期刊论文详细信息
BMC Evolutionary Biology
Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana)
Ming Li3  Zhi-Jin Liu3  Hui-Juan Pan1  Mao-Fang Luo2 
[1] College of Nature Conservation, Beijing Forestry University, Beijing, 100083, China;Graduate School of the Chinese Academy of Sciences, Beijing, 100049, China;Key laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1-5 Beixhenxi Road, Chaoyang, Beijing, 100101, China
关键词: Rhinopithecus roxellana;    MHC;    Gene drift;    Conservation genetics;    Balancing selection;   
Others  :  1140162
DOI  :  10.1186/1471-2148-12-207
 received in 2012-02-28, accepted in 2012-10-05,  发布年份 2012
PDF
【 摘 要 】

Background

Small, isolated populations often experience loss of genetic variation due to random genetic drift. Unlike neutral or nearly neutral markers (such as mitochondrial genes or microsatellites), major histocompatibility complex (MHC) genes in these populations may retain high levels of polymorphism due to balancing selection. The relative roles of balancing selection and genetic drift in either small isolated or bottlenecked populations remain controversial. In this study, we examined the mechanisms maintaining polymorphisms of MHC genes in small isolated populations of the endangered golden snub-nosed monkey (Rhinopithecus roxellana) by comparing genetic variation found in MHC and microsatellite loci. There are few studies of this kind conducted on highly endangered primate species.

Results

Two MHC genes were sequenced and sixteen microsatellite loci were genotyped from samples representing three isolated populations. We isolated nine DQA1 alleles and sixteen DQB1 alleles and validated expression of the alleles. Lowest genetic variation for both MHC and microsatellites was found in the Shennongjia (SNJ) population. Historical balancing selection was revealed at both the DQA1 and DQB1 loci, as revealed by excess non-synonymous substitutions at antigen binding sites (ABS) and maximum-likelihood-based random-site models. Patterns of microsatellite variation revealed population structure. FST outlier analysis showed that population differentiation at the two MHC loci was similar to the microsatellite loci.

Conclusions

MHC genes and microsatellite loci showed the same allelic richness pattern with the lowest genetic variation occurring in SNJ, suggesting that genetic drift played a prominent role in these isolated populations. As MHC genes are subject to selective pressures, the maintenance of genetic variation is of particular interest in small, long-isolated populations. The results of this study may contribute to captive breeding and translocation programs for endangered species.

