Hybridization and stratification of nuclear genetic variation in Macaca mulatta and M. fascicularis

International Journal of Primatology

Volumn 29, Issue 5, 2008, Pages 1295-1311

  Kanthaswamy, Sree ^a,b   Satkoski, Jessica ^a   George, Debra ^a   Kou, Alexander ^a   Erickson, Bethany Joy Alise ^a   Smith, David Glenn ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gene flow; Genetic structure; Hybridization; Introgression; Microsatellites

Indexed keywords

ALLELE; CAPTIVITY; COMPARATIVE STUDY; FOUNDER EFFECT; GENE FLOW; GENETIC DIFFERENTIATION; GENETIC DRIFT; GENETIC MARKER; GENETIC STRUCTURE; HYBRIDIZATION; INTROGRESSION; ISOLATED POPULATION; PRIMATE;

ASIA; EURASIA;

MACACA; MACACA FASCICULARIS; MACACA MULATTA;

EID: 54449097114     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-008-9295-0     Document Type: Article

References (69)

1. C. Abegg B. Thierry 2002 Macaque evolution and dispersal in insular south-east Asia Biological Journal of the Linnean Society. Linnean Society of London 75 555 576
2. R. R. Ackermann J. Rogers J. M. Cheverud 2006 Identifying the morphological signatures of hybridization in primate and human evolution Journal of Human Evolution 51 632 645
3. Allendorf, F. W. (1983). Isolation, gene flow and genetic differentiation among populations. In C. M. Shonewald-Cox, S. M. Chambers, B. MacBryde, & L. Thomas (Eds.), Genetics and Conservation (pp. 51-65). London: Benjamin-Cummings.
4. M. C. R. Andrade M. C. T. Penedo T. Ward V. F. Silva L. R. Bertolini J. A. Roberts 2004 Determination of genetic status in a closed colony of rhesus monkeys (Macaca mulatta) Primates 45 183 186
5. M. Bonhomme A. Blancher S. Cuarteros L. Chikhi B. Crouau-Roy 2008 Origin and number of founders in an introduced insular primate: Estimation from nuclear genetic data Molecular Ecology 17 1009 1019
6. E. L. Bynum D. Z. Bynum J. Supriatna 1997 Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in Central Sulawesi, Indonesia American Journal of Primatology 43 181 209
7. J. Cohen 2000 Vaccine studies stymied by shortage of animals Science 287 959 960
8. Delson, E. (1980). Fossil macaques, phyletic relationships and a scenario of deployment. In D. G. Lindburg (Ed.), The Macaques: Studies in ecology, behavior, and evolution (pp. 10-30). New York: Van Nostrand-Reinhold.
9. G. G. M. Doxiadis N. Otting N. G. de Groot N. de Groot A. J. M. Rouweler R. Noort E. J. Vershoor I. Bontjer R. E. Bontrop 2003 Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations Immunogenetics 55 540 551
10. G. G. M. Doxiadis A. J. M. Rouweler N. G. de Groot A. Louwerse N. Otting E. J. Verschoor 2006 Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques Immunogenetics 58 259 268
11. B. J. Evans J. Supriatna D. J. Melnick 2001 Hybridization and population genetics of two macaque species in Sulawesi, Indonesia Evolution; International Journal of Organic Evolution 55 1685 1702
12. B. Ferguson S. I. Street H. Wright C. Pearson Y. Jia S. L. Thompson 2007 Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta) BMC Genomics 8 43
13. Fittinghoff Jr, N. A., & Lindburg, D. G. (1980). Riverine refuging in east Bornean Macaca fascicularis. In D. G. Lindburg (Ed.), The Macaques: Studies in ecology, behavior and evolution. New York: Van Nostrand Reinhold.
14. J. Fooden 1964 Rhesus and crab-eating macaques: integradation in Thailand Science 143 363 364
15. J. Fooden 1976 Primates obtained in peninsular Thailand June-July, 1973, with notes on the distribution of continental Southeast Asian leaf-monkeys (Presbytis) Primates 17 95 118
16. J. Fooden 1995 Systematic review of Southeast Asian longtail macaques, Macaca fascicularis (Raffles 1821) Fieldiana Zoology 81 1 206
17. J. Fooden 1997 Tail length variation in Macaca fascicularis and M. mulatta Primates 38 221 232
18. Fooden, J. (2000). Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Field Museum of Natural History, Chicago.
19. J. Froehlich J. Supriatna Y. Muskita 1996 Biodiversity and the conservation biology of Macaca nigra: An anthropological view Tropical Biodiversity 3 85 102
20. Groves, C. P. (2001). Primate Taxonomy. Washington, DC: Smithsonian Institution Press.
