期刊论文详细信息
BMC Evolutionary Biology
Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles
Huai-Liang Xu2  Ming-Wang Zhang1  Qing-Yong Ni1  Jing Li3  Qiu-Xia Dai1  Yong-Fang Yao1 
[1] College of Animal Science and Technology, Sichuan Agricultural University, Ya´an 625014, China;Experimental Animal Engineering Center/National Experimental Macaque Reproduce Laboratory, Sichuan Agricultural Universiy, Ya′an 625014, China;College of Life Sciences, Sichuan University, Chengdu 610064, China
关键词: Trans-species evolution;    Major histocompatibility complex;    Macaca mulatta;    Genetic differentiation;    Genetic diversity;   
Others  :  855278
DOI  :  10.1186/1471-2148-14-130
 received in 2013-12-14, accepted in 2014-06-02,  发布年份 2014
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【 摘 要 】

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Background

Rhesus macaques living in western Sichuan, China, have been separated into several isolated populations due to habitat fragmentation. Previous studies based on the neutral or nearly neutral markers (mitochondrial DNA or microsatellites) showed high levels of genetic diversity and moderate genetic differentiation in the Sichuan rhesus macaques. Variation at the major histocompatibility complex (MHC) loci is widely accepted as being maintained by balancing selection, even with a low level of neutral variability in some species. However, in small and isolated or bottlenecked populations, balancing selection may be overwhelmed by genetic drift. To estimate microevolutionary forces acting on the isolated rhesus macaque populations, we examined genetic variation at Mhc-DQB1 loci in 119 wild rhesus macaques from five geographically isolated populations in western Sichuan, China, and compared the levels of MHC variation and differentiation among populations with that previously observed at neutral microsatellite markers.

Results

23 Mamu-DQB1 alleles were identified in 119 rhesus macaques in western Sichuan, China. These macaques exhibited relatively high levels of genetic diversity at Mamu-DQB1. The Hanyuan population presented the highest genetic variation, whereas the Heishui population was the lowest. Analysis of molecular variance (AMOVA) and pairwise FST values showed moderate genetic differentiation occurring among the five populations at the Mhc-DQB1 locus. Non-synonymous substitutions occurred at a higher frequency than synonymous substitutions in the peptide binding region. Levels of MHC variation within rhesus macaque populations are concordant with microsatellite variation. On the phylogenetic tree for the rhesus and crab-eating macaques, extensive allele or allelic lineage sharing is observed betweenthe two species.

Conclusions

Phylogenetic analyses confirm the apparent trans-species model of evolution of the Mhc-DQB1 genes in these macaques. Balancing selection plays an important role in sharing allelic lineages between species, but genetic drift may share balancing selection dominance to maintain MHC diversity. Great divergence at neutral or adaptive markers showed that moderate genetic differentiation had occurred in rhesus macaque populations in western Sichuan, China, due to the habitat fragmentation caused by long-term geographic barriers and human activity. The Heishui population should be paid more attention for its lowest level of genetic diversity and relatively great divergence from others.

