Population variation revealed high-altitude adaptation of tibetan mastiffs

Molecular Biology and Evolution

Volumn 31, Issue 5, 2014, Pages 1200-1205

  Li, Yan ^a,b   Wu, Dong Dong ^a,b   Boyko, Adam R ^c   Wang, Guo Dong ^a,b   Wu, Shi Fang ^a   Irwin, David M ^a,d,e   Zhang, Ya Ping ^a,b,f  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c Animal Health Diagnostic Center   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f YUNNAN UNIVERSITY   (China)

Author keywords

Domestication; High altitude adaptation; Tibetan Mastiff

Indexed keywords

ALTITUDE ACCLIMATIZATION; ANIMAL EXPERIMENT; ARTICLE; CHINA; CIVILIZATION; DOG; EPAS1 GENE; GENE; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; HYPOXIA; MAFG GENE; NONHUMAN; PLXNA4 GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SIRT7 GENE;

DOMESTICATION; HIGH-ALTITUDE ADAPTATION; TIBETAN MASTIFF;

ACCLIMATIZATION; ALTITUDE; ANIMALS; CHINA; DOGS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; GENOME; HUMANS; MODELS, GENETIC; PETS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; TIBET; WOLVES;

EID: 84899565331     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu070     Document Type: Article

References (49)