【 授权许可】

   
2012 Luo et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324122513951.pdf 3102KB PDF download
Figure 5. 60KB Image download
Figure 4. 93KB Image download
Figure 3. 15KB Image download
Figure 2. 54KB Image download
Figure 1. 58KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Peacock MM, Smith AT: The effects of habitat fragmentation on dispersal patterns, mating behavior and genetic variation in a pica (Ochotona princeps) metapopulation. Oecol 1997, 112:524-533.
  • [2]Sommer S: The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2005, 2:16. BioMed Central Full Text
  • [3]Allendorf FW, Luikart G: Units of conservation. In: Conservation and the genetics of populations. Oxford: Blackwell Publishing; 2007:380-420.
  • [4]Frankham R: Genetics and extinction. Biol Conserv 2005, 126:131-140.
  • [5]Frankham R, Ballou JD, Briscoe DA: Introduction to Conservation Genetics (2nd edn). Cambridge: Cambridge University Press; 2010:1-618.
  • [6]Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW: Conservation genetics in transition to conservation genomics. Trends Genet 2010, 26:177-187.
  • [7]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.
  • [8]Morin PA, Luikart G, Wayne RK, the SNP workshop group: SNPs in ecology, evolution and conservation. Trends Ecol Evo 2004, 19:208-216.
  • [9]Spurgin LG, Richardson DS: How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 2010, 277:979-988.
  • [10]Garrigan D, Hedrick PW: Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 2003, 57:1707-1722.
  • [11]Andersson L, Mikko S: Generation of MHC class II diversity by intra- and intergenic recombination. Immunol Rev 1995, 143:5-12.
  • [12]Bergstrom TF, Josefsson A, Erlich HA, Gyllensten U: Recent origin of HLA-DRB1 alleles and implications for human evolution. Nat Genet 1998, 18:237-242.
  • [13]Van Oosterhout C, Joyce DA, Cummings SM, Blais J, Barson NJ, Ramnarine IW, Mohammed RS, Persad N, Cable J: Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 2006, 60:2562-2574.
  • [14]Sutton JT, Nakagawa S, Robertson BC, Jamieson IG: Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 2011, 20:4408-4420.
  • [15]Miller KM, Kaukinen KH, Beacham TD, Withler RE: Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 2001, 111:237-257.
  • [16]Hedrick PW, Lee RN, Buchanan C: Canine parvovirus enteritis, canine distemper, and major histocompatibility complex genetic variation in Mexican wolves. J Wildlife Dis 2003, 39:909-913.
  • [17]Castro-Prieto A, Wachter B, Melzheimer J, Thalwitzer S, Sommer S: Diversity and evolutionary patterns of immune genes in free-ranging Namibian leopards (Panthera pardus pardus). Heredity 2011, 102:653-665.
  • [18]Mikko S, Roed K, Schmutz S, Andersson L: Monomorphism and polymorphism at MHC DRB loci in domestic and wild ruminants. Immunol Rev 1999, 167:169-178.
  • [19]Weber DS, Stewart BS, Schienman J, Lehman N: Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol 2004, 13:711-718.
  • [20]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.
  • [21]Mason RAB, Browning TL, Eldridge DB: Reduced MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (Petrogale lateralis lateralis). Conserv Genet 2011, 12:91-103.
  • [22]Biedrzycka A, Radwan J: Population fragmentation and major histocompatibility complex variation in the spotted suslik, Spermophilus suslicus. Mol Ecol 2008, 17:4801-4811.
  • [23]Beaumont MA, Nichols RA: Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B 1996, 263:1619-1626.
  • [24]Radwan J, Biedrzycka A, Babik W: Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 2010, 143:537-544.
  • [25]Aguilar A, Garza JC: A comparison of variability and population structure for major histocompatibiltiy complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykiss Walbaum). Mol Ecol 2006, 15:923-937.
  • [26]Zhang RZ: The primates of China: biogeography and conservation status—past, present and future. Beijing: China Forestry Publishing House; 2002.
  • [27]Li M, Liu ZJ, Gou JX, Ren BP, Pan RL, Su YJ, Funk SM, Wei FW: Phylogeography and population structure of the golden monkeys (Rhinopithecus roxellana): inferred from mitochondrial DNA sequences. Am J Primatol 2007, 69:1195-1209.
  • [28]Pan D, Hu HX, Meng SJ, Men ZM, Fu YX, Zhang YP: A high polymorphism level in Rhinopithecus roxellana. Int J Primatol 2009, 30:337-351.
  • [29]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.
