适应性演化的分子遗传机制：以高海拔适应为例

doi:10.16288/j.yczz.22-108

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Hereditas(Beijing) ›› 2022, Vol. 44 ›› Issue (8): 635-654.doi: 10.16288/j.yczz.22-108

• Special Section: Excellent Doctoral Thesis • Previous Articles Next Articles

Genetic mechanism of adaptive evolution: the example of adaptation to high altitudes

Yan Hao¹, Fumin Lei^1,^2,³()

1. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
2. College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
3. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China

Received:2022-04-13 Revised:2022-06-25 Online:2022-08-20 Published:2022-07-19
Contact: Lei Fumin E-mail:leifm@ioz.ac.cn
Supported by:
Supported by the National Natural Science Foundation of China Nos(32100332, 3213000355);the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program No(2019QZKK0304);the Young Elite Scientists Sponsorship Program by CAST No(2021QNRC001);the China Postdoctoral Science Foundation No(2021M700144)

Abstract

Abstract:

Since Darwin’s time, elucidating the mechanism of adaptive evolution has been one of the most important scientific issues in evolutionary biology and ecology. Adaptive evolution usually means that species evolve special phenotypic traits to increase fitness under selective pressures. Phenotypic adaptation can be observed at different hierarchical levels of morphology, physiology, biochemistry, histology, and behavior. With the breakthroughs of molecular biology and next-generation sequencing technologies, mounting evidence has uncovered the genetic architecture driving adaptive complex phenotypes. Studying the molecular genetic mechanisms of evolutionary adaption will enable us to understand the forces shaping biodiversity and set up genotype-phenotype-environment interactions. Genetic bases of adaptive evolution have been explained by multiple hypotheses, including major-effect genes, supergenes, polygenicity, noncoding regions, repeated regions, and introgression. The strong selection pressure exerted by high-altitude extreme environments greatly promotes the occurrence of phenotypic and genetic adaptation in species. Studies on multi-omics data provide new insights into adaptive evolution. In this review, we systematically summarize the genetic mechanism of adaptive evolution, research progress in adaptation to high-altitude environmental conditions, and existing challenges and discuss the future perspectives, thereby providing guidance for researchers in this field.

Key words: phenotype, noncoding region, multi-omics, regulation, high altitudes

Yan Hao, Fumin Lei. Genetic mechanism of adaptive evolution: the example of adaptation to high altitudes[J]. Hereditas(Beijing), 2022, 44(8): 635-654.

Figures/Tables 2

Fig. 1

Table 1

Case studies of high-altitude adaptation"

类群	物种	测序技术	主要支持的假说	参考文献
人类	藏人(Homo sapiens)	Affymetrix 6.0 SNP Array	主效基因假说	[92,95]
	藏人(Homo sapiens)	Illumina 610-Quad Genotyping Array	主效基因假说	[93]
	藏人(Homo sapiens)	Affymetrix 6.0 SNP Array和Illumina HiSeq (resequencing和RNA-seq)	主效基因假说	[94]
	藏人(Homo sapiens)	Illumina CoreExome Array	主效基因假说	[96]
	藏人(Homo sapiens)	Illumina HiSeq (RNA-seq、ATAC-seq、Resequencing和Hi-C)	非编码区调控假说	[53]
	藏人(Homo sapiens)	Illumina HiSeq (resequencing)	基因渐渗假说	[116]
哺乳类	高原鼢鼠(Myospalax baileyi)和高原鼠兔(Ochotona curzoniae)	Illumina HiSeq (whole-genome sequencing)	主效基因假说	[79]
	牦牛(Bos grunniens)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[97]
	滇金丝猴(Rhinopithecus bieti)、怒江金丝猴(Rhinopithecus strykeri )和川金丝猴(Rhinopithecus roxellana)	Illumina HiSeq (whole-genome sequencing、RNA-seq和resequencing)	多基因遗传假说	[98]
	藏灰狼(Canis lupus chanco)	Illumina HiSeq (resequencing)	多基因遗传假说	[99]
	高原鼢鼠(Myospalax baileyi)	Pacific Biosciences (PacBio) RS II (whole- genome sequencing)和Illumina HiSeq (whole- genome sequencing和resequencing)	多基因遗传假说	[80]
	藏獒(Canis lupus familiaris)	Illumina HiSeq (whole-genome sequencing)	基因渐渗假说	[117]
鸟类	地山雀(Pseudopodoces humilis)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[100]
	地山雀(Pseudopodoces humilis)、白眉山雀(Poecile superciliosus)、褐冠山雀(Lophophanes dichrous)和黑冠山雀(Periparus rubidiventris)	Illumina HiSeq (resequencing)	多基因遗传假说	[101]
	褐冠山雀(Lophophanes dichrous)、黑冠山雀(Periparus rubidiventris)和棕额长尾山雀(Aegithalos iouschistos)	Illumina HiSeq (RNA-seq)	非编码区调控假说	[115]
	白腰雪雀(Onychostruthus taczanowskii)、棕颈雪雀(Pyrgilauda ruficollis)和褐翅雪雀(Montifringilla adamsi)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[85]
	树麻雀(Passer montanus)	Illumina HiSeq (whole-genome sequencing和resequencing)	多基因遗传假说	[43]
	绿尾虹雉(Lophophorus lhuysii)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[102]
	黑颈鹤(Grus nigricollis)	Oxford Nanopore Technologies (ONT) PromethION (whole-genome sequencing)和Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[103]
	四川雉鹑(Tetraophasis szechenyii)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[104]
鱼类	厚唇裸重唇鱼 (Gymnodiptychus pachycheilus)	Illumina HiSeq (RNA-seq)	多基因遗传假说	[105]
鱼类	达里湖高原鳅(Triplophysa dalaica)、拟鲶高原鳅(Triplophysa siluroides)和硬刺高原鳅(Triplophysa scleroptera)	Illumina HiSeq (RNA-seq)	多基因遗传假说	[106,107]
两栖类	高山倭蛙(Nanorana parkeri)	Illumina HiSeq (whole-genome sequencing)	多基因遗传假说	[108]
两栖类	高山倭蛙(Nanorana parkeri)、棘臂蛙(Nanorana liebigii)和双团棘胸蛙(Nanorana phrynoides)	Illumina HiSeq (RNA-seq)	多基因遗传假说	[109]
爬行类	青海沙蜥(Phrynocephalus vlangalii)、红尾沙蜥(Phrynocephalus erythrurus)和贵德沙蜥(Phrynocephalus putjatia)	Illumina HiSeq (RNA-seq)	多基因遗传假说	[109]
爬行类	温泉蛇(Thermophis baileyi)、四川温泉蛇(Thermophis zhaoermii)和香格里拉温泉蛇(Thermophis shangrila)	Illumina HiSeq (whole-genome sequencing和resequencing)	多基因遗传假说	[110]

