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PLOS ONE  2013 

Patterns of Adaptive and Neutral Diversity Identify the Xiaoxiangling Mountains as a Refuge for the Giant Panda

DOI: 10.1371/journal.pone.0070229

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Abstract:

Genetic variation plays a significant role in maintaining the evolutionary potential of a species. Comparing the patterns of adaptive and neutral diversity in extant populations is useful for understanding the local adaptations of a species. In this study, we determined the fine-scale genetic structure of 6 extant populations of the giant panda (Ailuropoda melanoleuca) using mtDNA and DNA fingerprints, and then overlaid adaptive variations in 6 functional Aime-MHC class II genes (DRA, DRB3, DQA1, DQA2, DQB1, and DQB2) on this framework. We found that: (1) analysis of the mtDNA and DNA fingerprint-based networks of the 6 populations identified the independent evolutionary histories of the 2 panda subspecies; (2) the basal (ancestral) branches of the fingerprint-based Sichuan-derived network all originated from the smallest Xiaoxiangling (XXL) population, suggesting the status of a glacial refuge in XXL; (3) the MHC variations among the tested populations showed that the XXL population exhibited extraordinary high levels of MHC diversity in allelic richness, which is consistent with the diversity characteristics of a glacial refuge; (4) the phylogenetic tree showed that the basal clades of giant panda DQB sequences were all occupied by XXL-specific sequences, providing evidence for the ancestor-resembling traits of XXL. Finally, we found that the giant panda had many more DQ alleles than DR alleles (33:13), contrary to other mammals, and that the XXL refuge showed special characteristics in the DQB loci, with 7 DQB members of 9 XXL-unique alleles. Thus, this study identified XXL as a glacial refuge, specifically harboring the most number of primitive DQB alleles.

