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The influence of positive selection and trans-species evolution on DPB diversity in the golden snub-nosed monkeys (Rhinopithecus roxellana)

Primates volume 57, pages 489–499 (2016)Cite this article

Abstract

Genetic variation plays a significant role in the adaptive potential of the endangered species. The variation at major histocompatibility complex (MHC) genes can offer valuable information on selective pressure related to natural selection and environmental adaptation, particularly the ability of a host to continuously resist evolving parasites. Thus, the genetic polymorphism on exon 2 of the MHC DPB1 gene in the golden snub-nosed monkeys (Rhinopithecus roxellana) was specifically analyzed. The results show that the 6 Rhro-DPB1 alleles identified from 87 individuals exhibit positive selection and trans-species polymorphism. The results also imply that although the populations of the species have experienced dramatic reduction and severe habitat fragmentation in recent Chinese history, balancing selection still maintains relatively consistent, with moderate DPB1 polymorphism. Thus, the study provides valuable information and evidence in developing effective strategies and tactics for genetic health and population size expansion of the species. It also offers strong genetic background for further studies on other primate species, particularly those in Rhinopithecus—a further endeavor that would result in fully understanding the MHC genetic information of the Asian colobines.

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Fig. 1
Fig. 2

Abbreviations

MHC:

Major histocompatibility complex

TSP:

Trans-species polymorphism

ABS:

Antigen binding sites

PCR:

Polymerase chain reaction

References

  • Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Allen M, Engström AS, Meyers S, Handt O, Saldeen T, von Haeseler A, Pääbo S, Gyllensten U (1998) Mitochondrial DNA sequencing of shed hairs and saliva on robbery caps: sensitivity and matching probabilities. J Forensic Sci 43:453–464

    CAS  Article  PubMed  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, Malden

    Google Scholar 

  • Anisimova M, Nielsen R, Yang ZH (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Antunes SG, de Groot NG, Brok H, Doxiadis G, Menezes AAL, Otting N, Bontrop RE (1998) The common marmoset: a new world primate species with limited MHC class II variability. Proc Natl Acad Sci USA 95:11745–11750

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Babik W, Pabijan M, Arntzen JW, Cogâlniceanu D, Durka W, Radwan J (2009) Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol 18:769–781

    CAS  Article  PubMed  Google Scholar 

  • Bamshad MJ, Mummidi S, Gonzalez E, Ahuja SS, Dunn DM, Watkins WS, Wooding S, Stone AC, Jorde LB, Weiss RB, Ahuja SK (2002) A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc Natl Acad Sci USA 99:10539–10544

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377

    CAS  Article  PubMed  Google Scholar 

  • Bollmer JL, Hull JM, Ernest HB, Sarasola JH, Parker PG (2011) Reduced MHC and neutral variation in the Galápagos hawk, an island endemic. BMC Evol Biol 11:143

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bontrop RE (2006) Comparative genetics of MHC polymorphisms in different primate species: duplications and deletions. Hum Immunol 67:388–397

    CAS  Article  PubMed  Google Scholar 

  • Bontrop RE, Otting N, de Groot NG, Doxiadis GG (1999) Major histocompatibility complex class II polymorphisms in primates. Immunol Rev 167:339–350

    CAS  Article  PubMed  Google Scholar 

  • Boyson JE, Iwanaga KK, Urvater JA, Hughes AL, Golos TG, Watkins DI (1999) Evolution of a new nonclassical MHC class I locus in two Old World primate species. Immunogenetics 49:86–98

    CAS  Article  PubMed  Google Scholar 

  • Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501–1515

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Doxiadis GG, Otting N, de Groot NG, Noort R, Bontrop RE (2000) Unprecedented polymorphism of MHC-DRB region configurations in rhesus macaques. J Immunol 164:3193–3199

    CAS  Article  PubMed  Google Scholar 

  • Doxiadis GG, 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

    CAS  Article  PubMed  Google Scholar 

  • Fang SG (2011) Does population increase alone ensure the long-term survival of endangered species? Chin Sci Bull 56:2521–2522

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)

