Mitochondrial DNA hypervariable region-1 sequence variation and phylogeny of the concolor gibbons, Nomascus

American Journal of Primatology

Volumn 69, Issue 11, 2007, Pages 1285-1306

  Monda, Keri ^a,b   Simmons, Rachel E ^a,c   Kressirer, Philipp ^a,d   Su, Bing ^a,e   Woodruff, David S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b IL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^e KUNMING INSTITUTE OF ZOOLOGY   (China)

Author keywords

Control region; Hylobatidae; Molecular evolution; Noninvasive genotyping; Species; Taxonomy

Indexed keywords

MITOCHONDRIAL DNA;

EVOLUTION; GENOTYPE; MITOCHONDRIAL DNA; PHYLOGENY; PHYLOGEOGRAPHY; PRIMATE; TAXONOMY;

ANIMAL; ARTICLE; CHEMISTRY; COMPLEMENTARITY DETERMINING REGION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HAPLORHINI; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT;

ANIMALS; BASE SEQUENCE; COMPLEMENTARITY DETERMINING REGIONS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENOTYPE; HYLOBATES; PHYLOGENY; SEQUENCE ALIGNMENT; VARIATION (GENETICS);

ASIA; CAMBODIA; CHINA; EURASIA; EUROPE; FAR EAST; LAOS; MYANMAR; NORTH AMERICA; SOUTHEAST ASIA; VIET NAM;

ANIMALIA; HAPLORHINI; HYLOBATES LAR; HYLOBATIDAE; NOMASCUS; NOMASCUS LEUCOGENYS;

EID: 35648974834     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20439     Document Type: Article

References (101)