Table 1

References 132

[1]	Svensson EI, Berger D. The role of mutation bias in adaptive evolution. Trends Ecol Evol, 2019, 34(5): 422-434. doi: S0169-5347(19)30030-8 pmid: 31003616
[2]	Darwin CR. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray, 1859.
[3]	Morgan T. The Scientiﬁc Basis of Evolution. London: Faber and Faber, Ltd., 1932.
[4]	Nei M. Molecular Evolutionary Genetics. New York: Columbia University Press, 1987.
[5]	Kimura M. Evolutionary rate at the molecular level. Nature, 1968, 217(5129): 624-626. doi: 10.1038/217624a0
[6]	Nei M. Selectionism and neutralism in molecular evolution. Mol Biol Evol, 2005, 22(12): 2318-2342. doi: 10.1093/molbev/msi242
[7]	Feng SH, Stiller J, Deng Y, Armstrong J, Fang Q, Reeve AH, Xie D, Chen GJ, Guo CX, Faircloth BC, Petersen B, Wang ZJ, Zhou Q, Diekhans M, Chen WJ, Andreu-Sánchez S, Margaryan A, Howard JT, Parent C, Pacheco G, Sinding MHS, Puetz L, Cavill E, Ribeiro ÂM, Eckhart L, Fjeldså J, Hosner PA, Brumfield RT, Christidis L, Bertelsen MF, Sicheritz-Ponten T, Tietze DT, Robertson BC, Song G, Borgia G, Claramunt S, Lovette IJ, Cowen SJ, Njoroge P, Dumbacher JP, Ryder OA, Fuchs J, Bunce M, Burt DW, Cracraft J, Meng GL, Hackett SJ, Ryan PG, Jønsson KA, Jamieson IG, da Fonseca RR, Braun EL, Houde P, Mirarab S, Suh A, Hansson B, Ponnikas S, Sigeman H, Stervander M, Frandsen PB, van der Zwan H, van der Sluis R, Visser C, Balakrishnan CN, Clark AG, Fitzpatrick JW, Bowman R, Chen N, Cloutier A, Sackton TB, Edwards SV, Foote DJ, Shakya SB, Sheldon FH, Vignal A, Soares AER, Shapiro B, González-Solís J, Ferrer-Obiol J, Rozas J, Riutort M, Tigano A, Friesen V, Dalén L, Urrutia AO, Székely T, Liu Y, Campana MG, Corvelo A, Fleischer RC, Rutherford KM, Gemmell NJ, Dussex N, Mouritsen H, Thiele N, Delmore K, Liedvogel M, Franke A, Hoeppner MP, Krone O, Fudickar AM, Milá B, Ketterson ED, Fidler AE, Friis G, Parody-Merino ÁM, Battley PF, Cox MP, Lima NCB, Prosdocimi F, Parchman TL, Schlinger BA, Loiselle BA, Blake JG, Lim HC, Day LB, Fuxjager MJ, Baldwin MW, Braun MJ, Wirthlin M, Dikow RB, Ryder TB, Camenisch G, Keller LF, DaCosta JM, Hauber ME, Louder MIM, Witt CC, McGuire JA, Mudge J, Megna LC, Carling MD, Wang B, Taylor SA, Del-Rio G, Aleixo A, Vasconcelos ATR, Mello CV, Weir JT, Haussler D, Li QY, Yang HM, Wang J, Lei FM, Rahbek C, Gilbert MTP, Graves GR, Jarvis ED, Paten B, Zhang GJ. Dense sampling of bird diversity increases power of comparative genomics. Nature, 2020, 587(7833): 252-257.
[8]	Consortium Z. A comparative genomics multitool for scientific discovery and conservation. Nature, 2020, 587(7833): 240-245. doi: 10.1038/s41586-020-2876-6
[9]	Chen L, Qiu Q, Jiang Y, Wang K, Lin ZS, Li ZP, Bibi F, Yang YZ, Wang JH, Nie WH, Su WT, Liu GC, Li QY, Fu WW, Pan XY, Liu C, Yang J, Zhang CZ, Yin Y, Wang Y, Zhao Y, Zhang C, Wang ZK, Qin YL, Liu W, Wang B, Ren YD, Zhang R, Zeng Y, da Fonseca RR, Wei B, Li R, Wan WT, Zhao RP, Zhu WB, Wang YT, Duan SC, Gao Y, Zhang YE, Chen CY, Hvilsom C, Epps CW, Chemnick LG, Dong Y, Mirarab S, Siegismund HR, Ryder OA, Gilbert MTP, Lewin HS, Zhang GJ, Heller R, Wang W. Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science, 2019, 364(6446): eaav6202.
[10]	Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu LH, Pan HL, Wang ZJ, Jin LJ, Zhang P, Hu HF, Yang W, Hu J, Xiao J, Yang ZK, Liu Y, Xie QL, Yu H, Lian JM, Wen P, Zhang F, Li H, Zeng YL, Xiong ZJ, Liu SP, Zhou L, Huang ZY, An N, Wang J, Zheng QM, Xiong YQ, Wang GB, Wang B, Wang JJ, Fan Y, da Fonseca RR, Alfaro-Núñez A, Schubert M, Orlando L, Mourier T, Howard JT, Ganapathy G, Pfenning A, Whitney O, Rivas MV, Hara E, Smith J, Farré M, Narayan J, Slavov G, Romanov MN, Borges R, Machado JP, Khan I, Springer MS, Gatesy J, Hoffmann FG, Opazo JC, Håstad O, Sawyer RH, Kim H, Kim KW, Kim HJ, Cho S, Li N, Huang YH, Bruford MW, Zhan XJ, Dixon A, Bertelsen MF, Derryberry E, Warren W, Wilson RK, Li SB, Ray DA, Green RE, O'Brien SJ, Griffin D, Johnson WE, Haussler D, Ryder OA, Willerslev E, Graves GR, Alström P, Fjeldså J, Mindell DP, Edwards SV, Braun EL, Rahbek C, Burt DW, Houde P, Zhang Y, Yang HM, Wang J, Avian Genome Consortium, Jarvis ED, Gilbert MTP, Wang J. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 2014, 346(6215): 1311-1320.
[11]	Van't Hof AE, Edmonds N, Dalíková M, Marec F, Saccheri IJ. Industrial melanism in British peppered moths has a singular and recent mutational origin. Science, 2011, 332(6032): 958-960. doi: 10.1126/science.1203043
[12]	Orr HA. The genetic theory of adaptation: a brief history. Nat Rev Genet, 2005, 6(2): 119-127. doi: 10.1038/nrg1523
[13]	Jain K, Stephan W. Modes of rapid polygenic adaptation. Mol Biol Evol, 2017, 34(12): 3169-3175. doi: 10.1093/molbev/msx240
[14]	Messer PW, Petrov DA. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol Evol, 2013, 28(11): 659-669. doi: 10.1016/j.tree.2013.08.003
[15]	Papa R, Martin A, Reed RD. Genomic hotspots of adaptation in butterfly wing pattern evolution. Curr Opin Genet Dev, 2008, 18(6): 559-564. doi: 10.1016/j.gde.2008.11.007
[16]	Cooke TF, Fischer CR, Wu P, Jiang TX, Xie KT, Kuo J, Doctorov E, Zehnder A, Khosla C, Chuong CM, Bustamante CD. Genetic mapping and biochemical basis of yellow feather pigmentation in budgerigars. Cell, 2017, 171(2): 427-439.e21. doi: 10.1016/j.cell.2017.08.016
[17]	Grant PR, Grant BR. How and why species multiply. The radiation of Darwin's finches. Princeton University Press, 2008.
