Skip to main content
Log in

Y-Chromosome and Mitochondrial Markers in Macaca fascicularis Indicate Introgression with Indochinese M. mulatta and a Biogeographic Barrier in the Isthmus of Kra

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

This is the first report of Y-chromosome introgression between primate species. We sequenced 3.1 Kb of Y-chromosome DNA and 1.5 Kb of mtDNA for 27 macaques of Fooden's (Folia Primatol. [1976] 25: 225–236) fascicularis species group and 5 outgroup taxa (Macaca sylvanus, Papio hamadryas, Theropithecus gelada, Allenopithecus nigroviridis, and Cercopithecus mona). Phylogenies constructed separately for the paternal and maternal data sets show a Y-chromosome paraphyly among lineages of Macacafascicularis, but a mitochondrial monophyly for the same individuals. The Y-chromosome topology depicts Indochinese Macaca fascicularis haplotypes joining with those of M. mulatta, followed by M. cyclopis and M. fuscata, before clustering with a clade of lineages of M. fascicularis from peninsular Malaysia, Indonesia, and the Philippines. These contrasting patterns of mitochondrial and Y-chromosome DNA, evaluated in the context of the evolutionary consequences of macaque sex-biased dispersal, present strong evidence for contemporary hybridization between Macaca fascicularis and M. mulatta in Indochina and a biogeographic barrier in the Isthmus of Kra.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Affara, N., Bishop, C., Brown, W., Cooke, H., Davey, P., Ellis, N., Graves, J. M., Jones, M., Mitchell, M., Rappold, G., Tyler-Smith, C., Yen, P., and Lau, Y.-F. C. (1996). Report of the second international workshop on Y chromosome mapping 1995. Cytogenet. Cell. Genet. 73: 33–76.

    Google Scholar 

  • Bradley, D.G., Loftus, R.T., Cunningham, P., and MacHugh, D. E. (1998). Genetics and domestic cattle origins. Evol. Anthropol. 6: 79–86.

    Google Scholar 

  • Brown, W. M., Prager, E. M., Wang, A., and Wilson, A.C. (1982). Mitochondrial DNA sequences of primates: Tempo and mode of evolution. J. Mol. Evol. 18: 225–239.

    Google Scholar 

  • Corbet, G. B., and Hill, J. E. (1992). The Mammals of the Indomalayan Region: A Systematic Review, Oxford University Press, Oxford.

    Google Scholar 

  • Darga, L. L., Goodman, M., Weiss, M., Moore, G. W., Prychodko, W., Dene, H., Tashian, R., and Koen, A. (1975). Molecular systematics and clinal variation in macaques. In Market, C. L. (ed.), Isozymes IV: Genetics and Evolution, Academic Press, New York, pp. 797–812.

    Google Scholar 

  • Disotell, T. R. (1999). Sex-specific contributions to genome variation. Curr. Biol. 9: R29–R31.

    Google Scholar 

  • Dutrillaux, B., Couturier, J., Muleris, M., Lombard, M., and Chauvier, G. (1982). Chromosomal phylogeny of forty-two species or subspecies of cercopithecoids (Primates: Catarrhini). Ann. Genet. 25: 96–109.

    Google Scholar 

  • Fooden, J. (1964). Rhesus and crab-eating macaques: Intergradation in Thailand. Science 143: 363–365.

    Google Scholar 

  • Fooden, J. (1975). Taxonomy and evolution of liontail and pigtail macaques (Primates: Cercopithecidae). Fieldiana Zool. 67: 1–169.

    Google Scholar 

  • Fooden, J. (1976). Provisional classification and key to living species of macaques (Primates: Macaca). Folia Primatol. 25: 225–236.

    Google Scholar 

  • Fooden, J. (1980). Classification and distribution of living macaques. In Lindburg, D. G. (ed.), The Macaques: Studies in Ecology, Behavior, and Evolution, Van Nostrand Reinhold Co., New York, pp. 1–9.

    Google Scholar 

  • Fooden, J. (1995). Systematic review of southeast Asian longtail macaques, Macaca fascicularis (Raffles, 1821). Fieldiana Zool. 81: 1–206.

    Google Scholar 

  • Fooden, J. (1997). Tail length variation in Macaca fascicularis and M. mulatta. Primates 38(3): 221–231.

    Google Scholar 

  • Fooden, J., and Albrecht, G. H. (1999). Tail-length evolution in fascicularis-group macaques (Cercopithecidae: Macaca). Int. J. Primatol. 20(3): 431–440.

