Diversification of sulawesi macaque monkeys: Decoupled evolution of mitochondrial and autosomal DNA

Evolution

Volumn 57, Issue 8, 2003, Pages 1931-1946

  Evans, Ben J ^a,b   Supriatna, Jatna ^c,d   Andayani, Noviar ^c   Melnick, Don J ^a  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF INDONESIA   (Indonesia)

^d Conservation International Indonesia ^*  (Indonesia)

Author keywords

Microsatellites; Philopatry; Phylogeny; Population genetics; Southeast Asia

Indexed keywords

EVOLUTION; GENE FLOW; PHILOPATRY; PRIMATE;

INDONESIA; SULAWESI;

ANIMALIA; MACACA; MAMMALIA; PRIMATES;

EID: 0041783471     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00599.x     Document Type: Article

References (76)

1. Abegg, C., and B. Thierry. 2002. Macaque evolution and dispersal in insular south-east Asia. Biol. J. Linn. Soc. 75:555-576.
2. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Autom. Contr. 19:716-723.
3. Albrecht, G. H. 1978. The craniofacial morphology of the Sulawesi macaques, multivariate approaches to biological problems. Pp. 1-151 in F. S. Szalay, ed. Contributions to primatology. Karger, Basel, Switzerland.
4. Avise, J. C., and R. M. Ball. 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Oxf. Surv. Evol. Biol. 7:45-67.
5. Bergman, S. C., D. Q. Coffield, J. P. Talbot, and R. A. Garrard. 1996. Tertiary tectonic and magmatic evolution of western Sulawesi and the Makassar Strait: evidence for a Miocene continent-continent collision. Pp. 391-429 in R. Hall and D. Blundell, eds. Tectonic evolution of Southeast Asia. Geological Society, London.
6. Bernstein, I., and T. Gordon. 1980. Mixed taxa introductions, hybrids, and macaque systematics. Pp. 125-147 in D. G. Lindburg, ed. The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold Co., New York.
7. Birky, C. W. 1991. Evolution and population genetics of organelle genes: mechanisms and models. Pp. 112-134 in R. K. Selander, A. G. Clark, and T. S. Whittam, eds. Evolution at the molecular level. Sinauer, Sunderland, MA.
8. Buttikofer, J. 1917. Die kurzschwanz affen von celebes. Zool. Meded. (Leiden) 3:1-86.
9. Bynum, E. L., D. Z. Bynum, and J. Supriama. 1997. Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in Central Sulawesi, Indonesia. Am. J. Primatol. 43:181-209.
10. Bynum, E. L., A. K. Kohlhass, and A. H. Pramono. 1999. Conservation status of Sulawesi macaques. Trop. Biodiv. 6:123-144.
11. Chesser, R. K., and R. J. Baker. 1996. Effective sizes and dynamics of uniparentally and diparentally inherited genes. Genetics 144:1225-1235.
12. Ciani, A., R. Stanton, W. Scheffrahn, and B. Sampurno. 1989. Evidence of gene flow between Sulawesi macaques. Am. J. Primatol. 17:257-270.
13. Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:257-270.
14. de Ruiter, J. R., W. Scheffrahn, G. J. J. M. Trommelen, A. G. Uitterlinden, R. D. Martin, and J. A. R. A. M. Van Hoof. 1992. Male social rank and reproductive success in wild long-tailed macaques. Pp. 175-191 in R. D. Martin, A. F. Dixon, and E. J. Wickings, eds. Paternity in primates: genetic tests and theories. Karger, Basel, Switzerland.
15. Deinard, A., and D. Glen Smith. 2001. Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. J. Hum. Evol. 41:45-59.
16. Delson, E. 1980. Fossil macaques, phyletic relationships and a scenario of development. Pp. 10-30 in D. G. Lindburg, ed. The macaques: studies in ecology, behavior, and evolution. Van Nostrand Reinhold, New York.
17. Dittus, W. 1975. Population dynamics of the toque macaque, Macaca sinica. Pp. 125-152 in R. H. Turtle, ed. Socioecology and psychology of primates. Mounton, The Hague, The Netherlands.
18. Evans, B. J., J. C. Morales, J. Supriatna, and D. J. Melnick. 1999. Origin of the Sulawesi macaques (Cercopithecidae, Macaca) as inferred from a mitochondrial DNA phylogeny. Biol. J. Linn. Soc. 66:539-560.
19. Evans, B. J., J. Supriatna, and D. J. Melnick. 2001. Hybridization and population genetics of two macaque species in Sulawesi, Indonesia. Evolution 55:1686-1702.
20. Evans, B. J., J. Supriatna, N. Andayani, M. I. Setiadi, D. C. Cannatella, and D. J. Melnick. 2003. Monkeys and toads define areas of endemism on Sulawesi. Evolution 57:1436-1443.
