An SNP marker at the STAT6 locus can identify the hybrids between rhesus (Macaca mulatta) and long-tailed macaques (M. fascicularis) in Thailand: a rapid and simple screening method and its application
详细信息    查看全文
  • 作者:Janya Jadejaroen ; Yoshi Kawamoto ; Yuzuru Hamada ; Suchinda Malaivijitnond
  • 关键词:STAT6 ; PCR–RFLP ; ApaI ; Macaca fascicularis ; M. mulatta ; Hybridization
  • 刊名:Primates
  • 出版年:2016
  • 出版时间:January 2016
  • 年:2016
  • 卷:57
  • 期:1
  • 页码:93-102
  • 全文大小:575 KB
  • 参考文献:Barr A, Premasuthan A, Satkoski J, Smith DG, George D, Kanthaswamy S (2011) A rapid quantitative real-time PCR-based quantification assay coupled with species-assignment capabilities for two-hybridizing Macaca species. Folia Primatol 82:71–80PubMed PubMedCentral CrossRef
    Bonhomme M, Cuartero S, Blancher A, Crouau-Roy B (2009) Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis). J Hered 100:158–169PubMed CrossRef
    Code of Best Practices for Field Primatology (2014) http://​www.​internationalpri​matologicalsocie​ty.​org/​docs/​Code%20​of_​Best_​Practices%20​Oct%20​2014.​pdf . Accessed 1 Dec 2014
    Creager HM, Becker EA, Sandman KK, Karl JA, Lank SM, Bimber BN, Wiseman RW, Hughes AL, O’Connor SL, O’Connor DH (2011) Characterization of full-length MHC class II sequences in Indonesian and Vietnamese cynomolgus macaques. Immunogenetics 63:611–618PubMed PubMedCentral CrossRef
    Delphin S, Stavnezer J (1995) Characterization of an interleukin 4 (IL-4) responsive region in the immunoglobulin heavy chain germline epsilon promoter: regulation by NF-IL-4, a C/EBP family member and NF-kappa B/p50. J Exp Med 81:181–192CrossRef
    Ferguson B, Street SL, Wright H, Pearson C, Jia Y, Thompson SL, Allibone P, Dubay CJ, Spindel E, Norgren RB (2007) Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genom 8:43CrossRef
    Fooden J (1982) Ecogeographic segregation of macaque species. Primates 23:574–579CrossRef
    Fooden J (1995) Systematic review of Southeast Asian long-tailed macaques, Macaca fascicularis (Raffles, 1821). Fieldiana Zool 81:1–206
    Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana Zool 96:1–180
    Godava M, Vrtel R, Vodicka R (2013) STAT6- polymorphisms, haplotypes and epistasis in relation to atopy and asthma. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 157:172–180PubMed
    Hamada Y, Watanabe T, Chatani K, Hayakawa S, Iwamoto M (2005) Morphometrical comparison between Indian- and Chinese-derived rhesus macaques (Macaca mulatta). Anthropol Sci 113:183–188CrossRef
    Hamada Y, Urasopon N, Hadi I, Malaivijitnond S (2006) Body size and proportions and pelage color of free-ranging Macaca mulatta from a zone of hybridization in northern Thailand. Int J Primatol 27:497–513CrossRef
    Hamada Y, Suryobroto B, Goto S, Malaivijitnond S (2008) Morphological and body color variation in Thai Macaca fascicularis fascicularis north and south of the Isthmus of Kra. Int J Primatol 29:1271–1294CrossRef
    Hayashi S, Kawamoto Y (2006) Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island. Primates 47:158–164CrossRef
    Hou J, Schindler U, Henzel WJ, Ho TC, Brasseur M, McKnight SL (1994) An interleukin-4-induced transcription factor: IL-4 Stat. Science 265:1701–1706PubMed CrossRef
    Jadejaroen J, Hamada Y, Kawamoto Y, Malaivijitnond S (2015) Use of photogrammetry as a means to assess the hybrid between rhesus (Macaca mulatta) and long-tailed macaques (M. fascicularis). Primates 56:77–88PubMed CrossRef
    Kanthaswamy S, Satkoski J, George D, Erickson BJ-A, Smith DG (2008) Hybridization and stratification of nuclear genetic variation in Macaca mulatta and M. fascicularis. Int J Primatol 29:1295–1311PubMed PubMedCentral CrossRef
    Kanthaswamy S, Satkoski J, Kou A, Malladi V, Smith DG (2010) Detecting signatures of inter-regional and inter-specific hybridization among the Chinese rhesus macaque specific pathogen-free (SPF) population using single nucleotide polymorphic (SNP) markers. J Med Primatol 39:252–265PubMed PubMedCentral CrossRef
    Kawamoto Y, Ishida T, Suzuki J, Takenaka O, Varavudhi P (1989) A preliminary report on the genetic variation of crab-eating macaques in Thailand. Kyoto Univ Overseas Res Rep Stud Asian Non Human Primates 7:94–103
    Kawamoto Y, Takemoto H, Higuchi S, Sakamaki T, Hart JA, Hart TB, Tokuyama N, Reinartz GE, Guislain P, Dupain J, Cobden AK, Mulavwa MN, Yangozene K, Darroze S, Devos C, Furuichi T (2013) Genetic structure of wild bonobo populations: diversity of mitochondrial DNA and geographical distribution. PLoS ONE 8:e59660PubMed PubMedCentral CrossRef
    Ling F, Wei L-Q, 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 63:155–166PubMed CrossRef
    Malaivijitnond S, Hamada Y (2008) Current situation and status of long-tailed macaques (Macaca fascicularis) in Thailand. Nat Hist J Chulalongkorn Univ 8:185–204
    Malaivijitnond S, Sae-Low W, Hamada Y (2008) The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand. J Med Primatol 37:31–37PubMed
    Malaivijitnond S, Vazquez Y, Hamada Y (2011) Human impact on long-tailed macaques in Thailand. In: Jones-Engel L, Michael G, Augustin F (eds) Managing commensalism in long-tailed macaques. Cambridge University Press, Cambridge, pp 118–158