【 授权许可】

   
2014 Yao et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Sommer S: Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 2003, 12(10):2845-2851.
  • [2]Gregorius HR: The relationship between the concepts of genetic diversity and differentiation. Theor Appl Genet 1987, 74(3):397-401.
  • [3]Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne R: High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 2004, 101:3490-3494.
  • [4]Kohn MH, Murphy WJ, Ostrander EA, Wayne RK: Genomics and conservation genetics. Trends Ecol Evol 2006, 21:629-637.
  • [5]Bonin A, Nicole F, Pompanon F, Miaud C, Taberlet P: Population adaptive index: a new method to help measure intraspecific genetic diversity and prioritize populations for conservation. Conserv Biol 2007, 21:697-708.
  • [6]Miller HC, Allendorf F, Daugherty CH: Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 2010, 19:3894-3908.
  • [7]Siddle HV, Kreiss A, Eldridge MDB, Noonan E, Clarke CJ, Pyecroft S, Woods GM, Belov K: Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci USA 2007, 104:16221-16226.
  • [8]Spurgin LG, Richardson DS: How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 2010, 277:979-988.
  • [9]Bernatchez L, Landry C: MHC studies in nonmodel vertebrates: what have we learned about natural selection in15 years? J Evol Biol 2003, 16:363-377.
  • [10]Piertney SB, Oliver MK: The evolutionary ecology of the major histocompatibility complex. Heredity 2006, 96:7-21.
  • [11]Alcaide M, Lemus JA, Blanco G, Tella J, Serrand D, Negro JJ, Rodriguez A, Garcia-Montijano M: MHC diversity and differential exposure to pathogens in kestrels (Aves: Falconidae). Mol Ecol 2010, 19:691-705.
  • [12]Campos JL, Posada D, Moran P: Genetic variation at MHC, mitochondrial and microsatellite loci in isolated populations of Brown trout (Salmo trutta). Conserv Genet 2006, 7:515-530.
  • [13]Babik W, Pabijan M, Arntzen JW, Cogalniceanu D, Durka W, Radwan J: Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol 2009, 18:769-781.
  • [14]Luo MF, Pan HJ, Liu ZJ, Li M: Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana). BMC Evol Biol 2012, 12:207. BioMed Central Full Text
  • [15]Sommer S: The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2005, 2:1-18. BioMed Central Full Text
  • [16]Oubory NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW: Conservation genetics in transition to conservation genomics. Trends Genet 2010, 26(4):177-187.
  • [17]Allendorf FW, Luikart G: Conservation and the Genetics of Populations. Malden, MA: Blackwell Publishing; 2007.
  • [18]Frankham R: Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 2010, 143(9):1919-1927.
  • [19]Frankham R: Genetics and extinction. Biol Conserv 2005, 126(2):131-140.
  • [20]Jiang XL, Wang YX, Ma SL: Taxonomic revision and distributin of subspecies of rhesus monke (macaca mulatta) in China. Zool Res 1991, 12:241-247.
  • [21]Lewontin RC: The Genetic Basis of Evolutionary Change. New York: Columbia University Press; 1974.
  • [22]Rockman MV: The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 2012, 66(1):1-17.
  • [23]Morin PA, Luikart G: Wayne RK, the SNP workshop group: SNPs in ecology, evolution and conservation. Trends Ecol Evol 2004, 19(4):208-216.
  • [24]Xu HL, Wang YT, Cheng AC, Yao YF, Ni QY, Zeng W, Bi FJ, Yang ZX, Chen XY: Polymorphism of MHC-DPB1 gene exon 2 in rhesus macaques (Macaca mulatta). Yi Chuan 2010, 32:588-598.
  • [25]Li DY, Xu HL, Trask JS, Zhu Q, Cheng AC, Smith DG, George D, Zhang L: Genetic diversity and population structure in wild Sichuan rhesus macaques. Mol Biol Rep 2013, 40:3033-3041.
  • [26]Wu SJ, Luo J, Li QQ, Wang YQ, Robert WM, Blair C, Wu SF, Yue BS, Zhang YP: Ecological genetics of Chinese rhesus macaque in response to mountain building: all things are not equal. PLoS One 2013, 8:2.
  • [27]Leuchte N, Berry N, Köhler B, Almond N, LeGrand R, Thorstensson R, Titti F, Sauermann U: MhcDRB-sequences from cynomolgus macaques (Macaca fascicularis) of different origin. Tissue Antigens 2004, 63(6):529-537.