  • Guindon S, Gascuel O (2003) PhyML: “a simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood”. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guo ST, Ji WH, Li M, Chang HL, Li BG (2010) The mating system of the Sichuan snub-nosed monkey (Rhinopithecus roxellana). Am J Primatol 72:25–32

    Article  PubMed  Google Scholar 

  • Gyllensten U, Bergstrom T, Josefsson A, Sundvall M, Erlich HA (1996) Rapid allelic diversification and intensified selection at antigen recognition sites of the MHC class II DPB1 locus during hominoid evolution. Tissue Antigens 47:212–221

    CAS  Article  PubMed  Google Scholar 

  • Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109

    Article  Google Scholar 

  • Huang K (2014) Genetic structure and phylogeography of Rhinopithecus roxellana qinlingensis. Doctoral dissertation, Northwest University, Xi’an, China, p 189. Available from: Northwest University

  • Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86:958–962

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jablonski NG, Whitfort MJ (1999) Environmental change during the Quaternary in East Asia and its consequences for mammals. Rec West Aust Mus (Suppl 57):307–315

  • Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695

    CAS  Article  PubMed  Google Scholar 

  • Kenter M, Otting N, Anholts J, Leunissen J, Jonker M, Bontrop RE (1992) Evolutionary relationships among the primate MHC-DQA1 and DQA2 alleles. Immunogenetics 36:71–78

    CAS  Article  PubMed  Google Scholar 

  • Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162

    CAS  Article  PubMed  Google Scholar 

  • Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219

    CAS  PubMed  Google Scholar 

  • Klein J, Sato A, Nikolaidis N (2007) MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Annu Rev Genet 41:281–304

    CAS  Article  PubMed  Google Scholar 

  • Li BG, Pan RL, Oxnard CE (2002) Extinction of snub-nosed monkeys in China during the past 400 years. Int J Primatol 23:1227–1244

    Article  Google Scholar 

  • Li BG, Jia ZY, Pan RL, Ren BP (2003) Changes in distribution of the snub-nosed monkey in China. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer/Plenum Publishers, New York, pp 29–51

    Chapter  Google Scholar 

  • Li JY, Yao YF, Zhou L, Xu HL (2012) Polymorphic analysis of MHC-DPB1 gene exon 2 in Tibetan macaques (Macaca thibetana). Hereditas 34:1417–1426

    CAS  Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  Article  PubMed  Google Scholar 

  • Ling F, Wei LQ, Wang T, Wang HB, Zhuo M, Du HL, Wang JF, Wang XN (2011) Characterization of the major histocompatibility complex class II DOB, DPB1, and DQB1 alleles in cynomolgus macaques of Vietnamese origin. Immunogenetics 63:155–166

    CAS  Article  PubMed  Google Scholar 

  • Lobo D, Godinho R, Álvares F, López-Bao JV, Rodríguez A (2015) A new method for noninvasive genetic sampling of saliva in ecological research. PLoS One 10:e0139765

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo MF, Pan HJ (2013) MHC II DRB variation and trans-species polymorphism in the golden snub-nosed monkey (Rhinopithecus roxellana). Chin Sci Bull 58:2119–2127

    CAS  Article  Google Scholar 

  • Luo MF, Liu ZJ, Pan HJ, Zhao L, Li M (2012a) Historical geographic dispersal of the golden snub-nosed monkey (Rhinopithecus roxellana) and the influence of climatic oscillations. Am J Primatol 74:91–101

    Article  PubMed  Google Scholar 

  • Luo MF, Pan HJ, Liu ZJ, Li M (2012b) 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 12:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshal TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and non-synonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • Ohta T (1998) On the pattern of polymorphisms at major histocompatibility complex loci. J Mol Evol 46:633–638

    CAS  Article  PubMed  Google Scholar 

  • Otting N, Doxiadis GG, Versluis L, de Groot NG, Anholts J, Verduin W, Rozemuller E, Claas F, Tilanus MG, Bontrop RE (1998) Characterization and distribution of MHC-DPB1 alleles in chimpanzee and rhesus macaque populations. Hum Immunol 59:656–664