[18]	Bright JA, Marugán-Lobón J, Cobb SN, Rayfield EJ. The shapes of bird beaks are highly controlled by nondietary factors. Proc Natl Acad Sci USA, 2016, 113(19): 5352-5357. doi: 10.1073/pnas.1602683113
[19]	Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. Bmp4 and morphological variation of beaks in Darwin's finches. Science, 2004, 305(5689): 1462-1465. pmid: 15353802
[20]	Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, Promerová M, Rubin CJ, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 2015, 518(7539): 371-375. doi: 10.1038/nature14181
[21]	Cheng YL, Miller MJ, Zhang DZ, Song G, Jia CX, Qu YH, Lei FM. Comparative genomics reveals evolution of a beak morphology locus in a high-altitude songbird. Mol Biol Evol, 2020, 37(10): 2983-2988. doi: 10.1093/molbev/msaa157
[22]	Hunt BG. Supergene evolution: recombination finds a way. Curr Biol, 2020, 30(2): R73-R76. doi: 10.1016/j.cub.2019.12.006
[23]	Gutiérrez-Valencia J, Hughes PW, Berdan EL, Slotte T. The genomic architecture and evolutionary fates of supergenes. Genome Biol Evol, 2021, 13(5): evab057.
[24]	Thompson MJ, Jiggins CD. Supergenes and their role in evolution. Heredity (Edinb), 2014, 113(1): 1-8. doi: 10.1038/hdy.2014.20
[25]	Schwander T, Libbrecht R, Keller L. Supergenes and complex phenotypes. Curr Biol, 2014, 24(7): R288-R294. doi: 10.1016/j.cub.2014.01.056
[26]	Xu LH, Auer G, Peona V, Suh A, Deng Y, Feng SH, Zhang GJ, Blom MPK, Christidis L, Prost S, Irestedt M, Zhou Q. Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds. Nat Ecol Evol, 2019, 3(5): 834-844. doi: 10.1038/s41559-019-0850-1
[27]	Zhou Q, Zhang JL, Bachtrog D, An N, Huang QF, Jarvis ED, Gilbert MTP, Zhang GJ. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science, 2014, 346(6215): 1246338. doi: 10.1126/science.1246338
[28]	Küpper C, Stocks M, Risse JE, Dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, Kitaysky AS, Wingfield JC, Piersma T, Zeng K, Slate J, Blaxter M, Lank DB, Burke T. A supergene determines highly divergent male reproductive morphs in the ruff. Nat Genet, 2016, 48(1): 79-83.
[29]	Lamichhaney S, Fan GY, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi CC, Zhang H, Chen WB, Liang XM, Huang LH, Wang JH, Liang EJ, Wu Q, Lee SMY, Xu X, Höglund J, Liu X, Andersson L. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet, 2016, 48(1): 84-88. doi: 10.1038/ng.3430 pmid: 26569123
[30]	Tuttle EM, Bergland AO, Korody ML, Brewer MS, Newhouse DJ, Minx P, Stager M, Betuel A, Cheviron ZA, Warren WC, Gonser RA, Balakrishnan CN. Divergence and functional degradation of a sex chromosome-like supergene. Curr Biol, 2016, 26(3): 344-350.
[31]	Campagna L. Supergenes: the genomic architecture of a bird with four sexes. Curr Biol, 2016, 26(3): R105-R107. doi: 10.1016/j.cub.2015.12.005
[32]	Tuttle EM. Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence. Behav Ecol, 2003, 14(3): 425-432. doi: 10.1093/beheco/14.3.425
[33]	Funk ER, Mason NA, Pálsson S, Albrecht T, Johnson JA, Taylor SA. A supergene underlies linked variation in color and morphology in a Holarctic songbird. Nat Commun, 2021, 12(1): 6833. doi: 10.1038/s41467-021-27173-z
[34]	Sanchez-Donoso I, Ravagni S, Rodríguez-Teijeiro JD, Christmas MJ, Huang Y, Maldonado-Linares A, Puigcerver M, Jiménez-Blasco I, Andrade P, Gonçalves D, Friis G, Roig I, Webster MT, Leonard JA, Vilà C. Massive genome inversion drives coexistence of divergent morphs in common quails. Curr Biol, 2022, 32(2): 462-469.e6. doi: 10.1016/j.cub.2021.11.019
[35]	Lagunas-Robles G, Purcell J, Brelsford A. Linked supergenes underlie split sex ratio and social organization in an ant. Proc Natl Acad Sci USA, 2021, 118(46): e2101427118.
[36]	Yan Z, Martin SH, Gotzek D, Arsenault SV, Duchen P, Helleu Q, Riba-Grognuz O, Hunt BG, Salamin N, Shoemaker D, Ross KG, Keller L. Evolution of a supergene that regulates a trans-species social polymorphism. Nat Ecol Evol, 2020, 4(2): 240-249. doi: 10.1038/s41559-019-1081-1
[37]	Charlesworth D, Charlesworth B. Mimicry: the hunting of the supergene. Curr Biol, 2011, 21(20): R846-R848. doi: 10.1016/j.cub.2011.09.004
[38]	Zhang W, Westerman E, Nitzany E, Palmer S, Kronforst MR. Tracing the origin and evolution of supergene mimicry in butterflies. Nat Commun, 2017, 8(1): 1269. doi: 10.1038/s41467-017-01370-1 pmid: 29116078
[39]	Sodeland M, Jentoft S, Jorde PE, Mattingsdal M, Albretsen J, Kleiven AR, Synnes AEW, Espeland SH, Olsen EM, Andrè C, Stenseth NC, Knutsen H. Stabilizing selection on Atlantic cod supergenes through a millennium of extensive exploitation. Proc Natl Acad Sci USA, 2022, 119(8): e2114904119.
[40]	Matschiner M, Barth JMI, Tørresen OK, Star B, Baalsrud HT, Brieuc MSO, Pampoulie C, Bradbury I, Jakobsen KS, Jentoft S. Supergene origin and maintenance in Atlantic cod. Nat Ecol Evol, 2022, 6(4): 469-481. doi: 10.1038/s41559-022-01661-x pmid: 35177802
[41]	Todesco M, Owens GL, Bercovich N, Légaré JS, Soudi S, Burge DO, Huang K, Ostevik KL, Drummond EBM, Imerovski I, Lande K, Pascual-Robles MA, Nanavati M, Jahani M, Cheung W, Staton SE, Muños S, Nielsen R, Donovan LA, Burke JM, Yeaman S, Rieseberg LH. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature, 2020, 584(7822): 602-607. doi: 10.1038/s41586-020-2467-6
[42]	Pritchard JK, Pickrell JK, Coop G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol, 2010, 20(4): R208-R215. doi: 10.1016/j.cub.2009.11.055