1. Anderson S, Bankier AT, Barrell BG, de Bruijin MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG. 1981. Sequence and organization of the human mitochondrial genome. Nature 290:457-465.
2. Arnold ML, Meyer A. 2006. Natural hybridization in primates: one evolutionary mechanism. Zoology 109:261-276.
3. Arnold N, Stanyon R, Jauch A, O'Brien P, Weinberg J. 1996. Identification of complex chromosome rearrangements in the gibbon by fluorescent in situ hybridization (FISH) of a human chromosome 2q specific microlibrary, yeast artificial chromosomes, and reciprocal chromosome painting. Cytogenet Cell Genet 74:80-85.
4. Baker LR, Geissmann T, Nadler T, Long B, Walston J. 2002. Cambodia: Primate field guide. Phnom Penh, Cambodia: Fauna & Flora Cambodia. 8 p.
5. Bandelt H-J, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37-48.
6. Bartlett TQ. 2005. The hylobatidae. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK, editors. Primates in perspective. New York: Oxford University Press. p 274-289.
7. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM. 2001. Mitochondrial pseudogenes: evolution's misplaced witnesses. TREE 16:314-321.
8. Bigoni F, Stanyon R. 2006. Hylobates concolor. In: O'Brien SJ, Menninger JC, Nash WG, editors. Atlas of mammalian chromosomes. Hoboken, NJ: Wiley. p 160.
9. Bleisch WV, Jiang X. 2000. Action plan for conservation of the gibbons of the Wuliang Mountains. Sino-Dutch Forest Conservation and Community Development Project, Kunming, Yunnan, China.
10. Bleisch W, Zhang Y. 2004. The view across the border: China and the future of Vietnamese primates. In: Nadler T, Streicher U, Ha Thang L, editors. Conservation of primates in Vietnam. Hanoi: Frankfurt Zool Soc, Vietnam Primate Conserv Progr, Cue Phuong National Park, Endangered Primate Rescue Center. p 107-114.
11. Brandon-Jones D, Eudey AA, Geissmann T, Groves CP, Melnick DJ, Morales JC, Shekelle M, Stewart CB. 2004. Asian primate classification. Int J Primatol 25:97-164.
12. Brockelman WY, Schilling D. 1984. Inheritance of stereotyped gibbon songs. Nature 312:634-636.
13. Carbone L, Vessere GM, Hallers BFH, Zhu B, Osoegawa K, Mootnick M, Kofler A, Wienberg J, Rogers J, Humphray S, Scott C, Harris RA, Milosavljevic A, de Jong PA. 2006. A high-resolution map of synteny disruptions in gibbon and human genomes. PLoS Genet 2:2162-2175.
14. Chambers KE, Reichard UH, Moller A, Nowak K, Vigilant L. 2004. Cross-species amplification of human microsatellite markers using noninvasive samples from white-handed gibbons (Hylobates lar). Am J Primatol 64:19-27.
15. Chan BPL, Fellowes JR, Geissmann T, Zhang J, editors. 2005. Status survey and conservation action plan for the Hainan gibbon - version I (last updated November 2005). Hong Kong: Kadoorie Farm & Botanic Garden Technical Report 3. p 1-33.
16. Chatterjee HJ. 2006. Phylogeny and biogeography of gibbons: a dispersal-vicariance analysis. Int J Primatol 27:699-712.
17. Chivers DJ. 2005. Gibbons: the small apes. In: Caldecott J, Miles L, editors. World atlas of great apes and their conservation. Berkeley: University of California Press. p 205-214.
18. Clement M, Posada D, Crandall KA. 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657-1659.
19. Corbet GB, Hill JE. 1992. The mammals of the Indomalayan Region: a systematic review. Oxford: British Museum (Natural History) & Oxford University Press.
20. Couturier J, Lernould JM. 1991. Karyotypic study of four gibbon forms provisionally considered as subspecies of Hylobates (Nomascus) concolor (Primates, Hylobatidae). Folia Primatol 56:95-104.
21. Couturier J, Dutrillaux B, Turleau C, De-Grouchy J. 1992. Comparative karyotyping of four gibbon species or subspecies. Ann Genet 25:5-10.
22. Dao VT. 1983. On the north Indochinese gibbons (Hylobates concolor) (Primates: Hylobatidae) in North Vietnam. J Hum Evol 12:367-372.