References

[1]  Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2: 16–33.
[2]  Blais J, Rico C, van Oosterhout C, Cable J, Turner GF, et al. (2007) MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids. PLoS One 2: e734.
[3]  Cronin JK, Bundock PC, Henry RJ, Nevo E (2007) Adaptive climatic molecular evolution in wild barley at the Isa defense locus. P Natl Acad Sci Usa 104: 2773–2778.
[4]  Hu JC (2001) Research on the giant panda. Shanghai: Shanghai Publishing House of Science and Technology.
[5]  State Forestry Administration of China (2006) The third national survey report on giant panda in China. Beijing: Science Press.
[6]  Fang SG, Feng WH, Zhang AJ, Li SC, Yu JQ, et al. (1997) The comparative analysis on the genetic diversity of giant pandas between Liangshan and Xiaoxiangling Mountains. Acta Theriologica Sinica 17: 248–252.
[7]  Zhang YP, Ryder OA, Fan ZY, Fan ZY, He TM, et al. (1997) Sequence variation and genetic diversity in the giant panda. Sci China C Life Sci 40: 210–216.
[8]  Fang SG, Wan QH, Fujihara T (2003) Loss of genetic variation in giant panda due to limited population and habitat fragmentation. J Appl Anim Res 24: 137–144.
[9]  Zhang B, Li M, Zhang ZJ, Goossens B, Zhu LF, et al. (2007) Genetic viability and population history of the giant panda, putting an end to the “evolutionary dead end”? Mol Biol Evol 24: 1801–1810.
[10]  He W, Lin L, Shen FJ, Zhang WP, Zhang ZH, et al. (2008) Genetic diversities of the giant panda (Ailuropoda melanoleuca) in Wanglang and Baoxing Nature Reserves. Conserv Genet 9: 1541–1546.
[11]  Shen FJ, Zhang ZH, He W, Yue BS, Zhang AJ, et al. (2009) Microsatellite variability reveals the necessity for genetic input from wild giant pandas (Ailuropoda melanoleuca) into the captive population. Mol Ecol 18: 1061–1070.
[12]  Fang SG, Wan QH, Fujihara N (2002) Genetic diversity of the giant panda (Ailuropoda melanoleuca) between big and small populations. J Appl Anim Res 21: 65–74.
[13]  Lu Z, Johnson WE, Menotti-Raymond M, Yuhki N, Martenson JS, et al. (2001) Patterns of genetic diversity in remaining giant panda populations. Conserv Biol 15: 1596–1607.
[14]  Wan QH, Fang SG, Li JG, Zhang LM, Ou WF, et al. (2005) A family net of giant pandas in the Tangjiahe Natural Reserve: Assessment of current individual migration. Chinese Sci Bull 50: 1879–1886.
[15]  Zhu LF, Zhan XJ, Wu H, Zhang SN, Meng T, et al. (2010) Conservation implications of drastic reductions in the smallest and most isolated populations of giant pandas. Conserv Biol 24: 1299–1306.
[16]  Wan QH, Fang SG, Wu H, Fujihara T (2003) Genetic differentiation and subspecies development of the giant panda as revealed by DNA fingerprinting. Electrophoresis 24: 1353–1359.
[17]  Wan QH, Wu H, Fang SG (2005) A New Subspecies of Giant Panda (Ailuropoda melanoleuca) from Shaanxi, China. J Mammal 86: 397–402.
[18]  Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32: 415–435.
[19]  Piertney S, Oliver M (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7–21.
[20]  Bondinas GP, Moustakas AK, Papadopoulos GK (2007) The spectrum of HLA-DQ and HLA-DR alleles, 2006: a listing correlating sequence and structure with function. Immunogenetics 59: 539–553.
[21]  Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, et al. (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. P Natl Acad Sci Usa 101: 3490–3494.
[22]  Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings Of The Royal Society Of London Series B-biological Sciences 277: 979–988.
[23]  Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170.
[24]  Clarke B, Kirby DRS (1966) Maintenance of histocompatibility polymorphisms. Nature 211: 999–1000.
[25]  Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56: 1902–1908.
[26]  Zeng CJ, Yu JQ, Pan HJ, Wan QH, Fang SG (2005) Assignment of the giant panda MHC class II gene cluster to chromosome 9q by fluorescence in situ hybridization. Cytogenet Genome Res 109: 534H.
[27]  Wan QH, Zhu L, Wu H, Fang SG (2006) Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca). Mol Ecol 15: 2441–2450.
[28]  Zeng CJ, Pan HJ, Gong SB, Yu JQ, Wan QH, et al. (2007) Giant panda BAC library construction and assembly of a 650-kb contig spanning major histocompatibility complex class II region. BMC genomics 8: 315.
[29]  Wan QH, Zeng CJ, Ni XW, Pan HJ, Fang SG (2009) Giant panda genomic data provide insight into the birth-and-death process of mammalian major histocompatibility complex class II genes. PLoS One 4: e4147.
[30]  Chen YY, Zhang YY, Zhang HM, Ge YF, Wan QH, et al. (2010) Natural Selection Coupled With Intragenic Recombination Shapes Diversity Patterns in the Major Histocompatibility Complex Class II Genes of the Giant Panda. J Exp Zool B Mol Dev Evol 314B: 208–223.
[31]  Wan QH, Zhang P, Ni XW, Wu HL, Chen YY, et al. (2011) A novel HURRAH protocol reveals high numbers of monomorphic MHC class II loci and two asymmetric multi-locus haplotypes in the Père David's deer. PLoS One 6: e14518.
[32]  Sambrook J, Russell DW (2001) Molecular cloning: A laboratory manual, 3rd edn. New York: Cold Spring Harbor Laboratory Press.
[33]  Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, et al. (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24: 3189–3194.
[34]  Kennedy L, Ryvar R, Gaskell R, Addie D, Willoughby K, et al. (2002) Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54: 348–352.
[35]  Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
[36]  Bandelt HJ, Forster P, R?hl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48.
[37]  Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17: 4015–4026.
[38]  Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10: 556–557.
[39]  Rousset F (2008) genepop'007: a complete reimplementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103–106.
[40]  Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9: 552–569.
[41]  Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497.
[42]  Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
[43]  Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253–1256.
[44]  Saarma U, Ho SY, Pybus OG, Kaljuste M, Tumanov IL, et al. (2007) Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages. Mol Ecol 16: 401–413.
[45]  Rambaut A, Drummond A (2007) Tracer v1. 5. http://tree.bio.ed.ac.uk/software/tracer?/.
[46]  Fang SG, Wan QH, Fujihara N (2002) A new oligonucleotide probe for the giant panda. Mol Ecol Notes 2: 352–355.
[47]  Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sunderland, MA: Sinauer Associates.
[48]  Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proceedings of the National Academy of Sciences 95: 3708–3713.
[49]  Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.
[50]  Yang Z, Nielsen R, Goldman N, Pedersen A-MK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431–449.
[51]  Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929–936.
[52]  Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107–1118.
[53]  Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
[54]  Kuduk K, Babik W, Bojarska K, ?liwińska E, Kindberg J, et al. (2012) Evolution of major histocompatibility complex class I and class II genes in the brown bear. BMC Evol Biol 12: 197.
[55]  Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3).
[56]  Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567.
[57]  Zhao S, Zheng P, Dong S, Zhan X, Wu Q, et al. (2013) Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45: 67–71.
[58]  Yasukochi Y, Kurosaki T, Yoneda M, Koike H, Satta Y (2012) MHC class II DQB diversity in the Japanese black bear, Ursus thibetanus japonicus. BMC Evol Biol 12: 230.
[59]  Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140: 767–782.
[60]  Pan W, Gao Z, Lu Z (1988) The Giant Panda's Natural Refuge in Qinling Beijing: Peking University Press.
[61]  Zhang RZ (1998) Zoogeography of China Beijing Science Press.
[62]  Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58: 247–276.
[63]  Doxiadis GGM, Otting N, De Groot NG, Bontrop RE (2001) Differential evolutionary MHC class II strategies in humans and rhesus macaques: relevance for biomedical studies. Immunol Rev 183: 76–85.
[64]  Zhan X, Zhang Z, Wu H, Goossens B, Li M, et al. (2007) Molecular analysis of dispersal in giant pandas. Mol Ecol 16: 3792–3800.
[65]  Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evolution Biol 16: 363–377.
[66]  Goda N, Mano T, Kosintsev P, Vorobiev A, Masuda R (2010) Allelic diversity of the MHC class II DRB genes in brown bears (Ursus arctos) and a comparison of DRB sequences within the family Ursidae. Tissue Antigens 76: 404–410.
[67]  Hedrick PW, Lee RN, Parker KM (2000) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity 85: 617–624.
[68]  Nigenda-Morales S, Flores-Ramírez S, Urbán-R J, Vázquez-Juárez R (2008) MHC DQB-1 polymorphism in the Gulf of California fin whale (Balaenoptera physalus) population. J Hered 99: 14–21.
[69]  Klein J, Sato A, Nagl S, O'hUigín C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29: 1–21.

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