[43]	Qu YH, Chen CH, Xiong Y, She HS, Zhang YE, Cheng YL, DuBay S, Li DM, Ericson PGP, Hao Y, Wang HY, Zhao HF, Song G, Zhang HL, Yang T, Zhang C, Liang LP, Wu TY, Zhao JY, Gao Q, Zhai WW, Lei FM. Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in Eurasian Tree Sparrows. Natl Sci Rev, 2020, 7(1): 113-127. doi: 10.1093/nsr/nwz138
[44]	Fagny M, Austerlitz F. Polygenic adaptation: integrating population genetics and gene regulatory networks. Trends Genet, 2021, 37(7): 631-638. doi: 10.1016/j.tig.2021.03.005
[45]	Marouli E, Graff M, Medina-Gomez C, Lo KS, Wood AR, Kjaer TR, Fine RS, Lu YC, Schurmann C, Highland HM, Rüeger S, Thorleifsson G, Justice AE, Lamparter D, Stirrups KE, Turcot V, Young KL, Winkler TW, Esko T, Karaderi T, Locke AE, Masca NGD, Ng MCY, Mudgal P, Rivas MA, Vedantam S, Mahajan A, Guo XQ, Abecasis G, Aben KK, Adair LS, Alam DS, Albrecht E, Allin KH, Allison M, Amouyel P, Appel EV, Arveiler D, Asselbergs FW, Auer PL, Balkau B, Banas B, Bang LE, Benn M, Bergmann S, Bielak LF, Blüher M, Boeing H, Boerwinkle E, Böger CA, Bonnycastle LL, Bork-Jensen J, Bots ML, Bottinger EP, Bowden DW, Brandslund I, Breen G, Brilliant MH, Broer L, Burt AA, Butterworth AS, Carey DJ, Caulfield MJ, Chambers JC, Chasman DI, Chen YDI, Chowdhury R, Christensen C, Chu AY, Cocca M, Collins FS, Cook JP, Corley J, Galbany JC, Cox AJ, Cuellar-Partida G, Danesh J, Davies G, de Borst GJ, de Denus S, de Groot MCH, de Mutsert R, Deary IJ, Dedoussis G, Demerath EW, den Hollander AI, Dennis JG, Di Angelantonio E, Drenos F, Du MM, Dunning AM, Easton DF, Ebeling T, Edwards TL, Ellinor PT, Elliott P, Evangelou E, Farmaki AE, Faul JD, Feitosa MF, Feng S, Ferrannini E, Ferrario MM, Ferrieres J, Florez JC, Ford I, Fornage M, Franks PW, Frikke-Schmidt R, Galesloot TE, Gan W, Gandin I, Gasparini P, Giedraitis V, Giri A, Girotto G, Gordon SD, Gordon-Larsen P, Gorski M, Grarup N, Grove ML, Gudnason V, Gustafsson S, Hansen T, Harris KM, Harris TB, Hattersley AT, Hayward C, He L, Heid IM, Heikkilä K, Helgeland Ø, Hernesniemi J, Hewitt AW, Hocking LJ, Hollensted M, Holmen OL, Hovingh GK, Howson JMM, Hoyng CB, Huang PL, Hveem K, Ikram MA, Ingelsson E, Jackson AU, Jansson JH, Jarvik GP, Jensen GB, Jhun MA, Jia YC, Jiang XJ, Johansson S, Jørgensen ME, Jørgensen T, Jousilahti P, Jukema JW, Kahali B, Kahn RS, Kähönen M, Kamstrup PR, Kanoni S, Kaprio J, Karaleftheri M, Kardia SLR, Karpe F, Kee F, Keeman R, Kiemeney LA, Kitajima H, Kluivers KB, Kocher T, Komulainen P, Kontto J, Kooner JS, Kooperberg C, Kovacs P, Kriebel J, Kuivaniemi H, Küry S, Kuusisto J, La Bianca M, Laakso M, Lakka TA, Lange EM, Lange LA, Langefeld CD, Langenberg C, Larson EB, Lee IT, Lehtimäki T, Lewis CE, Li HX, Li J, Li-Gao RF, Lin HH, Lin LA, Lin X, Lind L, Lindström J, Linneberg A, Liu YH, Liu YM, Lophatananon A, Luan JA, Lubitz SA, Lyytikäinen LP, Mackey DA, Madden PAF, Manning AK, Männistö S, Marenne G, Marten J, Martin NG, Mazul AL, Meidtner K, Metspalu A, Mitchell P, Mohlke KL, Mook-Kanamori DO, Morgan A, Morris AD, Morris AP, Müller-Nurasyid M, Munroe PB, Nalls MA, Nauck M, Nelson CP, Neville M, Nielsen SF, Nikus K, Njølstad PR, Nordestgaard BG, Ntalla I, O'Connel JR, Oksa H, Loohuis LMO, Ophoff RA, Owen KR, Packard CJ, Padmanabhan S, Palmer CNA, Pasterkamp G, Patel AP, Pattie A, Pedersen O, Peissig PL, Peloso GM, Pennell CE, Perola M, Perry JA, Perry JRB, Person TN, Pirie A, Polasek O, Posthuma D, Raitakari OT, Rasheed A, Rauramaa R, Reilly DF, Reiner AP, Renström F, Ridker PM, Rioux JD, Robertson N, Robino A, Rolandsson O, Rudan I, Ruth KS, Saleheen D, Salomaa V, Samani NJ, Sandow K, Sapkota Y, Sattar N, Schmidt MK, Schreiner PJ, Schulze MB, Scott RA, Segura-Lepe MP, Shah S, Sim XL, Sivapalaratnam S, Small KS, Smith AV, Smith JA, Southam L, Spector TD, Speliotes EK, Starr JM, Steinthorsdottir V, Stringham HM, Stumvoll M, Surendran P, Hart LM, Tansey KE, Tardif JC, Taylor KD, Teumer A, Thompson DJ, Thorsteinsdottir U, Thuesen BH, Tönjes A, Tromp G, Trompet S, Tsafantakis E, Tuomilehto J, Tybjaerg-Hansen A, Tyrer JP, Uher R, Uitterlinden AG, Ulivi S, van der Laan SW, Van Der Leij AR, van Duijn CM, van Schoor NM, van Setten J, Varbo A, Varga TV, Varma R, Edwards DRV, Vermeulen SH, Vestergaard H, Vitart V, Vogt TF, Vozzi D, Walker M, Wang FJ, Wang CA, Wang S, Wang YQ, Wareham NJ, Warren HR, Wessel J, Willems SM, Wilson JG, Witte DR, Woods MO, Wu Y, Yaghootkar H, Yao J, Yao P, Yerges-Armstrong LM, Young R, Zeggini E, Zhan XW, Zhang WH, Zhao JH, Zhao W, Zhao W, Zheng H, Zhou W, EPIC-InterAct Consortium, CHD Exome+ Consortium, ExomeBP Consortium, T2D-Genes Consortium, GoT2D Genes Consortium, Global Lipids Genetics Consortium, ReproGen Consortium, MAGIC Investigators, Rotter JI, Boehnke M, Kathiresan S, McCarthy MI, Willer CJ, Stefansson K, Borecki IB, Liu DJ, North KE, Heard-Costa NL, Pers TH, Lindgren CM, Oxvig C, Kutalik Z, Rivadeneira F, Loos RJF, Frayling TM, Hirschhorn JN, Deloukas P, Lettre G,. Rare and low-frequency coding variants alter human adult height. Nature, 2017, 542(7640): 186-190.
[46]	Bergey CM, Lopez M, Harrison GF, Patin E, Cohen JA, Quintana-Murci L, Barreiro LB, Perry GH. Polygenic adaptation and convergent evolution on growth and cardiac genetic pathways in African and Asian rainforest hunter-gatherers. Proc Natl Acad Sci USA, 2018, 115(48): E11256-E11263.