23. DiFiore A, Gagneux P. 2006. Molecular primatology. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK, editors. Primates in perspective. New York: Oxford University Press. p 369-393.
24. Fooden J. 1996. Zoogeography of Vietnamese primates. Int J Primatol 67:845-899.
25. Fooden J, Quan G, Luo Y. 1987. Gibbon distribution in China. Acta Theriol Sin 7:161-167.
26. Garza JC, Woodruff DS. 1992. A phylogenetic study of the gibbons (Hylobates) using DNA obtained noninvasively from hair. Mol Phylogen Evol 1:202-210.
27. Garza JC, Woodruff DS. 1994. Crested gibbon (Hylobates [Nomascus]) identification using noninvasively obtained DNA. Zoo Biol 13:383-387.
28. Geissmann T. 1989. A female black gibbon, Hylobates concolor subspecies, from north-eastern Vietnam. With appendix: a note on the Laotian black gibbon, H. concolor lu. Int J Primatol 10:455-476.
29. Geissmann T. 1993. Evolution of communication in gibbons (Hylobatidae). Ph.D. dissertation. Zurich University, Switzerland.
30. Geissmann T. 1995. Gibbon systematics and species identification. Int Zoo News 42:65-77.
31. Geissmann T. 1997. New sounds from the crested gibbons (Hylobates concolor group): first results of a systematic revision. In: Zissler D, editor. Verhandlungen der Deutschen Zoologischen Gesellschaft: Kurzpublikationen, 90. Jahresversammlung, Gustav Fischer, Stuttgart. p 170.
32. Geissmann T. 2002. Taxonomy and evolution of gibbons. Evol Anthropol 11(Suppl 1):28-31.
33. Geissmann T. 2005a. Der Hainan-Schopfgibbon: Der bedrohteste Menschenaffe der Welt. Gibbon J 1:10-12.
34. Geissmann T. 2005b. Auf der Suche nach den letzten Gibbons von Hainan. Gibbon J 1:18-22.
35. Geissmann T. 2006a. Gibbon research lab. Available from: http://www.gibbons.de
36. Geissmann T. 2006b. Schutz des Hainan-Schopfgibbons, des seltensten Menschenaffen der Welt: ein Projektbericht. Gibbon J 2:11-13.
37. Geissmann T, Lim KKP. 1994. Extraction of bacula from tanned gibbon skins. Raffles Bull Zool 42:29-41.
38. Geissmann T, Nijman V. 2006. Calling in wild silvery gibbons (Hylobates moloch) in Java (Indonesia): behavior, phylogeny, and conservation. Am J Primatol 68:1-19.
39. Geissmann T, Nguyen Xuan D, Lormée N, Momberg F. 2000. Vietnam primate conservation status review 2000. Part 1: Gibbons. Hanoi: Fauna & Flora International, Indochina Programme. 139p.
40. Geissmann T, La Quang T, Trinh Dinh H, Vu Dinh T, Dang Ngoc C, Pham Duc T. 2003. Rarest ape species rediscovered in Vietnam. Asian Primates 8(3-4):8-9.
41. Geissmann T, Traber S, von Allmen A. 2006. Das Nangunhe-Naturreservat, Provinz Yunnan, China: Ein Projektbericht [Nangunhe Nature Reserve, Yunnan Province, China: a project report]. Gibbon J 2:14-17.
42. Groves CP. 1972. Systematics and phylogeny of gibbons. In: Rumbaugh, DM, editor. Gibbon and siamang, vol. 1. Basel: Karger. p 1-89.
43. Groves CP. 1993. Speciation in living hominoid primates. In: Kimbel WH, Martin LB, editors. Species, species concepts, and primate evolution. New York: Plenum. p 109-121.
44. Groves CP. 2001. Primate taxonomy. Washington, DC: Smithsonian Institution Press.
45. Groves CP. 2004. Taxonomy and biogeography of primates in Vietnam and neighbouring regions. In: Nadler T, Streicher U, Ha Thang Long, editors. Conservation of primates in Vietnam. Hanoi: Frankfurt Zool Soc, Vietnam Primate Conservation Programme, Cue Phuong National Park, Endangered Primate Rescue Center. p 15-22.
46. Groves CP, Wang Y. 1990. The gibbons of the subgenus Nomascus (Primates, Mammalia). Zool Res 11:148-154.
47. Hall LM, Jones D, Wood B. 1998. Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. Mol Phylogen Evol 10:281-286.
48. Hirai H, Wijayanto H, Tanaka H, Mootnick AR, Hayano A, Perwitasari-Farajallah D, Iskandriati D, Sajuthi D. 2005. A whole-arm translocation (WAT8/9) separating agile gibbons and its evolutionary features. Chromosome Res 13:123-133.
49. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
50. IUCN. 2006. IUCN Red list of threatened species. Available from: http://www.iucnredlist.org.