  • [28]Sano K, Shiina T, Kohara S, Yanagiya K, Hosomichi K, Shimizu S, Anzai T, Watanabe A, Ogasawara K, Torii R, Kulski JK, Inoko H: Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South-East Asian populations. Tissue Antigens 2006, 67(4):297-306.
  • [29]Diaz D, Naegeli M, Rodriguez R, Nino-Vasquez JJ, Moreno A, Patarroyo ME, Pluschke G, Daubenberger CA: Sequence and diversity of MHC DQA and DQB genes of the owl monkey Aotus nancymaae. Immunogenetics 2000, 51(7):528-537.
  • [30]Otting N, de Groot NG, Doxiadis GG, Bontrop RE: Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 2002, 54(4):230-239.
  • [31]Qiu CL, Yang GB, Yu K, Li Y, Li LX, Liu Q, Zhao H, Xing H, Shao YM: Characterization of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles in a cohort of Chinese rhesus macaques (Macaca mulatta). Hum Immunol 2008, 69:513-521.
  • [32]Hansson B, Westerberg L: On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 2002, 11:2467-2474.
  • [33]Reed DH, Frankham R: Correlation between fitness and genetic diversity conserve. Biogeosciences 2003, 17:230-237.
  • [34]Leimu R, Mutikainen P, Koricheva J, Fischer M: How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 2006, 94:942-952.
  • [35]Joron M, Brakefield PM: Captivity masks inbreeding effects on male mating success in butterflies. Nature 2003, 424:191-194.
  • [36]Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B: Genetic diversity and the survival of populations Plant. Biogeosciences 2000, 2:379-395.
  • [37]Smith DG, McDonough J: Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am J Primatol 2005, 65(1):1-25.
  • [38]Doxiadis GG, Otting N, de Groot NG, de Groot N, Rouweler AJ, Noort R: Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 2003, 55:540.
  • [39]Miller KM, Kaukinen KH, Beacham TD, Withler RE: Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetics 2001, 111:237-257.
  • [40]Bryja J, Charbonnel N, Berthier K, Galan M, Cosson JF: Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Mol Ecol 2007, 16:5084-5097.
  • [41]Ekblom R, Saether SA, Jacobsson P, Fiske P, Sahlman T, Grahn M, Kalas JA, Hoglund J: Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 2007, 16:1439-1451.
  • [42]Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL: Extensive polymorphism and geographical variation at a positively selected MHC class IIB gene of the lesser kestrel (Falco naumanni). Mol Ecol 2008, 17:2652-2665.
  • [43]Penn DJ: The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 2002, 108:1-21.
  • [44]Milinski M: The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 2006, 37:159-186.
  • [45]Huchard E, Baniel A, Schliehe-Diecks S, Kappeler PM: MHC-disassortative mate choice and inbreeding avoidance in a solitary primate. Mol Ecol 2013, 22(15):4071-4086.
  • [46]Klein J: Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 1987, 19:155-162.
  • [47]Kamath PL, Getz WM: Adaptive molecular evolution of the major histocompatibility complex genes, DRA and DQA, in the genus Equus. BMC Evol Biol 2011, 11:128. BioMed Central Full Text
  • [48]Radwan J, Biedrzycka A, Babik W: Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 2010, 143:537-544.
  • [49]Wei K, Zhang ZH, Wang XF, Zhang WP, Xu X, Shen FJ, Yue BS: Lineage pattern, trans-species polymorphism, and selection pressure among the major lineages of feline Mhc-DRB peptide-binding region. Immunogenetics 2010, 62:307-317.
  • [50]Yao YF, Zhao JJ, Dai QX, Li JY, Zhou L, Wang YT, Ni QY, Zhang MW, Xu HL: Identification and characterization of the major histocompatibility complex class II DQB (MhcMath-DQB1) alleles in Tibetan macaques (Macaca thibetana). Tissue Antigens 2013, 82(2):113-121.
  • [51]van Oosterhout C: Trans-species polymorphism, HLA-disease associations and the evolution of the MHC. Commun Integr Biol 2009, 2:408-410.
  • [52]Figureroa F, Gunther E, Klein J: MHC polymorphism pre-dating speciation. Nature 1988, 335:265-267.