[47]	Visconti A, Duffy DL, Liu F, Zhu G, Wu WT, Chen Y, Hysi PG, Zeng CQ, Sanna M, Iles MM, Kanetsky PA, Demenais F, Hamer MA, Uitterlinden AG, Ikram MA, Nijsten T, Martin NG, Kayser M, Spector TD, Han JL, Bataille V, Falchi M. Genome-wide association study in 176,678 Europeans reveals genetic loci for tanning response to sun exposure. Nat Commun, 2018, 9(1): 1684. doi: 10.1038/s41467-018-04086-y pmid: 29739929
[48]	Morgan MD, Pairo-Castineira E, Rawlik K, Canela-Xandri O, Rees J, Sims D, Tenesa A, Jackson IJ. Genome-wide study of hair colour in UK Biobank explains most of the SNP heritability. Nat Commun, 2018, 9(1): 5271. doi: 10.1038/s41467-018-07691-z
[49]	Hysi PG, Valdes AM, Liu F, Furlotte NA, Evans DM, Bataille V, Visconti A, Hemani G, McMahon G, Ring SM, Smith GD, Duffy DL, Zhu G, Gordon SD, Medland SE, Lin BD, Willemsen G, Jan Hottenga J, Vuckovic D, Girotto G, Gandin I, Sala C, Concas MP, Brumat M, Gasparini P, Toniolo D, Cocca M, Robino A, Yazar S, Hewitt AW, Chen Y, Zeng CQ, Uitterlinden AG, Ikram MA, Hamer MA, van Duijn CM, Nijsten T, Mackey DA, Falchi M, Boomsma DI, Martin NG, Hinds DA, Kayser M, Spector TD. Genome-wide association meta-analysis of individuals of European ancestry identifies new loci explaining a substantial fraction of hair color variation and heritability. Nat Genet, 2018, 50(5): 652-656. doi: 10.1038/s41588-018-0100-5
[50]	Carroll SB. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell, 2008, 134(1): 25-36. doi: 10.1016/j.cell.2008.06.030 pmid: 18614008
[51]	King MC, Wilson AC. Evolution at two levels in humans and chimpanzees. Science, 1975, 188(4184): 107-116. pmid: 1090005
[52]	Hao Y, Qu YH, Song G, Lei FM. Genomic insights into the adaptive convergent evolution. Curr Genomics, 2019, 20(2): 81-89. doi: 10.2174/1389202920666190313162702
[53]	Xin JX, Zhang H, He YX, Duren Z, Bai CJ, Chen L, Luo X, Yan DS, Zhang CY, Zhu X, Yuan QY, Feng ZY, Cui CY, Qi XB, Ouzhuluobu, Wong WH, Wang Y, Su B. Chromatin accessibility landscape and regulatory network of high-altitude hypoxia adaptation. Nat Commun, 2020, 11(1): 4928. doi: 10.1038/s41467-020-18638-8
[54]	Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science, 2011, 333(6046): 1137-1141. doi: 10.1126/science.1208227
[55]	Signor SA, Liu Y, Rebeiz M, Kopp A. Genetic convergence in the evolution of male-specific color patterns in Drosophila. Curr Biol, 2016, 26(18): 2423-2433. doi: S0960-9822(16)30785-0 pmid: 27546578
[56]	Frankel N, Wang S, Stern DL. Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution. Proc Natl Acad Sci USA, 2012, 109(51): 20975-20979. doi: 10.1073/pnas.1207715109
[57]	Merritt JR, Grogan KE, Zinzow-Kramer WM, Sun D, Ortlund Eric A, Yi SV, Maney DL. A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird. Proc Natl Acad Sci USA, 2020, 117(35): 21673-21680. doi: 10.1073/pnas.2011347117
[58]	Babbitt CC, Fedrigo O, Pfefferle AD, Boyle AP, Horvath JE, Furey TS, Wray GA. Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain. Genome Biol Evol, 2010, 2: 67-79. doi: 10.1093/gbe/evq002
[59]	Pollard KS, Salama SR, King B, Kern AD, Dreszer T, Katzman S, Siepel A, Pedersen JS, Bejerano G, Baertsch R, Rosenbloom KR, Kent J, Haussler D. Forces shaping the fastest evolving regions in the human genome. PLoS Genet, 2006, 2(10): e168. doi: 10.1371/journal.pgen.0020168
[60]	Prabhakar S, Noonan JP, Pääbo S, Rubin EM. Accelerated evolution of conserved noncoding sequences in humans. Science, 2006, 314(5800): 786. pmid: 17082449
[61]	Sackton TB, Grayson P, Cloutier A, Hu ZR, Liu JS, Wheeler NE, Gardner PP, Clarke JA, Baker AJ, Clamp M, Edwards SV. Convergent regulatory evolution and loss of flight in paleognathous birds. Science, 2019, 364(6435): 74-78. doi: 10.1126/science.aat7244
[62]	Ferris E, Gregg C. Parallel accelerated evolution in distant hibernators reveals candidate cis elements and genetic circuits regulating mammalian obesity. Cell Rep, 2019, 29(9): 2608-2620.e4. doi: 10.1016/j.celrep.2019.10.102
[63]	Cahill JA, Armstrong J, Deran A, Khoury CJ, Paten B, Haussler D, Jarvis ED. Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans. Genome Res, 2021, 31(11): 2035-2049. doi: 10.1101/gr.275989.121 pmid: 34667117
[64]	Van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ. The industrial melanism mutation in British peppered moths is a transposable element. Nature, 2016, 534(7605): 102-105. doi: 10.1038/nature17951
[65]	Wells JN, Feschotte C. A field guide to eukaryotic transposable elements. Annu Rev Genet, 2020, 54: 539-561. doi: 10.1146/annurev-genet-040620-022145
[66]	Lamichhaney S, Catullo R, Keogh JS, Clulow S, Edwards SV, Ezaz T. A bird-like genome from a frog: mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum. Proc Natl Acad Sci USA, 2021, 118(11): e2011649118.
[67]	Goubert C, Zevallos NA, Feschotte C. Contribution of unfixed transposable element insertions to human regulatory variation. Philos Trans R Soc Lond B Biol Sci, 2020, 375(1795): 20190331. doi: 10.1098/rstb.2019.0331
[68]	Harrison RG, Larson EL. Hybridization, introgression, and the nature of species boundaries. J Hered, 2014, 105 Suppl 1: 795-809. doi: 10.1093/jhered/esu033 pmid: 25149255
[69]	Zhang W, Dasmahapatra KK, Mallet J, Moreira GRP, Kronforst MR. Genome-wide introgression among distantly related Heliconius butterfly species. Genome Biol, 2016, 17: 25. doi: 10.1186/s13059-016-0889-0 pmid: 26921238
[70]	Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai WW, Fritz MHY, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Ž, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S. A draft sequence of the Neandertal genome. Science, 2010, 328(5979): 710-722. doi: 10.1126/science.1188021