21. Evans, B. J., R. M. Brown, J. A. McGuire, J. Supriatna, N. Andayani, A. Diesmos, D. T. Iskandar, D. J. Melnick, and D. C. Cannatella. 2003. Phylogenetics of fanged frogs (Anura; Ranidae; Limnonectes): testing biogeographical hypotheses at the Asian-Australian faunal zone interface. Syst. Biol. In press.
22. Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479-491.
23. Fooden, J. 1969. Taxonomy and evolution of the monkeys of Celebes (Primates: Cercopithecidae). S. Karger, Basel, Switzerland.
24. _. 1975. Taxonomy and evolution of liontail and pigtail macaques (Primates: Cercopithecidae). Fieldiana Zool. 67:1-169.
25. _. 1976. Provisional classification and key to the living species of macaques (Primates: Macaca). Folia Primatol. 25:225-236.
26. Gaggiotti, O. E., O. Lange, K. Rassman, and C. Gliddon. 1999. A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol. Ecol. 8:1513-1520.
27. Goldman, N. 1993. Statistical tests of models of DNA substitution. J. Mol. Evol. 36:182-198.
28. Goldman, N., J. P. Anderson, and A. G. Rodrigo. 2000. Likelihood-based tests of topologies in phylogenetics. Syst. Biol. 49:652-670.
29. Groves, C. P. 1980. Speciation in Macaca: the view from Sulawesi. Pp. 84-124 in D. G. Lindburg, ed. The macaques: studies in ecology, behavior, and evolution. Van Nostrand Reinhold Co., New York.
30. Hall, R. 1996. Reconstructing Cenozoic SE Asia. Pp. 153-184 in R. Hall and D. Blundell, eds. Tectonic evolution of Southeast Asia. Geological Society of London Special Publication no. 106.
31. _. 1998. The plate tectonics of Cenozoic SE Asia and the distribution of land and sea. Pp. 99-131 in R. Hall and D. J. Holloway, eds. Biogeography and geological evolution of Southeast Asia. Backhuys Publishers, Leiden, The Netherlands.
32. _. 2001. Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. Pp. 35-56 in I. Metcalfe, J. Smith, M. Morwood, and I. Davidson, eds. Faunal and floral migrations and evolution in SE Asia-Australia. Swets and Zeitlinger Publishers, Lisse, The Netherlands.
33. Heaney, L. R. 1986. Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction, and speciation. Biol. J. Linn. Soc. 28:127-165.
34. Hillis, D. M., B. K. Mable, and C. Moritz. 1996. Applications of molecular systematics: the state of the field and a look to the future. Pp. 515-543 in D. M. Hillis, C. Moritz, and B. K. Mable, eds. Molecular systematics. Sinauer, Sunderland, MA.
35. Hoelzer, G. A. 1997. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51:622-626.
36. Hoelzer, G. A., W. Dittus, M. V. Ashley, and D. J. Melnick. 1994. The local distribution of highly divergent mitochondrial DNA haplotypes in toque macaques (Macaca sinica) at Polonnaruwa, Sri Lanka. Mol. Ecol. 3:451-458.
37. Hoelzer, G. A., J. Wallman, and D. J. Melnick. 1998. The effects of social structure, geographical structure, and population size on the evolution of mitochondrial DNA: II. Molecular clocks and the lineage sorting period. J. Mol. Evol. 47:21-31.
38. Huelsenbeck, J. P., D. M. Hillis, and R. Jones. 1996. Parametric bootstrapping in molecular phylogenetics: applications and performance. Pp. 19-45 in J. D. Ferraris and S. R. Palumbi, eds. Molecular zoology: advances, strategies, and protocols. Wiley-Liss, New York.
39. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-123 in H. N. Munro, ed. Mammalian protein metabolism. Academic Press, New York.
40. Kloss, C. B. 1929. The zoo-geographical boundaries between Asian and Australia and some oriental sub-regions. Bull. Raffles Mus. 2:1-10.
41. Knowles, L. L., and W. P. Maddison. 2002. Statistical phylogeography. Mol. Ecol. 11:2623-2635.
42. McGuire, J. A. 2002. Bayesian phylogenetics and biogeography of the Dracolineatus group. P. 212 in Program book and abstracts of the joint meeting of ichythologists and herpetologists, 3-8 July, Kansas City, KS.
43. Melnick, D. J. 1988. The genetic structure of a primate species: rhesus and other cercopithecine monkeys. Int. J. Primatol. 9:195-231.
44. Melnick, D. J., and G. A. Hoelzer. 1992. Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. Int. J. Primatol. 13:379-393.
45. Melnick, D. J., and M. C. Pearl. 1987. Cercopithecines in multimale groups: genetic diversity and population structure. Pp. 121-134 in D. L. C. B. B. Smuts, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, ed. Primate societies. Univ. of Chicago Press, Chicago, IL.