1. Akey JM, RuheAL, AkeyDT,WongAK, Connelly CF, Madeoy J, Nicholas TJ, Neff MW. 2010. Tracking footprints of artificial selection in the dog genome. Proc Natl Acad Sci U S A. 107:1160-1165.
2. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD. 2002. Interrogating a high-density SNP map for signatures of natural selection. Genome Res. 12:1805-1814.
3. Bassett JHD, Gogakos A, White JK, Evans H, Jacques RM, van der Spek AH, Ramirez-Solis R, Ryder E, Sunter D, Boyde A, et al. 2012. Rapidthroughput skeletal phenotyping of 100 knockout mice identifies 9 new genes that determine bone strength. PLoS Genet. 8:e1002858.
4. Beall CM, Cavalleri GL, Deng L, Elston RC, Gao Y, Knight J, Li C, Li JC, Liang Y, McCormack M, et al. 2010. Natural selection on EPAS1 (HIF2a) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci U S A. 107:11459-11464.
5. Bigham A, Bauchet M, Pinto D, Mao X, Akey JM, Mei R, Scherer SW, Julian CG, Wilson MJ, Lopez Herraez D, et al. 2010. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6:e1001116.
6. Bigham AW, Mao X, Mei R, Brutsaert T, Wilson MJ, Julian CG, Parra EJ, Akey JM, Moore LG, Shriver MD. 2009. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum Genomics. 4:79-90.
7. Blank V, Kim MJ, Andrews NC. 1997. Human MafG is a functional partner for p45 NF-E2 in activating globin gene expression. Blood 89:3925-3935.
8. Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, Lohmueller KE, Zhao K, Brisbin A, Parker HG. 2010. A simple genetic architecture underlies morphological variation in dogs. PLoS Biol. 8:e1000451.
9. Bruno WJ, Socci ND, Halpern AL. 2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol. 17:189-197.
10. Cai Q,Qian X, Lang Y, Luo Y, Pan S, Hui Y, Gou C, Cai Y, HaoM, Zhao J, et al. 2013. The genome sequence of the ground tit Pseudopodoces humilis provides insights into its adaptation to high altitude. Genome Biol. 14:R29.
11. Carbonaro M, Escuin D, O'Brate A, Thadani-Mulero M, Giannakakou P. 2012. Microtubules regulate hypoxia-inducible factor-1a protein trafficking and activity: implications for taxane therapy. J Biol Chem. 287:11859-11869.
12. Cheviron ZA, Bachman GC, Connaty AD, McClelland GB, Storz JF. 2012. Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice. Proc Natl Acad Sci U S A. 109:8635-8640.
13. Cui TB, Guo X. 2010. A monograph of Tibetan Mastiff in China. Shanghai (China): Shanghai Scientific & Technical Publishers.
14. Gardner DS, Fletcher AJW, Fowden AL, Giussani DA. 2001. Plasma adrenocorticotropin and cortisol concentrations during acute hypoxemia after a reversible period of adverse intrauterine conditions in the ovine fetus during late gestation. Endocrinology 142: 589-598.
15. Ge R-L, Cai Q, Shen Y-Y, San A, Ma L, Zhang Y, Yi X, Chen Y, Yang L, Huang Y, et al. 2013. Draft genome sequence of the Tibetan antelope. Nat Commun. 4:1858.
16. Germonpre M, Sablin MV, Stevens RE, Hedges REM, Hofreiter M, Stiller M, Despres VR. 2009. Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Archaeol Sci. 36:473-490.
17. HeinigerCD, Kostadinova RM, RochatMK, SerraA, Ferrari P, Dick B, Frey BM, Frey FJ. 2003. Hypoxia causes down-regulation of 11 betahydroxysteroid dehydrogenase type 2 by induction of Egr-1. FASEB J. 17:917-919.
18. Hubbi ME, Hu H, Gilkes DM, Semenza GL. 2013. Sirtuin-7 Inhibits the Activity of Hypoxia-Inducible Factors. J Biol Chem. 288: 20768-20775.
19. Jiang F, Dong Y, Wu C, Yang X, Zhao L, Guo J, Li Y, Dong J, Zheng G-Y, Cao H, et al. 2011. Fine mapping of chromosome 3q22.3 identifies two haplotype blocks in ESYT3 associated with coronary artery disease in female Han Chinese. Atherosclerosis 218:397-403.
20. Kigel B, Rabinowicz N, Varshavsky A, Kessler O, Neufeld G. 2012. Plexin-A4 promotes tumor progression and tumor angiogenesis by enhancement of VEGF and bFGF signaling. Blood 118:4285-4296.
21. Kodama T, Shimizu N, Yoshikawa N, Makino Y, Ouchida R, Okamoto K, Hisada T, Nakamura H, Morimoto C, Tanaka H. 2003. Role of the glucocorticoid receptor for regulation of hypoxia-dependent gene expression. J Biol Chem. 278:33384-33391.
22. Li Y, vonHoldt BM, Reynolds A, Boyko AR, Wayne RK, Wu D-D, Zhang Y-P. 2013. Artificial selection on brain-expressed genes during the domestication of dog. Mol Biol Evol. 30:1867-1876.
23. Li Y, Zhang Y. 2012. High genetic diversity of Tibetan Mastiffs revealed by mtDNA sequences. Chin Sci Bull. 57:1483-1487.
24. Maher JT, Jones LG, Hartley LH, Williams GH, Rose LI. 1975. Aldosterone dynamics during graded exercise at sea level and high altitude. J Appl Physiol. 39:18-22.
25. Messerschmidt DA. 1983. The Tibetan Mastiff: canine sentinels of the range. Rangelands 5:172-174.
26. Moncloa F, Donayre J, Sobrevilla LA, Guerra-Garcia R. 1965. Endocrine studies at high altitude. II. Adrenal cortical function in sea level natives exposed to high altitudes (4300 meters) for two weeks. J Clin Endocrinol Metab. 25:1640-1642.
27. Peng Y, Yang Z, Zhang H, Cui C, Qi X, Luo X, Tao X, Wu T, Chen H, Shi H, et al. 2011. Genetic variations in Tibetan populations and highaltitude adaptation at the Himalayas. Mol Biol Evol. 28:1075-1081.
28. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
29. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. 2000. Association mapping in structured populations. Am J Hum Genet. 67:170-181.
30. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, De Bakker PIW, Daly MJ. 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559-575.
31. Qiu Q, Zhang G, Ma T, Qian W,Wang J, Ye Z, Cao C, Hu Q, Kim J, Larkin DM, et al. 2012. The yak genome and adaptation to life at high altitude. Nat Genet. 44:946-949.
32. Qu Y, Zhao H, Han N, Zhou G, Song G, Gao B, Tian S, Zhang J, Zhang R, Meng X, et al. 2013. Ground tit genome reveals avian adaptation to living at high altitudes in the Tibetan plateau. Nat Commun. 4:2071.
33. Rey S, Semenza GL. 2010. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res. 86:236-242.
34. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A,Mikkelsen TS, Altshuler D, Lander ES. 2006. Positive natural selection in the human lineage. Science 312:1614-1620.
35. Sawhney RC, Malhotra AS, Singh T. 1991. Glucoregulatory hormones in man at high altitude. Eur J Appl Physiol Occup Physiol. 62:286-291.
36. Scheet P, Stephens M. 2006. A fast and flexible statistical model for largescale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet. 78:629-644.
37. Scheinfeldt LB, Soi S, Thompson S, Ranciaro A, Woldemeskel D, Beggs W, Lambert C, Jarvis JP, Abate D, Belay G. 2012. Genetic adaptation to high altitude in the Ethiopian highlands. Genome Biol. 13:R1.
38. Semenza GL. 2011. Oxygen sensing, homeostasis, and disease. N Engl J Med. 365:537-547.
39. Simonson TS, Yang Y, Huff CD, Yun H, Qin G,Witherspoon DJ, Bai Z, Lorenzo FR, Xing J, Jorde LB. 2010. Genetic evidence for high-altitude adaptation in Tibet. Science 329:72.
40. Storz JF, Moriyama H. 2008. Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Alt Med Biol. 9:148-157.
41. Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW. 2007. The molecular basis of highaltitude adaptation in deer mice. PLoS Genet. 3:e45.
42. Vakhrusheva O, Smolka C, Gajawada P, Kostin S, Boettger T, Kubin T, Braun T, Bober E. 2008. Sirt7 increases stress resistance of cardiomyocytes and prevents apoptosis and inflammatory cardiomyopathy in mice. Circ Res. 102:703-710.
43. vonHoldt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H, Geffen E, Pilot M, Jedrzejewski W, Jedrzejewska B, et al. 2011. A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res. 21:1294-1305.
44. vonHoldt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A, et al. 2010. Genomewide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898-902.
45. Wang Y-X, Zheng Y-M. 2010. ROS-dependent signaling mechanisms for hypoxic Ca2+ responses in pulmonary artery myocytes. Antioxid Redox Signal. 12:611-623.
46. Wen J, Yuan N. 1998. Analysis on the parameters of blood in healthy Tibetan Mastiffs. J Qinghai Medical College. 20:7-9.
47. Xiang K, Ouzhuluobu, Peng Y, Yang Z, Zhang X, Cui C, Zhang H, Li M, Zhang Y, Bianba, et al. 2013. Identification of a Tibetan-specific mutation in the hypoxic gene EGLN1 and its contribution to high-altitude adaptation. Mol Biol Evol. 30:1889-1898.
48. Xu S, Li S, Yang Y, Tan J, Lou H, Jin W, Yang L, Pan X, Wang J, Shen Y, et al. 2011. A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol Biol Evol. 28:1003-1011.
49. Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZXP, Pool JE, Xu X, Jiang H, Vinckenbosch N, Korneliussen TS, et al. 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329: 75-78.