51. Jauch A, Weinberg J, Stanyon R, Arnold N, Tofanelli S, Ishida T, Cremer T. 1992. Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci USA 89:8611-8615.
52. Jiang XL, Wang YX. 1999. Population and distribution of black-crested gibbons (Nomascus concolor jingdongensis) in Wuliang Nature Reserve, Jingdong, Yunnan. Zool Res 20:421-425.
53. King M. 1993. Species evolution: the role of chromosome change. Cambridge: Cambridge University Press.
54. Koehler U, Bigoni F, Weinberg J, Stanyon R. 1995. Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30:287-292.
55. Konrad R, Geissmann T. 2006. The vocal diversity and taxonomy of crested gibbons (genus Nomascus) in Cambodia. Int J Primatol 27:713-745.
56. Konstant WR, Mittermeier RA, Rylands AB, Butynski TM, Eudey AA, Ganzhorn J, Kormos R. 2003. The world's top 25 most endangered primates. Asian Primates 8:29-34.
57. Kressirer P. 1993. Eine Molekulare Phylogenie der Gibbons (Hylobatidae). Munchen: Diplomarbeit der Fakultat fur Biologie der Ludwig-Maximilians-Universitat.
58. Ma S, Wang Y. 1986. The taxonomy and distribution of gibbons in southern China and its adjacent region, with description of three new subspecies. Zool Res 7:393-410.
59. Ma S, Wang Y, Poirier FE. 1988. Taxonomy, distribution, and status of gibbons (Hylobates) in southern China and adjacent areas. Primates 29:277-286.
60. Marshall J, Sugardjito J. 1986. Gibbon systematics. In: Swindler DR, Erwin J, editors. Comparative primate biology, vol. 1: systematics, evolution and anatomy. New York: Liss. p 137-185.
61. Monda K. 1995. A phylogenetic study of the gibbons (Hylobates) using the control region of the mitochondrial genome. San Diego: Master's thesis, University of California.
62. Mootnick AR. 2006. Gibbon (Hylobatidae) species identification recommended for rescue or breeding centers. Primate Conserv 21:103-138.
63. Mootnick AR, Groves CP. 2005. A new generic name for the hoolock gibbon (Hylobatidae). Int J Primatol 26:971-976.
64. Morin PA, Goldberg TL. 2003. Determination of genealogical relationships from genetic data: a review of methods and applications. In: Chapais B, Berman CM, editors. Kinship and behavior in primates. Oxford: Oxford University Press. p 15-45.
65. Mueller S, Hollatz M, Weinberg J. 2003. Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum Genet 113:493-501.
66. Nadler T, Streicher U. 2004. The primates of Vietnam - an overview. In: Nadler T, Streicher U, Ha Thang L, editors. Conservation of primates in Vietnam. Hanoi: Frankfurt Zool Soc, Vietnam Primate Conservation Programme, Cuc Phuong National Park, Endangered Primate Rescue Center. p 5-11.
67. Nie W, Rens W, Wang J, Yang F. 2001. Conserved chromosome segments in Hylobates hoolook revealed by human and H. leucogenys paint probes. Cytogenet Cell Genet 92:248-253.
68. Polzin T, Daneschmand SV. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12-20.
69. Prouty LA, Buchanan PD, Pollitzer WS, Mootnick AR. 1983a. Bunopithecus: a genus-level taxon for the hoolock gibbon (Hylobates hoolock). Am J Primatol 5:83-87.
70. Prouty LA, Buchanan PD, Pollitzer WS, Mootnick AR. 1983b. A presumptive new hylobatid subgenus with 38 chromosomes. Cytogen Cell Genet 35:141-142.
71. Roos C. 2003. Molekulare Phylogenie der Halbaffen, Schlankaffen und Gibbons. PhD thesis. Germany: Technical Univ Munich.
72. Roos C. 2004. Molecular evolution and systematics of Vietnamese primates. In: Nadler T, Streicher U, Ha Thang L, editors. Conservation of primates in Vietnam. Hanoi: Frankfurt Zool Soc, Vietnam Primate Conservation Programme, Endangered Primate Rescue Center, Cue Phuong National Park. p 23-28.
73. Roos C, Geissmann T. 2001. Molecular phylogeny of the major hylobatid divisions. Mol Phylogen Evol 19:486-494.
74. Rosenblum LL, Supriatna J, Melnick DJ. 1997. Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA. Amer J Phys Anthro 104:35-45.