46. Melnick, D. J., G. A. Hoelzer, R. Absher, and M. V. Ashley. 1993. MtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol. Biol. Evol. 10:282-295.
47. Neigel, J. E., and J. C. Avise. 1986. Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. Pp. 515-534 in E. Nevo and S. Karlin, eds. Evolutionary processes and theory. Academic Press, New York.
48. Palumbi, S. R., and F. Cipriano. 1998. Species identification using genetic tools: the value of nuclear and mitochondrial gene sequences in whale conservation. J. Hered. 89:459-464.
49. Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
50. Posada, D., K. A. Crandall, and A. R. Templeton. 2000. Geodis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9:487-488.
51. Rambaut, A, and N. C. Grassly. 1997. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput. Appl. Biosci. 13:235-238.
52. Raymond, M., and F. Rousset. 1995. Genepop program, version 3.1b: a population genetics software for exact tests and ecumenicism. J. Hered. 86:248-249.
53. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
54. Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequin: A software for population genetics data analysis. University of Geneva, Geneva.
55. Shekelle, M., S. M. Leksono, L. L. S. Ichwan, and Y. Masala. 1997. The natural history of the tarsiers of North and Central Sulawesi. Sulawesi Primate Newsletter 4:3-8.
56. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
57. Swofford, D. L. 2002. Phylogenetic analysis using parsimony (* and other methods). Ver. 4. Sinauer, Sunderland, MA.
58. Swofford, D., G. J. Olsen, P. J. Waddell, and D. M. Hillis. 1996. Phylogenetic inference. Pp. 407-514 in D. M. Hillis, C. Moritz, and B. K. Mable, eds. Molecular systematics. 2d ed. Sinauer, Sunderland, MA.
59. Takenaka, O., M. Hotta, B. Suryoboto, and E. Brotoisworo. 1987. Origin and evolution of the Sulawesi macaques. Complete amino acid sequences of seven B chains of three molecular types. Primates 28:99-109.
60. Templeton, A. R. 1998. Nested clade analysis of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7:381-397.
61. _. 2002. Out of Africa again and again. Nature 416:45-51.
62. Templeton, A. R., and C. F. Sing. 1993. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analysis with cladogram uncertainty and recombination. Genetics 134:659-669.
63. Templeton, A. R., E. Boerwinkle, and C. F. Sing. 1987. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343-351.
64. Templeton, A. R., K. A. Crandall, and C. F. Sing. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619-633.
65. Tosi, A. J., J. C. Morales, and D. J. Melnick. 2000. Comparison of Y-chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Mol. Phylogenct. Evol. 17:133-144.
66. Tosi, A. J., J. C. Morales, and D. J. Melnick. 2002. Macaca fascicularis Y-chromosome and mitochondrial markers indicate introgression with Indochinese M. mulatta and a biogeographic barrier in the Isthmus of Kra. Int. J. Primatol. 23:161-178.
67. Tosi, A. J., J. C. Morales, and D. M. Melnick. 2003. Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution. 57:1419-1435.
68. Van Noordwijk, M. A., and C. P. Van Schaik. 2002. Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138:359-395.
69. Voris, H. 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeog. 27:1153-1167.
70. Watanabe, K., and S. Matsumura. 1991. The borderlands and possible hybrids between three species of macaques, M. nigra, M. nigrescens, and M. hecki, in the northern peninsula of Sulawesi. Primates 32:365-369.
71. Watanabe, K., S. Matsumura, T. Watanabe, and Y. Hamada. 1991a. Distribution and possible intergradation between Macaca tonkeana and M. ochreata at the borderland of the species in Sulawesi. Primates 32:385-389.
72. Watanabe, K., K. Lapasere, and R. Tantu. 1991b. External characteristics and associated developmental changes in two species of Sulawesi macaques, Macaca tonkeana and M. hecki, with special reference to hybrids and the borderland between the species. Primates 32:61-76.
73. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
74. Whitten, T., G. S. Henderson, and M. Mustafa. 2002. The ecology of Sulawesi. Periplus Editions Ltd., Hong Kong.
75. Wright, S. 1931. Evolution in Mendelian populations. Genetics 28:114-138.
76. _. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395-420.