    Google Scholar 

  • Glaser, B., Grutzner, F., Willman, U., Stanyon, R., Arnold, N., Taylor, K., Rietschel, W., Zeitler, S., Toder, R., and Schempp, W. (1998). SimianYchromosomes: Species-specific rearrangements of DAZ, RBM, and TSPY versus contiguity of PAR and SRY. Mamm. Genome. 9: 226–231.

    Google Scholar 

  • Harihara, S., Saitou, N., Hirai, M., Aoto, N., Terao, K., Cho, F., Honjo, S., and Omoto, K. (1988). Differentiation of mitochondrial DNA types in Macaca fascicularis. Primates 29(1): 117–127.

    Google Scholar 

  • Hartl, D. L., and Clark, A. G. (1997). Principles of Population Genetics, 3rd edn, Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Hayasaka, K., Fujii, K., and Horai, S. (1996). Molecular phylogeny of macaques: Implications of nucleotide sequences from an 896 base pair region of mitochondrial DNA. Mol. Biol. Evol. 13(7): 1044–1053.

    Google Scholar 

  • Hoelzer, G.A. (1997). Inferring phylogenies from mtDNAvariation: Mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51(2): 622–626.

    Google Scholar 

  • Hoelzer, G. A., and Melnick, D. J. (1994). Patterns of speciation and limits to phylogenetic resolution. Trends Ecol. Evol. 9(3): 104–107.

    Google Scholar 

  • Hoelzer, G. A., Wallman, J., and Melnick, D. J. (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.

    Google Scholar 

  • Jobling, M. A., and Tyler-Smith, C. (1995). Fathers and sons: The Y chromosome and human evolution. Trends Genet. 11(11): 449–456.

    Google Scholar 

  • Keane, B., Dittus, W. P. J., and Melnick, D. J. (1997). Paternity assessment in wild groups of toque macaques Macaca sinica at Polonnaruwa, Sri Lanka using molecular markers. Mol. Ecol. 6: 267–282.

    Google Scholar 

  • Keng, H. (1970). Size and affinities of the flora of the Malay peninsula. J. Trop. Geog. 31: 43–56.

    Google Scholar 

  • Kim, H. S., Hirai, H., and Takenaka, O. (1996). Molecular features of the TSPY gene of gibbons and Old World monkeys. Chrom. Res. 4: 500–506.

    Google Scholar 

  • Kim, H. S., and Takenaka, O. (1996).Acomparison of TSPY genes from Y-chromosomal DNA of the great apes and humans: Sequence, Evolution, and Phylogeny. Am.J. Phys. Anthropol. 100: 301–309.

    Google Scholar 

  • Melnick, D. J. (1987). The genetic consequences of primate social organization: A review of macaques, baboons, and vervet monkeys. Genetica 73: 117–135.

    Google Scholar 

  • Melnick, D. J., and Hoelzer, G.A. (1992). Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. Int. J. Primatol. 13: 379–393.

    Google Scholar 

  • Melnick, D. J., Hoelzer, G. A., Absher, R., and Ashley, M. V. (1993). mtDNAdiversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol. Biol. Evol. 10: 282–295.

    Google Scholar 

  • Melnick, D. J., and Kidd, K. K. (1985). Genetic and evolutionary relationships among Asian macaques. Int. J. Primatol. 6: 123–160.

    Google Scholar 

  • Moore, W. S. (1995). Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nuclear-gene trees. Evolution 49(4): 718–726.

    Google Scholar 

  • Morales, J. C., and Melnick, D. J. (1998). Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. J. Hum. Evol. 34: 1–23.

    Google Scholar 

  • Pusey, A. E., and Packer, C. (1987). Dispersal and philopatry. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R.W., and Struhsaker, T.T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 250–266.

    Google Scholar 

  • Roldan, E. R. S., and Gomendio, M. (1999). The Y chromosome as a battle ground for sexual selection. Trends Ecol. Evol. 14(2): 58–62.

    Google Scholar 

  • Springer, M. S., and Douzery, E. (1996). Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. J. Mol. Evol. 43: 357–373.

    Google Scholar 

  • Swofford, D. L. (1999). PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0b2, Illinois Natural History Survey, Champaign.

  • Tosi, A. J., Morales, J. C., and Melnick, D. J. (2000). Comparison ofY-chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Mol. Phyl. Evol. 17(2):133–144.

    Google Scholar 

  • Wright, S. (1931). Evolution in Mendelian populations. Genetics 16: 97–159.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tosi, A.J., Morales, J.C. & Melnick, D.J. 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 (2002). https://doi.org/10.1023/A:1013258109954

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1013258109954

Navigation