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.
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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.
Avise, J. C. (1986). Mitochondrial DNA and the evolutionary genetics of higher animals.Phil. Trans. R. soc. Lond. 312: 325–342.
Avise, J. C. (1989). A role for molecular genetics in the recognition and conservation of endangered species. TREE 4: 279–281.
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.
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.
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.
Brown, W. M., George, M., and Wilson, A. C. (1979). Rapid evolution of animal mitochondrial DNA.Proc. Natl. Acad. Sci. USA 76: 1967–1971.
Clutton-Brock, T. H. (1989). Female transfer and inbreeding avoidance in social mammals.Nature 337: 70–72.
Darga, L. L. (1975).Immunological and Electrophoretic Investigations of Catarrhine Evolution, Ph.D. thesis, Wayne State University, Detroit, MI.
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.
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.
Ehrlich, P. R., and Raven, P. H. (1969). Differentiation of populations.Science 165: 1228–1232.
Fooden, J. (1988). Taxonomy and evolution of theSinica group of macaques. 6. Interspecific comparisons and synthesis.Field. Zool. 45: 1–44.
Greenwood, P. J. (1980). Mating systems, philopatry, and dispersal in birds and mammals.Anim. Behav. 28: 1140–1162.
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.
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.
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.
Lindburg, D. G. (1969). Rhesus monkeys: Mating season mobility of adult males.Science 166: 1176–1178.
Melnick, D. J. (1988). The genetic structure of a primate species: Rhesus macaques, and other cercopithecine monkeys.Int. J. Primatol. 9: 195–231.
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.
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.
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.
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.
Moore, J. (1984). Female transfer in primates.Int. J. Primatol. 5:537–589.
Moore, J., and Ali, R. (1984). Are dispersal and inbreeding related.Anim. Behav., 32: 94–112.
Napier, J. R., and Napier, P. H. (1967).A Handbook of Living Primates, Academic Press, London.
Nei, M. (1973). Analysis of gene diversity in subdivided populations.Proc. Natl. Acad. Sci. USA 70: 3321–3323.
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.
Nei, M., and Tajima, F. (1983). Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data.Genetics 105: 207–217.
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.
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.
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.
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.
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.
Wolfheim, J. H. (1983).Primates of the World, University of Washington Press, Seattle.
Wright, S. (1943). Isolation by distance.Genetics 28: 114–138.
Wright, S. (1951). The genetical structure of populations.Annu. Eugen. 15: 323–354.
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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
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DOI: https://doi.org/10.1007/BF02547824