[71]	Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PLF, Maricic T, Good JM, Marques-Bonet T, Alkan C, Fu QM, Mallick S, Li H, Meyer M, Eichler EE, Stoneking M, Richards M, Talamo S, Shunkov MV, Derevianko AP, Hublin JJ, Kelso J, Slatkin M, Pääbo S. Genetic history of an archaic hominin group from Denisova cave in Siberia. Nature, 2010, 468(7327): 1053-1060. doi: 10.1038/nature09710
[72]	Stolle E, Pracana R, López-Osorio F, Priebe MK, Hernández GL, Castillo-Carrillo C, Arias MC, Paris CI, Bollazzi M, Priyam A, Wurm Y. Recurring adaptive introgression of a supergene variant that determines social organization. Nat Commun, 2022, 13(1): 1180. doi: 10.1038/s41467-022-28806-7
[73]	Jones MR, Mills LS, Alves PC, Callahan CM, Alves JM, Lafferty DJR, Jiggins FM, Jensen JD, Melo-Ferreira J, Good JM. Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science, 2018, 360(6395): 1355-1358. doi: 10.1126/science.aar5273
[74]	Giska I, Farelo L, Pimenta J, Seixas FA, Ferreira MS, Marques JP, Miranda I, Letty J, Jenny H, Hackländer K, Magnussen E, Melo-Ferreira J. Introgression drives repeated evolution of winter coat color polymorphism in hares. Proc Natl Acad Sci USA, 2019, 116(48): 24150-24156. doi: 10.1073/pnas.1910471116
[75]	Oziolor EM, Reid NM, Yair S, Lee KM, Guberman VerPloeg S, Bruns PC, Shaw JR, Whitehead A, Matson CW. Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science, 2019, 364(6439): 455-457. doi: 10.1126/science.aav4155 pmid: 31048485
[76]	Ruddiman WF, Kutzbach JE. Plateau uplift and climatic change. Sci Am, 1991, 264(3): 66-75.
[77]	Moore LG, Niermeyer S, Zamudio S. Human adaptation to high altitude: regional and life-cycle perspectives. Am J Phys Anthropol, 1998, Suppl 27: 25-64. pmid: 9881522
[78]	Beall CM. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA, 2007, 104 Suppl 1(Suppl 1): 8655-8660.
[79]	Xu DM, Yang CP, Shen QS, Pan SK, Liu Z, Zhang TZ, Zhou X, Lei ML, Chen P, Yang H, Zhang T, Guo YT, Zhan XJ, Chen YB, Shi P. A single mutation underlying phenotypic convergence for hypoxia adaptation on the Qinghai-Tibetan Plateau. Cell Res, 2021, 31(9): 1032- 1035. doi: 10.1038/s41422-021-00517-6
[80]	Zhang T, Chen J, Zhang J, Guo YT, Zhou X, Li MW, Zheng ZZ, Zhang TZ, Murphy RW, Nevo E, Shi P. Phenotypic and genomic adaptations to the extremely high elevation in plateau zokor (Myospalax baileyi). Mol Ecol, 2021, 30(22): 5765-5779. doi: 10.1111/mec.16174 pmid: 34510615
[81]	Scott GR, Elogio TS, Lui MA, Storz JF, Cheviron ZA. Adaptive modifications of muscle phenotype in high-altitude deer mice are associated with evolved changes in gene regulation. Mol Biol Evol, 2015, 32(8): 1962-1976. doi: 10.1093/molbev/msv076
[82]	Zhu XJ, Guan YY, Signore AV, Natarajan C, DuBay SG, Cheng YL, Han NJ, Song G, Qu YH, Moriyama H, Hoffmann FG, Fago A, Lei FM, Storz JF. Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA, 2018, 115(8): 1865-1870. doi: 10.1073/pnas.1720487115
[83]	Xiong Y, Fan LQ, Hao Y, Cheng YL, Chang YB, Wang J, Lin HY, Song G, Qu YH, Lei FM. Physiological and genetic convergence supports hypoxia resistance in high-altitude songbirds. PLoS Genet, 2020, 16(12): e1009270.
[84]	She HS, Jiang ZY, Song G, Ericson PGP, Luo X, Shao SM, Lei FM, Qu YH. Quantifying adaptive divergence of the snowfinches in a common landscape. Divers Distrib, 2021, 0: 1-14.
[85]	Qu YH, Chen CH, Chen XM, Hao Y, She HS, Wang MX, Ericson PGP, Lin HY, Cai TL, Song G, Jia CX, Chen CY, Zhang HL, Li J, Liang LP, Wu TY, Zhao JY, Gao Q, Zhang GJ, Zhai WW, Zhang C, Zhang YE, Lei FM. The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA, 2021, 118(13): e2012398118.
[86]	Li DM, Davis JE, Sun YF, Wang G, Nabi G, Wingfield JC, Lei FM. Coping with extremes: convergences of habitat use, territoriality, and diet in summer but divergences in winter between two sympatric snow finches on the Qinghai-Tibet Plateau. Integr Zool, 2020, 15(6): 533-543. doi: 10.1111/1749-4877.12462
[87]	Shao SM, Quan Q, Cai TL, Song G, Qu YH, Lei FM. Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 Paridae species. Front Zool, 2016, 13: 30. doi: 10.1186/s12983-016-0162-0
[88]	Bickler PE, Buck LT. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol, 2007, 69: 145-170. pmid: 17037980
[89]	Projecto-Garcia J, Natarajan C, Moriyama H, Weber RE, Fago A, Cheviron ZA, Dudley R, McGuire JA, Witt CC, Storz JF. Repeated elevational transitions in hemoglobin function during the evolution of Andean hummingbirds. Proc Natl Acad Sci USA, 2013, 110(51): 20669-20674. doi: 10.1073/pnas.1315456110
[90]	Natarajan C, Projecto-Garcia J, Moriyama H, Weber RE, Muñoz-Fuentes V, Green AJ, Kopuchian C, Tubaro PL, Alza L, Bulgarella M, Smith MM, Wilson RE, Fago A, McCracken KG, Storz JF. Convergent evolution of hemoglobin function in high-altitude Andean waterfowl involves limited parallelism at the molecular sequence level. PLoS Genet, 2015, 11(12): e1005681.
[91]	Scott GR, Schulte PM, Egginton S, Scott ALM, Richards JG, Milsom WK. Molecular evolution of cytochrome c oxidase underlies high-altitude adaptation in the bar-headed goose. Mol Biol Evol, 2011, 28(1): 351-363. doi: 10.1093/molbev/msq205
[92]	Simonson TS, Yang YZ, Huff CD, Yun HX, Qin G, Witherspoon DJ, Bai ZZ, Lorenzo FR, Xing JC, Jorde LB, Prchal JT, Ge RL. Genetic evidence for high-altitude adaptation in Tibet. Science, 2010, 329(5987): 72-75. doi: 10.1126/science.1189406 pmid: 20466884
