Skip to main content
SpringerLink
Log in

Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation

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

Abstract

Male macaques typically leave their natal group before sexual maturity, while females remain for life. Thus genes flow between groups and populations almost solely through male transfer. This asymmetrical dispersal pattern, affects the distribution of variation in the nuclear and mitochondrial genomes differently Nuclear genetic variation, measured by allozyme polymorphisms, is relatively evenly distributed throughout the populations of a macaque species, provided there are no major geographical barriers. Conversely the distribution of maternally inherited mitochondrial DNA (mtDNA) diversity is characterized by local homogeneity and large interpopulational differences. Because of differences in inheritance, dispersal, and population structure, the information contained in nuclear and mitochondrial genomes is best used to address different types of behavioral, genetic, and conservation questions.

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

Access this article

Log in via an institution

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

  • Ashley, M. V., Melnick, D. J., and Western, D. (1989). Conservation genetics of the black rhinoceros (Diceros bicornis). I. Evidence from the mitochondrial DNA of three populations.Conserv. Biol. 4: 71–77.

    Article  Google Scholar 

  • Avise, J. C. (1986). Mitochondrial DNA and the evolutionary genetics of higher animals.Phil. Trans. R. soc. Lond. 312: 325–342.

    CAS  Google Scholar 

  • Avise, J. C. (1989). A role for molecular genetics in the recognition and conservation of endangered species. TREE 4: 279–281.

    Google Scholar 

  • Avise, J. C., Neigel, J. E., and Arnold, J. (1984). Demographic influences on mitochondrial DNA lineage, survivorship in animal populations.J. Mol. Evol. 20: 99–105.

    Article  PubMed  CAS  Google Scholar 

  • Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A., and Saunders N. C. (1987). Intraspecific phylogeography: The mitochondrial bridge between population, genetics and systematics.Annu. Rev. Ecol. Syst. 18: 489–522.

    Google Scholar 

  • Brown, W. M. (1983). Evolution of animal, mitochondrial DNA. In Nei, M., and Koehn, R. K. (eds),Evolution of Genes and Proteins, Sinauer Press, Sunderland, MA, pp. 62–88.

    Google Scholar 

  • Brown, W. M., George, M., and Wilson, A. C. (1979). Rapid evolution of animal mitochondrial DNA.Proc. Natl. Acad. Sci. USA 76: 1967–1971.

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock, T. H. (1989). Female transfer and inbreeding avoidance in social mammals.Nature 337: 70–72.

    Article  PubMed  CAS  Google Scholar 

  • Darga, L. L. (1975).Immunological and Electrophoretic Investigations of Catarrhine Evolution, Ph.D. thesis, Wayne State University, Detroit, MI.

    Google Scholar 

  • Dittus, W. P. J., (1975). Population dynamics of the toque monkey,Macaca sinica. In Tuttle, R. H. (ed.),Socioecology and Psychology of Primates, Mouton, The Hague, pp. 125–151.

    Google Scholar 

  • Dowling, T. E., Moritz, C., and Palmer, J. D. (1990). Nucleic acids II: Restriction site analysis. In Hillis, D., and Moritz, C. (eds.),Molecular Systematics, Sinauer Press, Sunderland, MA, pp. 250–317.

    Google Scholar 

  • Ehrlich, P. R., and Raven, P. H. (1969). Differentiation of populations.Science 165: 1228–1232.

    Article  PubMed  CAS  Google Scholar 

  • Fooden, J. (1988). Taxonomy and evolution of theSinica group of macaques. 6. Interspecific comparisons and synthesis.Field. Zool. 45: 1–44.

    Google Scholar 

  • Greenwood, P. J. (1980). Mating systems, philopatry, and dispersal in birds and mammals.Anim. Behav. 28: 1140–1162.

    Article  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 inMacaca fascicularis.Primates 29: 117–127.

    Article  CAS  Google Scholar 

  • Hayasaka, K., Horai, S., Gojobori, T., Shotake, T. Nozawa, K. and Matsunaga E. (1988), Phylogenetic relationships among Japanese, rhesus, Formosan, and crab-eating monkeys, inferred from restriction-enzyme analysis of mitochondrial DNAs.Mol. Biol. Evol. 5:270–281.

    PubMed  CAS  Google Scholar 

  • Hoelzer, G. A., Wallman, J., and Melnick, D. J. (1991a). The effects of social and geographic structure on the evolutionary dynamics of mitochondrial DNA (unpublished manuscript).

  • Hoelzer, G. A., Ashley, M. V., Dittus, W. P. J., and Melnick D. J. (1991b). Mitochondrial DNA variation and the matenal phylogeny of toque monkey social groups in Polonnaruwa, Sri Lanka (unpublished manuscript).

  • Honeycutt, R., and Wheeler, W. (1989). Mitochondrial DNA: Variation in humans and primates, In Dutta S. K., and Winter, W. (eds).DNA Systematics: Human and Higher Primates, CRC Press, Boca Raton, FL.

    Google Scholar 

  • Lindburg, D. G. (1969). Rhesus monkeys: Mating season mobility of adult males.Science 166: 1176–1178.

