, Life Sciences Institute, Zhejiang University, Hangzhou, Zhejiang 310058, China
3.
Department of Neuroscience and Developmental Biology, University of Vienna, Vienna 1090, Austria
4.
BGI-Shenzhen, Beishan Industrial Zone, Shenzhen, Guangdong 518083, China
5.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China
6.
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark
7.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan 650223, China
8.
Center for Reproductive Medicine, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310058, China

Funds: This study was supported by the National Natural Science Foundation of China (31671319, 31722050, 32061130208), Natural Science Foundation of Zhejiang Province (LD19C190001), and European Research Council Starting Grant (grant agreement 677696) to Q.Z.; the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31020000, XDB13000000), International Partnership Program of Chinese Academy of Sciences (152453KYSB20170002), Carlsberg Foundation (CF16-0663), and Villum Foundation (25900) to G.J.Z.

More Information

Corresponding author: E-mail: Guojie.Zhang@bio.ku.dk; zhouqi1982@zju.edu.cn
Received Date: 2020-07-01
Accepted Date: 2020-10-22

Published Online: 2020-10-16

Publish Date: 2021-01-18

Abstract

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.
- Paleognaths,
- Demographic history,
- Transposable elements,
- Gene families,
- Mitochondria

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References(46)

References

[1]	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
[2]	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.
[3]	Angst D, Buffetaut E. 2017. Paleobiology of Giant Flightless Birds. Oxford: Elsevier.
[4]	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
[5]	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
[6]	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
[7]	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
[8]	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
[9]	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
[10]	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
[11]	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
[12]	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
[13]	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
[14]	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
[15]	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
[16]	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
[17]	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
[18]	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
[19]	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
[20]	Kent WJ. 2002. BLAT—the BLAST-like alignment tool. Genome Research, 12(4): 656−664. doi: 10.1101/gr.229202
[21]	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
[22]	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.
[23]	Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature, 475(7357): 493−496. doi: 10.1038/nature10231
[24]	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
[25]	Lynch M. 2007. The Origins of Genome Architecture. Sunderland, MA: Sinauer Associates.
[26]	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
[27]	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
[28]	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
[29]	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
[30]	Pigozzi MI. 1999. Origin and evolution of the sex chromosomes in birds. Biocell, 23(2): 79−95.
[31]	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
[32]	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
[33]	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
[34]	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
[35]	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
[36]	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
[37]	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
[38]	Takagi N, Itoh M, Sasaki M. 1972. Chromosome studies in four species of Ratitae (Aves). Chromosoma, 36(3): 281−291.
[39]	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
[40]	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
[41]	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.
[42]	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
[43]	Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8): 1586−1591. doi: 10.1093/molbev/msm088
[44]	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
[45]	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
[46]	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