[93]	Beall CM, Cavalleri GL, Deng LB, Elston RC, Gao Y, Knight J, Li CH, Li JC, Liang Y, McCormack M, Montgomery HE, Pan H, Robbins PA, Shianna KV, Tam SC, Tsering N, Veeramah KR, Wang W, Wangdui P, Weale ME, Xu YM, Xu Z, Yang L, Zaman MJ, Zeng CQ, Zhang L, Zhang XL, Zhaxi PC, Zheng YT. Natural selection on EPAS1 (HIF2α) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci USA, 2010, 107(25): 11459-11464. doi: 10.1073/pnas.1002443107
[94]	Peng Y, Cui CY, He YX, Ouzhuluobu, Zhang H, Yang DY, Zhang Q, Bianbazhuoma, Yang LX, He YB, Xiang K, Zhang XM, Bhandari S, Shi P, Yangla, Dejiquzong, Baimakangzhuo, Duojizhuoma, Pan YY, Cirenyangji, Baimayangji, Gonggalanzi, Bai CJ, Bianba, Basang, Ciwangsangbu, Xu SH, Chen H, Liu SM, Wu TY, Qi XB, Su B. Down-regulation of EPAS1 transcription and genetic adaptation of Tibetans to high-altitude hypoxia. Mol Biol Evol, 2017, 34(4): 818-830. doi: 10.1093/molbev/msw280 pmid: 28096303
[95]	Lorenzo FR, Huff C, Myllymäki M, Olenchock B, Swierczek S, Tashi T, Gordeuk V, Wuren T, Ri-Li G, McClain DA, Khan TM, Koul PA, Guchhait P, Salama ME, Xing JC, Semenza GL, Liberzon E, Wilson A, Simonson TS, Jorde LB, Kaelin WG, Koivunen P, Prchal JT. A genetic mechanism for Tibetan high-altitude adaptation. Nat Genet, 2014, 46(9): 951-956. doi: 10.1038/ng.3067 pmid: 25129147
[96]	Yang J, Jin ZB, Chen J, Huang XF, Li XM, Liang YB, Mao JY, Chen X, Zheng ZL, Bakshi A, Zheng DD, Zheng MQ, Wray NR, Visscher PM, Lu F, Qu J. Genetic signatures of high-altitude adaptation in Tibetans. Proc Natl Acad Sci USA, 2017, 114(16): 4189-4194. doi: 10.1073/pnas.1617042114
[97]	Qiu Q, Zhang GJ, Ma T, Qian WB, Wang JY, Ye ZQ, Cao CC, Hu QJ, Kim J, Larkin DM, Auvil L, Capitanu B, Ma J, Lewin HA, Qian XJ, Lang YS, Zhou R, Wang LZ, Wang K, Xia JQ, Liao SG, Pan SK, Lu X, Hou HL, Wang Y, Zang XT, Yin Y, Ma H, Zhang J, Wang ZF, Zhang YM, Zhang DW, Yonezawa T, Hasegawa M, Zhong Y, Liu WB, Zhang Y, Huang ZY, Zhang SX, Long RJ, Yang HM, Wang J, Lenstra JA, Cooper DN, Wu Y, Wang J, Shi P, Wang J, Liu JQ. The yak genome and adaptation to life at high altitude. Nat Genet, 2012, 44(8): 946-949. doi: 10.1038/ng.2343
[98]	Yu L, Wang GD, Ruan J, Chen YB, Yang CP, Cao X, Wu H, Liu YH, Du ZL, Wang XP, Yang J, Cheng SC, Zhong L, Wang L, Wang X, Hu JY, Fang L, Bai B, Wang KL, Yuan N, Wu SF, Li BG, Zhang JG, Yang YQ, Zhang CL, Long YC, Li HS, Yang JY, Irwin DM, Ryder OA, Li Y, Wu CI, Zhang YP. Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation. Nat Genet, 2016, 48(8): 947-952. doi: 10.1038/ng.3615 pmid: 27399969
[99]	Zhang WP, Fan ZX, Han E, Hou R, Zhang L, Galaverni M, Huang J, Liu H, Silva P, Li P, Pollinger JP, Du LM, Zhang XY, Yue BS, Wayne RK, Zhang ZH. Hypoxia adaptations in the grey wolf (Canis lupus chanco) from Qinghai-Tibet Plateau. PLoS Genet, 2014, 10(7): e1004466.
[100]	Qu YH, Zhao HW, Han NJ, Zhou GY, Song G, Gao B, Tian SL, Zhang JB, Zhang RY, Meng XH, Zhang Y, Zhang Y, Zhu XJ, Wang WJ, Lambert D, Ericson PGP, Subramanian S, Yeung C, Zhu HM, Jiang Z, Li RQ, Lei FM. Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan Plateau. Nat Commun, 2013, 4: 2071. doi: 10.1038/ncomms3071
[101]	Cheng YL, Miller MJ, Zhang DZ, Xiong Y, Hao Y, Jia CX, Cai TL, Li SH, Johansson US, Liu Y, Chang YB, Song G, Qu YH, Lei FM. Parallel genomic responses to historical climate change and high elevation in East Asian songbirds. Proc Natl Acad Sci USA, 2021, 118(50): e2023918118.
[102]	Cui K, Li WJ, James JG, Peng CJ, Jin JZ, Yan CC, Fan ZX, Du LM, Price M, Wu YJ, Yue BS. The first draft genome of Lophophorus: a step forward for Phasianidae genomic diversity and conservation. Genomics, 2019, 111(6): 1209-1215. doi: 10.1016/j.ygeno.2018.07.016
[103]	Zhou C, Yu HR, Geng Y, Liu W, Zheng S, Yang N, Meng Y, Dou L, Price M, Ran JH, Yue BS, Wu YJ. A high-quality draft genome assembly of the black-necked crane (Grus nigricollis) based on Nanopore sequencing. Genome Biol Evol, 2019, 11(12): 3332-3340.
[104]	Zhou C, James JG, Xu Y, Tu HM, He XC, Wen QC, Price M, Yang N, Wu YJ, Ran J, Meng Y, Yue BS. Genome-wide analysis sheds light on the high-altitude adaptation of the buff-throated partridge (Tetraophasis szechenyii). Mol Genet Genomics, 2020, 295(1): 31-46. doi: 10.1007/s00438-019-01601-8
[105]	Yang LD, Wang Y, Zhang ZL, He SP. Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet fish, Gymnodiptychus pachycheilus. Genome Biol Evol, 2014, 7(1): 251-261. doi: 10.1093/gbe/evu279
[106]	Wang Y, Yang LD, Wu B, Song ZB, He SP. Transcriptome analysis of the plateau fish (Triplophysa dalaica): implications for adaptation to hypoxia in fishes. Gene, 2015, 565(2): 211-220. doi: 10.1016/j.gene.2015.04.023
[107]	Wang Y, Yang LD, Zhou K, Zhang YP, Song ZB, He SP. Evidence for adaptation to the Tibetan Plateau inferred from Tibetan loach transcriptomes. Genome Biol Evol, 2015, 7(11): 2970-2982. doi: 10.1093/gbe/evv192
[108]	Sun YB, Xiong ZJ, Xiang XY, Liu SP, Zhou WW, Tu XL, Zhong L, Wang L, Wu DD, Zhang BL, Zhu CL, Yang MM, Chen HM, Li F, Zhou L, Feng SH, Huang C, Zhang GJ, Irwin D, Hillis DM, Murphy RW, Yang HM, Che J, Wang J, Zhang YP. Whole-genome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes. Proc Natl Acad Sci USA, 2015, 112(11): E1257-E1262.
[109]	Sun YB, Fu TT, Jin JQ, Murphy RW, Hillis DM, Zhang YP, Che J. Species groups distributed across elevational gradients reveal convergent and continuous genetic adaptation to high elevations. Proc Natl Acad Sci USA, 2018, 115(45): E10634-E10641.