    Article  Google Scholar 

  • Melnick, D. J. (1988). The genetic structure of a primate species: Rhesus macaques, and other cercopithecine monkeys.Int. J. Primatol. 9: 195–231.

    Google Scholar 

  • Melnick, D. J., Jolly, C. J., and Kidd, K. K. (1984a). The genetics of a wild population of rhesus monkeys (Macaca mulatta). I. Genetic variability within and between social groups.Am. J. Phys. Anthropol. 63: 341–360.

    Article  Google Scholar 

  • Melnick, D. J., Pearl, M. C., and Richard, A. F. (1984b). Male migration and inbreeding avoidance in wild rhesus monkeys.Am. J. Primatol. 7: 229–243.

    Article  Google Scholar 

  • Melnick, D. J., Jolly, C. J., and Kidd, K. K., (1986). The genetics of a wild population of rhesus monkeys (Macaca mulatta) II. The Dunga Gali population in species-wide perspective.Am. J. Phys. Anthropol. 71: 129–140.

    Article  PubMed  CAS  Google Scholar 

  • Melnick, D. J., Hoelzer, G. A., Absher, R., and Ashley, M. V. (1991a). mtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species (unpublished manuscript).

  • Melnick, D. J., Goldstein, S. J., and Gale, L. C. (1991b). Matrilineal group structure, genetic heterogeneity, and the rapid evolution of nonhuman primates (unpublished manuscript).

  • Melnick, D. J., Hoelzer, G. A., and Honeycutt, R. (1992) The mitochondrial genome: Its uses in anthropological research. In Devor, E. (ed.),Molecular Applications in Biological Anthropology, Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Moore, J. (1984). Female transfer in primates.Int. J. Primatol. 5:537–589.

    Google Scholar 

  • Moore, J., and Ali, R. (1984). Are dispersal and inbreeding related.Anim. Behav., 32: 94–112.

    Article  Google Scholar 

  • Napier, J. R., and Napier, P. H. (1967).A Handbook of Living Primates, Academic Press, London.

    Google Scholar 

  • Nei, M. (1973). Analysis of gene diversity in subdivided populations.Proc. Natl. Acad. Sci. USA 70: 3321–3323.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M. (1982). Evolution of human races at the gene level. In Bonne-Tamir, B., Cohen, P., and Goodman, R. N. (eds),Human Genetics, Part A: The Unfolding Genome, A. R. Liss Press, New York, pp. 167–181.

    Google Scholar 

  • Nei, M., and Tajima, F. (1983). Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data.Genetics 105: 207–217.

    PubMed  CAS  Google Scholar 

  • Nozawa, K., Shotake, T., Okhura, Y., and Tanabe, Y. (1977). Genetic variations within and between species of Asian macaques.Jap. J. Genet. 52: 15–30.

    Google Scholar 

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

  • Richard, A. R., Goldstein, S. J., and Dewar, R. E. (1990). Weed macaques: The evolutionary implications of macaque feeding ecology.Int. J. Primatol. 10: 569–594.

    Google Scholar 

  • Sade, D. S. (1972). A longitudinal study of social behavior of rhesus monkeys. In Tuttle, R. H. (ed.),The Functional and Evolutionary Biology of Primates, Aldine Press, Chicago, pp. 378–398.

    Google Scholar 

  • Shotake, T. (1979). Serum albumin and erythrocyte adenosine deaminase polymorphisms in Asian macaques with special reference to taxonomic relationships amongM. assamensis, M. radiata, andM. mulatta.Primates 20: 443–451.

    Article  CAS  Google Scholar 

  • Williams, A. K., Ashley, M. V., Tenaza, R., and Melnick, D. J. (1991). Extreme mtDNA sequence divergence in pigtail monkeys (unpublished manuscript).

  • Wilson A. C., Cann, R. L., Carr, S. M., George, M., Gyllensten, U. B., Helm-Bychowski, K. M., Higuchi, R. F., Palumbi, S. R., Prager, E. M., Sage, R. D., and Stoneking, M. (1985). Mitochondrial DNA and two perspectives on evolutionary genetics.Biol. J. Linn. Soc. 26: 375–400.

    Google Scholar 

  • Wolfheim, J. H. (1983).Primates of the World, University of Washington Press, Seattle.

    Google Scholar 

  • Wright, S. (1943). Isolation by distance.Genetics 28: 114–138.

    Google Scholar 

  • Wright, S. (1951). The genetical structure of populations.Annu. Eugen. 15: 323–354.

    Google Scholar 

Download references

Author information

Author notes

  1. Guy A. Hoelzer

    Present address: Department of Biology and Department of Range, Wildlife and Forestry, University of Nevada Reno, 89557, Reno, Nevada

Authors and Affiliations

  1. Genetics Laboratory, Department of Anthropology, Columbia University, 10027, New York, New York

    Don J. Melnick & Guy A. Hoelzer

Authors
  1. Don J. Melnick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guy A. Hoelzer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Melnick, D.J., Hoelzer, G.A. Differences in male and female macaque dispersal lead to contrasting distributions of nuclear and mitochondrial DNA variation. International Journal of Primatology 13, 379–393 (1992). https://doi.org/10.1007/BF02547824

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02547824

Keywords

Search

Navigation