  • [53]Hayasaka K, Fujii K, Horai S: Molecular phylogeny of macaques: implications of nucleotide sequences from an 896 base pair region of mitochondrial DNA. Mol Biol Evol 1996, 13:1044-1053.
  • [54]Yan G, Zhang G, Fang X, Zhang Y, Li C, Ling F, Cooper DN, Li Q, Li Y, van Gool AJ, Du H, Chen J, Chen R, Zhang P, Huang Z, Thompson JR, Meng Y, Bai Y, Wang J, Zhuo M, Wang T, Huang Y, Wei L, Li J, Wang Z, Hu H, Yang P, Le L, Stenson PD, Li B, et al.: Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nat Biotechnol 2011, 29(11):1019-1023.
  • [55]Wright S: The genetical structure of populations. Ann Eugenics 1949, 15:323-354.
  • [56]Yasukochi Y, Nishida S, Han SH, Kurosaki T, Yoneda M, Koike H: Genetic structure of the Asiatic black bear in Japan using mitochondrial DNA analysis. J Hered 2009, 100:297-308.
  • [57]Wright S: The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 1965, 19:395-420.
  • [58]Millar C, Libby W: Strategies for conserving clinal, ccotypic, and disjunct population diversity in widespread species. In Genetics and Conservation of Rare Plants. Edited by Fald DA, Holsinger KE. New York: Oxford University Press; 1991:149-170.
  • [59]Slatkin M: Gene flow and the geographic structure of natural populations. Science 1987, 236(4803):787.
  • [60]Zhu L, Zhang S, Gu X, Wei F: Significant genetic boundaries and spatial dynamics of giant pandas occupying fragmented habitat across southwest China. Mol Ecol 2011, 20:1122-1132.
  • [61]Yao YF, Zhong LJ, Li BF, Li JY, Ni QY, Xu HL: Genetic variation between two Tibetan macaque (Macaca thibetana) populations in the eastern China based on mitochondrial DNA control region sequences. Mitochondrial DNA 2013, 24(3):267-275.
  • [62]Schierup MH, Hein J: Consequences of recombination on traditional phylogenetic analysis. Genetics 2000, 156(2):879-891.
  • [63]Luikart G, England PR, Tallmon D, Jordan S, Taberlet P: The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 2003, 4:981-994.
  • [64]Chang ZF, Luo MF, Liu ZJ, Yang JY, Xiang ZF, Li M, Vigilant L: Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Genetica 2012, 140:105-114.
  • [65]Oliver MK, Lambin X, Cornulier T, Piertney SB: Spatio-temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations. Mol Ecol 2009, 18:80-92.
  • [66]Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI: Nomenclature for the major histocompatibility complexes of different species: A proposal. Immunogenetics 1990, 31:217-219.
  • [67]Mason RAB, Browning TL, Eldridge DB: Reduced MHC class II diversity in island compared to mainland populations of the black-footed rockwallaby (Petrogale lateralis lateralis). Conserv Genet 2011, 12:91-103.
  • [68]Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning, A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press; 1989.
  • [69]Xia X, Xie Z: DAMBE: data analysis in molecular biology andevolution. J Hered 2001, 92:371-373.
  • [70]Rozas R, Sánchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19(18):2496-2497.
  • [71]Peakall R, Peter E: Smouse: genetic analysis in excel, population genetic software for teaching and research. Bioinformatics 2012, 28(19):2537-2539.
  • [72]Goudet J: FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). 2001. Available from http://www2.unil.ch/popgen/softwares/fstat.htm webcite
  • [73]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
  • [74]Amills M, Ramirez O, Tomas A, Obexer-Ruff G, Vidal O: Positive selection on mammalian MHC-DQ genes revisited from a multispecies perspective. Genes Immun 2008, 9:651-658.
  • [75]Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
  • [76]Yao YF, Dai QX, Li J, Ni QY, Zhang MW, Xu HL: Data from: Genetic diversity and differentiation of the rhesus macaque (Macaca mulatta) population in western Sichuan, China, based on the second exon of the major histocompatibility complex class II DQB (MhcMamu-DQB1) alleles. Dryad Digital Repository 2014. doi:10.5061/dryad.h8b93
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