[110]	Li JT, Gao YD, Xie L, Deng C, Shi P, Guan ML, Huang S, Ren JL, Wu DD, Ding L, Huang ZY, Nie H, Humphreys DP, Hillis DM, Wang WZ, Zhang YP. Comparative genomic investigation of high-elevation adaptation in ectothermic snakes. Proc Natl Acad Sci USA, 2018, 115(33): 8406-8411. doi: 10.1073/pnas.1805348115
[111]	Feigin CY, Newton AH, Doronina L, Schmitz J, Hipsley CA, Mitchell KJ, Gower G, Llamas B, Soubrier J, Heider TN, Menzies BR, Cooper A, O’Neill RJ, Pask AJ. Genome of the Tasmanian tiger provides insights into the evolution and demography of an extinct marsupial carnivore. Nat Ecol Evol, 2018, 2(1): 182-192. doi: 10.1038/s41559-017-0417-y
[112]	Carroll SB, Prud’homme B, Gompel N. Regulating evolution. Sci Am, 2008, 298(5): 60-67. pmid: 18444326
[113]	Gallant JR, Traeger LL, Volkening JD, Moffett H, Chen PH, Novina CD, Phillips GN, Anand R, Wells GB, Pinch M, Güth R, Unguez GA, Albert JS, Zakon HH, Samanta MP, Sussman MR.Genomic basis for the convergent evolution of electric organs. Science, 2014, 344(6191): 1522-1525.
[114]	Verta JP, Jones FC. Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. eLife, 2019, 8: e43785. doi: 10.7554/eLife.43785
[115]	Hao Y, Xiong Y, Cheng YL, Song G, Jia CX, Qu YH, Lei FM. Comparative transcriptomics of 3 high-altitude passerine birds and their low-altitude relatives. Proc Natl Acad Sci USA, 2019, 116(24): 11851-11856. doi: 10.1073/pnas.1819657116
[116]	Huerta-Sánchez E, Jin X, Asan, Bianba ZM, Peter BM, Vinckenbosch N, Liang Y, Yi X, He MZ, Somel M, Ni PX, Wang B, Ou XH, Huasang, Luosang JB, Cuo ZXP, Li K, Gao GY, Yin Y, Wang W, Zhang XQ, Xu X, Yang HM, Li YR, Wang J, Wang J, Nielsen R. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature, 2014, 512(7513): 194-197. doi: 10.1038/nature13408
[117]	Miao BP, Wang Z, Li YX. Genomic analysis reveals hypoxia adaptation in the Tibetan mastiff by introgression of the gray wolf from the Tibetan Plateau. Mol Biol Evol, 2017, 34(3): 734-743.
[118]	Zhang ZG, Xu DM, Wang L, Hao JJ, Wang JF, Zhou X, Wang WW, Qiu Q, Huang XD, Zhou JW, Long RJ, Zhao FQ, Shi P. Convergent evolution of rumen microbiomes in high-altitude mammals. Curr Biol, 2016, 26(14): 1873-1879. doi: 10.1016/j.cub.2016.05.012
[119]	Bo TB, Song G, Tang SY, Zhang MR, Ma ZW, Lv HR, Wu Y, Zhang DZ, Yang L, Wang DH, Lei FM. Incomplete concordance between host phylogeny and gut microbial community in Tibetan wetland birds. Front Microbiol, 2022, 13: 848906. doi: 10.3389/fmicb.2022.848906
[120]	Prabhakar S, Noonan JP, Pääbo S, Rubin EM. Accelerated evolution of conserved noncoding sequences in humans. Science, 2006, 314(5800): 786. pmid: 17082449
[121]	Wang YT, Dai GY, Gu ZL, Liu GP, Tang K, Pan YH, Chen YJ, Lin X, Wu N, Chen HS, Feng S, Qiu S, Sun HD, Li Q, Xu C, Mao YN, Zhang YE, Khaitovich P, Wang YL, Liu QX, Han JDJ, Shao Z, Wei G, Xu C, Jing NH, Li HP. Accelerated evolution of an Lhx2 enhancer shapes mammalian social hierarchies. Cell Res, 2020, 30(5): 408-420. doi: 10.1038/s41422-020-0308-7
[122]	Figuet E, Nabholz B, Bonneau M, Mas Carrio E, Nadachowska-Brzyska K, Ellegren H, Galtier N. Life history traits, protein evolution, and the nearly neutral theory in amniotes. Mol Biol Evol, 2016, 33(6): 1517-1527. doi: 10.1093/molbev/msw033
[123]	Axelsson E, Hultin-Rosenberg L, Brandström M, Zwahlén M, Clayton DF, Ellegren H. Natural selection in avian protein-coding genes expressed in brain. Mol Ecol, 2008, 17(12): 3008-3017. doi: 10.1111/j.1365-294X.2008.03795.x pmid: 18482257
[124]	Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA, 2005, 102(40): 14338-14343. doi: 10.1073/pnas.0504070102
[125]	Levy Karin E, Wicke S, Pupko T, Mayrose I. An integrated model of phenotypic trait changes and site-specific sequence evolution. Syst Biol, 2017, 66(6): 917-933. doi: 10.1093/sysbio/syx032 pmid: 28177510
[126]	Campbell-Staton SC, Velotta JP, Winchell KM. Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands. Nat Commun, 2021, 12(1): 6195. doi: 10.1038/s41467-021-26334-4 pmid: 34702827
[127]	Ho WC, Zhang JZ. Evolutionary adaptations to new environments generally reverse plastic phenotypic changes. Nat Commun, 2018, 9(1): 350. doi: 10.1038/s41467-017-02724-5
[128]	Ho WC, Li DY, Zhu Q, Zhang JZ. Phenotypic plasticity as a long-term memory easing readaptations to ancestral environments. Sci Adv, 2020, 6(21): eaba3388.
[129]	Velotta JP, Robertson CE, Schweizer RM, McClelland GB, Cheviron ZA.Adaptive shifts in gene regulation underlie a developmental delay in thermogenesis in high-altitude deer mice. Mol Biol Evol, 2020, 37(8): 2309-2321.
[130]	Gibbons TC, Metzger DCH, Healy TM, Schulte PM. Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats. Mol Ecol, 2017, 26(10): 2711-2725. doi: 10.1111/mec.14065 pmid: 28214359
[131]	Chen XM, Ji YZ, Cheng YL, Hao Y, Lei XH, Song G, Qu YH, Lei FM. Comparison between short-term stress and long-term adaptive responses reveal common paths to molecular adaptation. iScience, 2022, 25(3): 103899. doi: 10.1016/j.isci.2022.103899
[132]	Cheviron ZA, Bachman GC, Connaty AD, McClelland GB, Storz JF.Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice. Proc Natl Acad Sci USA, 2012, 109(22): 8635-8640.

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Genetic mechanism of adaptive evolution: the example of adaptation to high altitudes

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