  • [30]Boessenkool S, Taylor SS, Tepolt CK, Komdeur J, Jamieson IG: Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges. Conserv Genet 2007, 8:705-714.
  • [31]Hedrick PW, Parker KM, Miller EL, Miller PS: Major histocompatiblity complex variation in the endangered Przewalski's horse. Genetics 2001, 152:1701-1710.
  • [32]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.
  • [33]Chang ZF, Liu ZJ, Yang JY, Li M, Vigilant L: Noninvasive genetic assessment of the population trend and sex ratio of the Shennongjia population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Chinese Sci Bull 2011, 57:1135-1141.
  • [34]Luo MF, Liu ZJ, Pan HJ, Zhao L, Li M: Historical geographic dispersal of the golden snub-nosed monkey (Rhinopithecus roxellana) and the influence of climatic oscillations. Am J Primatol 2012, 74:91-101.
  • [35]Bijlsma R, Bundgaard J, Boerema AC: Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J Evolution Biol 2000, 13:502-514.
  • [36]Thoß M, Ilmonen P, Musolf K, Penn DJ: Major histocompatibility complex heterozygosity enhances reproductive success. Mol Ecol 2011, 20:1546-1557.
  • [37]Lukas D, Bradley BJ, Nsubuga AM, Doran-Sheehy D, Robbins MM, Vigilant L: Major histocompatibility complex and microsatellite variation in two populations of wild gorillas. Mol Ecol 2004, 13:3389-3402.
  • [38]Goda1 N, Mano T, Kosintsev P, Vorobie A, Masuda R: 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 2010, 76:404-410.
  • [39]Kennedy LJ, Randall DA, Knobel D, Brown JJ, Fooks AR, Argaw K, Shiferaw F, Ollier WER, Sillero-Zubiri C, Macdonald DW, Laurenson MK: Major histocompatibility complex diversity in the endangered Ethiopian wolf (Canis simensis). Tissue Antigens 2010, 77:118-125.
  • [40]Radwan J, Demiaszkiewicz AW, Kowalczyk R, Lachowicz J, Kawalko A, Wojcik JM, Pyziel AM, Babik W: An evaluation of two potential risk factors, MHC diversity and host density, for infection by an invasive nematode Ashworthius sidemi in endangered European bison (Bison bonasus). Biol Conserv 2010, 143:2049-2053.
  • [41]Pokorny I, Sharma R, Goyal SP, Mishra S, Tiedemann R: MHC class I and MHC class II DRB gene variability in wild and captive Bengal tigers (Panthera tigris tigris). Immunogenetics 2010, 62:667-679.
  • [42]Kimura M: Preponderance of synonymous changes as evidence for the neutrality theory of molecular evolution. Nature 1977, 267:275-276.
  • [43]Hughes AL, Nei M: Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 1988, 335:167-170.
  • [44]Hughes AL, Nei M: Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 1989, 86:958-962.
  • [45]Hughes AL: Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 2007, 99:364-373.
  • [46]Klein J, Sato A, Nikolaidis N: MHC, TSP, and the origin of species: From immunogenetics to evolutionary genetics. Annu Rev Genet 2007, 41:281-304.
  • [47]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.
  • [48]Li HS, Ligons DL, Rose NR: Genetic complexity of autoimmune myocarditis. Autoimm reviews 2008, 7:168-173.
  • [49]Schaschl H, Suchentruk F, Hammer S, Goodman SJ: Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.). Immunogenetics 2005, 57:108-115.
  • [50]Xu SX, Ren WH, Zhou XM, Zhou KY, Yang G: Sequence polymorphism and geographical variation at a positively selected MHC-DRB gene in the finless porpoise (Neophocaena phocaenoides): Implication for recent differentiation of the Yangtze finless porpoise? J Mol Ecol 2010, 71:6-22.
  • [51]Kauppi L, Jeffreys AJ, Keeney S: Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 2004, 5:413-424.
  • [52]Bonneaud C, Chastel O, Federici P, Westerdahl , Sorci G: Complex Mhc-based mate choice in a wild passerine. Proc R Soc B 2006, 273:1111-1116.
  • [53]Muirhead CA: Consequences of population structure on genes under balancing selection. Evolution 2001, 55:1532-1541.
  • [54]Richman AD, Herrera LG, Nash D: Evolution of MHC class II E beta diversity within the genus Peromysus. Genetics 2003, 164:289-297.
  • [55]Miller HC, Lambert DM: Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 2004, 13:3709-3721.
  • [56]Kimura M: The Neutral Theory of Molecular Evolution. Cambridge: Cambridge University Press; 1983.
  • [57]Maureen BP, Thomas FT: Genetic variation of the major histocompatibility complex (MHC class II b gene) in the threatened Gila trout, Oncorhynchus gilae gilae. Conserv Genet 2008, 9:257-270.