    CAS  Article  PubMed  Google Scholar 

  • Otting N, de Groot NG, Noort MC, Doxiadis GG, Bontrop RE (2000) Allelic diversity of MHC-DRB alleles in rhesus macaques. Tissue Antigens 56:58–68

    CAS  Article  PubMed  Google Scholar 

  • Otting N, de Groot NG, Doxiadis GG, Bontrop RE (2002) Extensive MHC-DQB variation in humans and nonhuman primate species. Immunogenetics 54:230–239

    CAS  Article  PubMed  Google Scholar 

  • Otting N, Heijmans C, Noort RC, de Groot NG, Doxiadis GG, van Rood JJ, Watkins DI, Bontrop RE (2005) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 102:1626–1631

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Pan YR, Jablonski NG (1987) The age and geographical distribution of fossil cercopithecids in China. J Hum Evol 2:59–69

    Article  Google Scholar 

  • Pan RL, Groves C, Oxnard C (2004) Relationships between the fossil colobine Mesopithecus pentelicus and extant cercopithecoids, based on dental metrics. Am J Primatol 62:287–299

    Article  PubMed  Google Scholar 

  • Pan D, Li Y, Hu HX, Meng SJ, Men ZM, Fu YX, Zhang YP (2005) Microsatellite polymorphisms of Sichuan golden monkeys. Chin Sci Bull 50:2850–2855

    Article  Google Scholar 

  • Pan D, Hu HX, Meng SJ (2009) A high polymorphism level in Rhinopithecus roxellana. Int J Primatol 30:337–351

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) Genalex 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity (Edinburgh) 96:7–21

    CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  Article  PubMed  Google Scholar 

  • Qi XG, Li BG, Garber PA, Ji WH, Watanabe K (2009) Social dynamics of the golden snub-nosed monkey (Rhinopithecus roxellana): female transfer and one-male unit succession. Am J Primatol 71:670–679

    Article  PubMed  Google Scholar 

  • Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544

    Article  Google Scholar 

  • Reche PA, Reinherz EL (2003) Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 331:623–641

    CAS  Article  PubMed  Google Scholar 

  • Reinders J, Rozemuller EH, van Gent R, Arts-Hilkes YH, van den Tweel JG, Tilanus MG (2005) Extended HLA-DPB1 polymorphism: an RNA approach for HLA-DPB1 typing. Immunogenetics 57:790–794

    CAS  Article  PubMed  Google Scholar 

  • Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SGE (2013) IPD—the immuno polymorphism database. Nucleic Acids Res 41:1234–1240

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  Article  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sano K, Shiina T, Kohara S, Yanagiya K, Hosomichi K, Shimizu S, Anzai T, Watanabe A, Ogasawara K, Torii R, Kulski JK, Inoko H (2006) Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South-East Asian populations. Tissue Antigens 67:297–306

    CAS  Article  PubMed  Google Scholar 

  • Slierendregt BL, Otting N, Kenter M, Bontrop RE (1995) Allelic diversity at the MHC-DP locus in rhesus macaques (Macaca mulatta). Immunogenetics 41:29–37

    CAS  Article  PubMed  Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Stenzel A, Lu T, Koch WA, Hampe J, Guenther SM, De La Vega FM, Krawczak M, Schreiber S (2004) Patterns of linkage disequilibrium in the MHC region on human chromosome 6p. Hum Genet 114:377–385

    CAS  Article  PubMed  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Vaiman D, Mercier D, Moazami-Goudarzi K, Eggen A, Ciampolini R, Lépingle A, Velmala R, Kaukinen J, Varvio SL, Martin P (1994) A set of 99 cattle microsatellites: characterization, synteny mapping and polymorphism. Mamm Genome 5:288–297

    CAS  Article  PubMed  Google Scholar 

  • Vogel TU, Evans DT, Urvater JA, O’Connor DH, Hughes AL, Watkins DI (1999) Major histocompatibility complex class I genes in primates: co-evolution with pathogens. Immunol Rev 167:327–337

    CAS  Article  PubMed  Google Scholar 

  • Wan QH, Zhang P, Ni XW, Wu HL, Chen YY, Kuang YY, Ge YF, Fang SG (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. doi:10.1371/journal.pone.0014518