75. Sheeran, LK, Zhang Y, Poirier FE, Yang D. 1998. Preliminary report on the behavior of the Jingdong black gibbon (Hylobates concolor furvogaster). Trop Biodiv 5:113-125.
76. Simmons RE. 2005. A phylogenetic study of the gibbons (Hylobatidae). Master's thesis. San Diego: University of California.
77. Simmons RE, Monda K, Woodruff DS. Phylogenetics of gibbons (Hylobatidae): mitochondrial and nuclear DNA sequence data resolve long-standing questions. in prep.
78. Sterling EJ, Hurley MM, Minh LD. 2006. Vietnam: a natural history. New Haven: Yale University Press.
79. Su B, Kressirer P, Wang W, Jiang X, Wang YX, Woodruff DS, Monda K, Zhang YP. 1996. Molecular phylogeny of Chinese N. c. concolor gibbons. Sci China (C) 26:414-419.
80. Swofford DL. 1998. Phylogenetic analysis using parsimony and other methods (PAUP* Version 4.0b). Sunderland, MA: Sinauer.
81. Takacs Z, Morales JC, Geissmann T, Melnick DJ. 2005. A complete species-level phylogeny of the Hylobatidae based on mitochondrial ND3-ND4 gene sequences. Mol Phylogen Evol 36:456-467.
82. Tanaka H, Wijayanto H, Mootnick AR, Iskandriati D, Perwitasari-Farajallah D, Sajuthi D, Hirai H. 2004. Molecular phylogenetic analyses of subspecific relationships in agile gibbons (Hylobates agilis) using mitochondrial and TSPY gene sequences. Folia Primatol 75(Suppl 1):418.
83. Thalmann O, Hebler J, Poinar HN, Paabo S, Vigilant L. 2004. Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol Ecol 13:321-335.
84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882.
85. Trung LQ, Hoang TD. 2004. Status review of the Cao Vit black-crested gibbon (Nomascus nasutus nasutus) in Vietnam. In: Nadler T, Streicher U, Ha Thang L, editors. Conservation of primates in Vietnam. Hanoi: Frankfurt Zool Soc, Vietnam Primate Conservation Progr. Cuc Phuong National Park, Endangered Primate Rescue Center. p 90-94.
86. van Gulik RH. 1967. The gibbon in China. An essay in Chinese animal lore. Leiden: Brill.
87. Wagele J-W. 2005. Foundations of phylogenetic systematics. Munich: Pfeil.
88. Wang Y. 2003. A complete checklist of mammal species and subspecies in China - a taxonomic and geographic reference. Beijing: China Forestry Publishing House. 394p.
89. Warren KS, Verschoor EJ, Langenhuijzen S, Swan RA, Vigilant L, Heeney JL. 2001. Speciation and intrasubspecific variation in Bornean orangutans, Pongo pygmaeus pygmaeus. Mol Biol Evol 18:472-480.
90. White MJD. 1978. Modes of speciation. San Francisco: Freeman.
91. Whittaker DJ. 2005. Evolutionary genetics of Kloss's gibbons (Hylobates klossii): systematics, phylogeography, and conservation. Ph.D. thesis. The City University of New York. 201p.
92. Woodruff DS. 1990. Genetics and demography in the conservation of biodiversity. J Sci Soc Thailand 16:117-132.
93. Woodruff DS. 1993. Non-invasive genotyping of primates. Primates 34:333-346.
94. Woodruff DS. 2003. Noninvasive genotyping and field studies of free-ranging nonhuman primates. In: Chapais B, Berman CM, editors. Kinship and behavior in primates. Oxford: Oxford University Press. p 46-68.
95. Woodruff DS, Monda K, Simmons RE. 2005. Mitochondrial DNA sequence variation and subspecific taxonomy in the white-handed gibbon, Hylobates lar. Nat Hist J Chulalongkorn Univ 1:71-78.
96. Zehr SM. 1999. A nuclear and mitochondrial phylogeny of the lesser apes (Primates, genus Hylobates). Ph.D. thesis. Harvard University. 221p.
97. Zhang Y. 1992. Hainan gibbon (Hylobates concolor hainanus) threatened. Asian Primates 2:6.
98. Zhang Y, Sheeran L. 1994. Current status of the Hainan black gibbon (Hylobates concolor hainanus). Asian Primates 3:3.
99. Zhang YP. 1997. Mitochondrial DNA sequence evolution and phylogenetic relationships of gibbons. Acta Genet Sin 24:231-237.
100. Zhang YW, Luo HR, Ryder OA, Zhang YP. 2004. Evolution of the tandem repeats in thymidylate synthase enhancer region (TSER) in primates. Gene 338:47-54.
101. Zhou J, Wei F, Li M, Zhang J, Wang D, Pan R. 2005. Hainan black-crested gibbon is headed for extinction. Int J Primatol 26:453-465.