    Malhi RS, Satkoski Trask J, Shattuck M, Johnson J, Chakraborty D, Kanthaswamy S, Ramakrishnan U, Smith DG (2011) Genotyping single nucleotide polymorphisms (SNPs) across species in old world monkeys. Am J Primatol 73:1031–1040PubMed
    Melnick DJ, Hoelzer GA (1992) Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. Int J Primatol 13:379–393CrossRef
    Osada N, Uno Y, Mineta K, Kameoka Y, Takahashi I, Terao K (2010) Ancient genome-wide admixture beyond the current hybrid zone between Macaca fascicularis and M. mulatta. Mol Ecol 19:2884–2895PubMed CrossRef
    Primate Research Institute, Kyoto University Guideline for field research for non-human primates. http://​www.​pri.​kyoto-u.​ac.​jp/​research/​guide-e2008.​html . Accessed 1 Dec 2014
    Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
    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. Tiss Antigens 67:297–306CrossRef
    Satkoski Trask JA, Garnica WT, Smith DG, Houghton P, Lerche N, Kanthaswamy S (2013) Single-nucleotide polymorphisms reveal patterns of allele sharing across the species boundary between rhesus (Macaca mulatta) and cynomolgus (M. fascicularis) macaques. Am J Primatol 75:135–144PubMed PubMedCentral CrossRef
    Stevison LS, Kohn MH (2009) Divergence population genetic analysis of hybridization between rhesus and cynomolgus macaques. Mol Ecol 18:2457–2475PubMed CrossRef
    Tosi AJ, Morales JC, Melnick DJ (2002) Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. Int J Primatol 23:161–178CrossRef
    Tosi AJ, Morales JC, Melnick DJ (2003) Paternal, maternal, and biparenteral molecular markers provide unique windows onto the evolutionary of macaque monkeys. Evolution 57:1419–1435PubMed CrossRef
    Weinbauer GF, Niehoff M, Niehaus M, Srivastav S, Fuchs A, Van Esch E, Cline JM (2008) Physiology and endocrinology of the ovarian cycle in macaques. Toxicol Pathol 36:7S–23SPubMed PubMedCentral CrossRef
    Yan G, Zhang G, Fang X, Zhang Y, Li C, Ling F et al (2011) Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nat Biotechnol 29:1019–1023PubMed CrossRef
    Zhang B-W, Li M, Ma L-C, Wei F-W (2006) A widely applicable protocol for DNA isolation from fecal samples. Biochem Genet 44:503–512PubMed
  • 作者单位:Janya Jadejaroen (1)
    Yoshi Kawamoto (2)
    Yuzuru Hamada (3)
    Suchinda Malaivijitnond (1) (4)

    1. Zoological Science Program, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand
    2. Genome Diversity Section, Department of Evolution and Phylogeny, Primate Research Institute, Kyoto University, Kyoto, Japan
    3. Evolutionary Morphology Section, Department of Evolution and Phylogeny, Primate Research Institute, Kyoto University, Kyoto, Japan
    4. National Primate Research Center of Thailand, Chulalongkorn University, Saraburi, Thailand
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Life Sciences
    Zoology
    Animal Ecology
    Behavioural Sciences
    Evolutionary Biology
  • 出版者:Springer Japan
  • ISSN:1610-7365
文摘
A polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) assay was developed to genetically discriminate rhesus (Macaca mulatta) macaques from long-tailed (M. fascicularis) macaques. The 745 bp PCR amplicon of the STAT6 locus that spans a potentially species-diagnostic single nucleotide polymorphism (SNP) marker was digested with ApaI and gel electrophoresed to give (1) two (234 and 511 bp), (2) one (745 bp) and (3) three (234, 511 and 745 bp) band patterns that correspond to the genotypes G/G (long-tailed macaque specific homozygote), A/A (rhesus macaque specific homozygote) and A/G (hybrid specific heterozygote), respectively. The diagnostic robustness and efficiency of this PCR–RFLP assay was tested on wild rhesus and long-tailed macaques inhabiting Thailand and a known hybrid population. The Indochinese and Sundaic long-tailed macaque samples (n = 18) all showed a homozygous G/G pattern, while the Indochinese rhesus macaques (n = 10) all showed a homozygous A/A pattern. The rhesus/long-tailed hybrid population at Khao Khieow Open Zoo, which resulted from an introduced group of rhesus macaques that hybridized with the indigenous long-tailed macaques about 20 years ago, revealed 47 % (56/118 samples analyzed) with the heterogenous A/G genotype. In addition, the frequency of the rhesus-specific allele A significantly decreased in the hybrid population during 2006–2014, where a strong association between the STAT6 genotype and the morphology of the individuals was detected. In conclusion, a robust PCR–RFLP assay allows a simple, effective and inexpensive approach, in particular for field studies, to assess hybrid individuals between rhesus and long-tailed macaques. Although this assay cannot conclusively identify all the hybrids over two or more generations, it at least can allow the evaluation of the process of hybridization, and so it is applicable to the assessment of the status of natural or anthropogenic hybridization between the two species across their geographic range. Keywords STAT6 PCR–RFLP ApaI Macaca fascicularis M. mulatta Hybridization

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700