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wang YX, Jiang XL, Li DW (2003) Classification and distribution of the extant subspecies of golden snub-nosed monkey (Rhinopithecus [Rhinopithecus] roxellana. The natural history of the doucs and snub-nosed monkeys. World Scientific Press, London, pp 53–64

    Google Scholar 

  • Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol 13:711–718

    CAS  Article  PubMed  Google Scholar 

  • Xu B, Yang ZH (2013) pamlx: a graphical user interface for paml. Mol Biol Evol 30:2723–2724

    CAS  Article  PubMed  Google Scholar 

  • Xu HL, Wang YT, Cheng AC, Yao YF, Ni QY, Zeng W, Bi FJ, Yang ZX, Chen XY (2010) Polymorphism of MHC-DPB1 gene exon 2 in rhesus macaques (Macaca mulatta). Hereditas 32:588–598

    CAS  Article  PubMed  Google Scholar 

  • Yang ZH (2007) paml 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    CAS  Article  PubMed  Google Scholar 

  • Yasuda N (1988) HLA polymorphism information content (PIC). Jinrui Idengaku Zasshi 33:385–387

    CAS  Article  PubMed  Google Scholar 

  • Yongcheng L, Richardson M (2008) Rhinopithecus roxellana ssp. roxellana. In: The IUCN red list of threatened species, 2008. p e.T39829A10273824

  • Zhang P, Song XY, Huang K, Chen D, Guo ST, Qi XG, He G, Li BG (2016) Genetic diversity and conservation strategy of the golden snub-nosed monkey (Rhinopithecus roxellana). Biochem Syst Ecol (in press)

  • Zhang P, Watanabe K, Li BG, Tan CL (2006) Social organization of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, Central China. Primates 47:374–382

    Article  PubMed  Google Scholar 

  • Zhou XM, Wang BS, Pan Q, Zhang JB, Kumar S, Sun XQ, Liu ZJ, Pan HJ, Lin Y, Liu GJ, Zhan W, Li MZ, Ren BP, Ma XY, Ruan H, Cheng C, Wang DW, Shi FL, Hui YY, Tao YJ, Zhang CL, Zhu PF, Xiang ZF, Jiang WK, Chang J, Wang HL, Cao ZS, Jiang Z, Li BG, Yang G, Roos C, Garber PA, Bruford MW, Li RQ, Li M (2014) Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history. Nat Genet 46:1303–1310

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We thank the staff at the Shaanxi Key Laboratory for Animal Conservation for the study samples in this study, which was/is being supported by the National Natural Science Foundation of China (NSFC, 31130061, 31201721, 31270441, 31270438, 31501872), the Natural Science Foundation of Shaanxi Province, China (2014JM3072), and Scientific Research Foundation of the Education Department of Shaanxi Province, China (12JK0837).

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    Affiliations

    1. Shaanxi Key Laboratory for Animal Conservation, and College of Life Sciences, Northwest University, Xi’an, 710069, China

      Xiaoyue Song, Pei Zhang, Kang Huang, Dan Chen, Songtao Guo, Xiaoguang Qi, Gang He, Ruliang Pan & Baoguo Li

    2. The School of Anatomy, Physiology and Human Biology, University of Western Australia, Perth, Australia

      Ruliang Pan

    3. Xi’an Branch of Chinese Academy of Sciences, Xi’an, China

      Baoguo Li

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    1. Xiaoyue Song
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    Our research complied with the protocols approved by animal care committees of the Wildlife Protection Society of Shaanxi Province, China. We strictly adhered to the legal requirements of the current laws of China’s animal conservation and protection.

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    X. Song and P. Zhang contributed equally to the work.

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    Song, X., Zhang, P., Huang, K. et al. The influence of positive selection and trans-species evolution on DPB diversity in the golden snub-nosed monkeys (Rhinopithecus roxellana). Primates 57, 489–499 (2016). https://doi.org/10.1007/s10329-016-0544-0

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    Keywords

    • MHC
    • Rhinopithecus roxellana
    • Positive selection
    • Trans-species polymorphism
    • Genetic diversity