21. Y. Hamada H. Ohsawa N. Urasopon S. Malaivijitnond 2004 Preliminary report on the distribution and status of macaques in Thailand Primate Report 20 97 108
22. Y. Hamada N. Urasopon I. Hadi S. Malaivijitnond 2006 Body size, proportions and pelage color of free-ranging rhesus macaques (Macaca mulatta) from a zone of hybridization in northern Thailand International Journal of Primatology 27 497 513
23. K. Hayasaka K. Fujii S. Horai 1996 Molecular phylogeny of macaques: implications of nucleotide sequences from a 896-base pair region of mitochondrial DNA Molecular Biology and Evolution 13 1044 1053
24. R. D. Hernandez M. J. Hubisz D. Wheeler D. G. Smith B. Ferguson J. Rogers 2007 Demographic histories and patterns of linkage disequilibrium for Chinese and Indian rhesus macaques Science 316 240 243
25. S. V. Joag E. B. Stephens R. J. Adams L. Foresman O. Narayan 1994 Pathogenesis of SIVmac infection in Chinese and Indian rhesus macaques: Effects of splenectomy on virus burden Virology 200 436 446
26. Jombart, T. (2008). adegenet: An R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford, England), submitted.
27. Kanthaswamy, S., Gill, L., Satkoski, J., Goyal, V., Malladi, V., Kou, A., et al. The development of a Chinese-Indian hybrid (Chindian) rhesus macaque colony at the California National Primate Research Center (CNPRC) by introgression. Journal of Medical Primatology, in press.
28. S. Kanthaswamy D. G. Smith 1998 Use of microsatellite polymorphisms for paternity exclusion in rhesus macaque (Macaca mulatta) Primates 39 135 145
29. S. Kanthaswamy D. G. Smith 2004 Effects of geographic origins on captive Macaca mulatta mtDNA variation Journal of Comparative Medicine 54 166 174
30. S. Kanthaswamy A. Von Dollen J. D. Kurushima O. Alminas J. Rogers B. Ferguson 2006 Microsatellite markers for standardized genetic management of captive colonies of rhesus macaques (Macaca mulatta) American Journal of Primatology 68 73 95
31. Y. Kawamoto T. M. Ischak J. Supriatna 1984 Genetic variations within and between troops of the crab-eating macaque (Macaca fascicularis) on Sumatra, Java, Bali, Lombok and Sumbawa, Indonesia Primates 25 131 159
32. Y. Kawamoto S. Kawamoto K. Matsubayashi K. Nozawa T. Watanabe M. A. Stanley 2008 Genetic diversity of longtail macaques (Macaca fascicularis) on the island of Mauritius: An assessment of nuclear and mitochondrial DNA polymorphisms Journal of Medical Primatology 37 45 54
33. K. C. Krebs Z. Jin R. Rudersdorf A. L. Hughes D. H. O'Connor 2005 Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques Journal of Immunology (Baltimore, MD.: 1950) 175 5230 5239
34. R. Kyes L. Jones-Engel M. K. Chalise G. Engel J. Heidrich R. Grant 2006 Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal American Journal of Primatology 68 445 455
35. B. Ling R. S. Veazey A. Luckay C. Penedo K. Xu J. D. Lifson 2002 SIVmac pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans AIDS (London, England) 16 1489 1496
36. S. Malaivijitnond S. -L. Wattana H. Yuzuru 2008 The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand Journal of Medical Primatology 37 31 37
37. R. S. Malhi B. Sickler D. Lin J. Satkoski D. George S. Kanthaswamy 2007 MamuSNP: A SNP resource for Rhesus macaques (Macaca mulatta) PLoS ONE 2 5 e438
38. J. Marmi J. Bertranpetit J. Terradas O. Takenaka X. Domingo-Roura 2004 Radiation and phylogeography in the Japanese macaque, Macaca fuscata Molecular Phylogenetics and Evolution 30 676 685
39. D. J. Melnick G. A. Hoelzer R. Absher M. V. Ashley 1993 mtDNA diversity in rhesus monkey reveals overestimates of divergence time and paraphyly with neighboring species Molecular Biology and Evolution 10 282 295
40. J. C. Morales D. J. Melnick 1998 Phylogenetic relationships of the macaques (Cercopithecidae: Macaca) as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes Journal of Human Evolution 34 1 23
41. P. A. Morin S. Kanthaswamy D. G. Smith 1997 Simple sequence repeat, SSR, polymorphisms for colony management and population genetics in rhesus macaques (Macaca mulatta) American Journal of Primatology 42 199 213
42. Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press: New York.