  • [58]Agudo R, Alcaide M, Rico C, Lemus JA, Blanco G, Hiraldo F, Donázar JA: Major histocompatibility complex varian in insular populations of the Egyptian vulture: inferences about the roles of genetic drift and selection. Mol Ecol 2011, 20:2329-2340.
  • [59]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.
  • [60]Ujvari B, Belov K: Major histocompatibility complex (MHC) markers in conservation biology. Int J Mol Sci 2011, 12:5168-5186.
  • [61]Tallmon DA, Luikart G, Waples RS: The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 2004, 19:489-496.
  • [62]Edmands S: Between a rock and a hard place: Evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 2007, 16:463-475.
  • [63]Vilà C, Sundqvist AK, Flagstad O, Seddon J, Björnerfeldt S, Kojola I, Casulli A, Sand H, Wabakken P, Ellegren H: Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc R Soc Lond B 2003, 270:91-97.
  • [64]Madsen T, Ujvari B, Olsson M: Novel genes continue to enhance population growth in adders (Vipera berus). Biol Conserv 2004, 120:145-147.
  • [65]Bouzat JL, Johnson JE, Toepfer JE, Simpson SA, Esker TL, Westemeier RL: Beyond the beneficial effects of translocations in an effective tool for the genetic restoration of isolated populations. Conserv Genet 2009, 10:191-201.
  • [66]Doxiadis GGM, Otting N, de Groot NG, Groot N, Rouweler AJM, Noort R, Verschoor EJ, Bontjer I, Bontrop RE: Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 2003, 55:540-551.
  • [67]Nei M: Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
  • [68]Excoffier L, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
  • [69]Goudet J: FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). 2001. Available from http://www.unil.ch/izea/softwares/fstat.html webcite. Updated from Goudet (1995).
  • [70]Rousset F: Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 2008, 8:103-106.
  • [71]Weir BS: Inferences about linkage disequilibrium. Biometrics 1979, 35:235-254.
  • [72]Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
  • [73]Tamura K, Dudley J, Nei M, Kumar S: MEGA 4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
  • [74]Kennedy LJ, Ryvar R, Gaskell RM, Addie D, Willoughby K, Carter S, Thomson W, Ollier W, Radford A: Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 2002, 54:348-352.
  • [75]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
  • [76]Falush D, Stephens M, Pritchard J: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587.
  • [77]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol 2005, 14:2611-2620.
  • [78]Guindon S, Gascuel O: A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [79]Posada D, Crandall KA: Modeltest: Testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
  • [80]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
  • [81]Hudson RR: Two-locus sampling distributions and their application. Genetics 2001, 159:1805-1817.
  • [82]McVean G, Awadalla P, Fearnhead P: A coalescennt-based method for detecting and estimating recombination from gene sequences. Genetics 2002, 160:1231-1241.
  • [83]Richman AD, Herrera LG, Nash D, Schierup MH: Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res 2003, 82:89-99.
  • [84]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
  • [85]Reche PA, Reinherz EL: Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 2003, 331:623-641.
  • [86]Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC: 3-Dimensional structure of the human class-II histocompatibility antigen HLA-DR1. Nature 1993, 364:33-39.
  • [87]Kuduk K, Johanet A, Allaine D, Cohas A, Radwan J: Contrasting patterns of selection acting on MHC class I and class II DRB genes in the Alpine marmot (Marmota marmota). J Evolutiona Biol 2012.
  • [88]Kloch A, Baran K, Buczek M, Konarzewski M, Radwan J: MHC influences infection with parasites and wintersurvival in the root vole Microtus oeconomus. Evol Ecol 2012.
  • [89]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
  • [90]Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 1994, 11:725-736.
  • [91]Yang Z, Nielsen R, Goldman N, Pedersen AMK: Codon substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
  • [92]Yang Z, Wong WSW, Nielsen R: Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22:1107-1111.
  • [93]Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G: LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 2008, 9:323. BioMed Central Full Text
  文献评价指标  
  下载次数:63次 浏览次数:19次