43. M. C. T. Penedo R. E. Bontrop C. M. C. Heijmans N. Offing R. Noort A. J. M. Rouweler 2005 Microsatellite typing of the rhesus macaque MHC region Immunogenetics 57 198 209
44. J. K. Pritchard M. Stephens P. Donnelly 2000 Inference of population structure using multilocus genotype data Genetics 155 945 959
45. M. Raymond F. Rousset 1995 GENEPOP: Population genetics software for exact tests and ecumenicism The Journal of Heredity 86 248 249
46. Satkoski, J., George, D., Smith, D. G., & Kanthaswamy, S. (2007). Genetic characterization of wild and captive rhesus macaques in China. Journal of Medical Primatology. www.blackwell-synergy.com/doi/abs/10.1111/j.1600-0684. 2007.00228.x.
47. M. Slatkin 1981 Estimating levels of gene flow in natural populations Genetics 99 323 335
48. M. Slatkin 1985 Gene flow in natural populations Annual Review of Ecology and Systematics 16 393 430
49. M. Slatkin N. H. Barton 1989 A comparison of three indirect methods for estimating the average level of gene flow Evolution; International Journal of Organic Evolution 43 1349 1368
50. D. G. Smith J. McDonough 2005 Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta) American Journal of Primatology 65 1 25
51. D. G. Smith D. George S. Kanthaswamy J. McDonough 2006 Identification of country of origin and admixture between Indian and Chinese rhesus macaques International Journal of Primatology 27 881 898
52. D. G. Smith J. W. McDonough D. A. George 2007 Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques American Journal of Primatology 69 182 189
53. S. L. Street R. C. Kyes R. Grant B. Ferguson 2007 Single nucleotide polymorphisms (SNPs) are highly conserved in rhesus (Macaca mulatta) and cynomolgus (Macaca fascicularis) macaques BMC Genomics 8 480
54. J. Supriatna J. W. Froehlich J. Erwin C. Southwick 1992 Population, habitat and conservation status of Macaca maurus, Macaca tonkeana and their putative hybrids Tropical Biodiversity 1 31 48
55. R. W. Sussman I. Tattersall 1981 Behavior and ecology of Macaca fascicularis in Mauritius: A preliminary study Primates 22 192 205
56. R. W. Sussman I. Tattersall 1986 Distribution, abundance, and putative ecological strategy of Macaca fascicularis on the island of Mauritius, southwestern Indian Ocean Folia Primatologica 46 28 43
57. A. J. Tosi C. S. Coke 2007 Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques Molecular Phylogenetics and Evolution 42 498 504
58. A. J. Tosi J. C. Morales D. J. Melnick 2000 Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history Molecular Phylogenetics and Evolution 17 133 144
59. A. J. Tosi J. C. Morales D. J. Melnick 2002 Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra International Journal of Primatology 23 161 178
60. A. J. Tosi J. C. Morales D. J. Melnick 2003 Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys Evolution; International Journal of Organic Evolution 57 1419 1435
61. J. Viray B. Rolfs D. G. Smith 2001 Comparison of the frequencies of major histocompatibility (MHC) class-II DQA1 and DQB1 alleles in Indian and Chinese rhesus macaques (Macaca mulatta) Comparative Medicine 51 555 561
62. Weir, B. S. (1996). Genetic Data Analysis II. MA: Sinauer, Sunderland.
63. B. S. Weir C. C. Cockerham 1984 Estimating F-statistics for the analysis of population structure Evolution; International Journal of Organic Evolution 38 1358 1370
64. R. W. Wiseman J. A. Wojcechowskyj J. M. Greene A. J. Blasky T. Gopon T. Soma 2007 Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius Journal of Virology 81 349 361
65. P. G. Wolf P. S. Soltis 1992 Estimates of gene flow among populations, geographic races, and species in the Ipomopsis aggregata complex (Polemoniaceae) Genetics 130 639 647
66. S. Wright 1951 The genetical structure of populations Annals of Eugenics 15 323 354
67. Wright, S. (1978). In Evolution and the Genetics of Populations, Vol. 4. University of Chicago Press, Chicago, pp. 79-90.
68. F. C. Yeh T. J. B. Boyle 1997 Population genetic analysis of co-dominant and dominant markers and quantitative traits Belgian Journal of Botany 129 157
69. Y. P. Zhang L. Shi 1993 Phylogeny of rhesus monkeys (Macaca mulatta) as revealed by mitochondrial DNA restriction enzyme analysis International Journal of Primatology 14 587 605