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Phylogenetic relationships among the galaginae as indicated by erythrocytic allozymes

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Abstract

At least four hypotheses regarding the phylogenetic relationships within the Galaginae have been proposed, based on features of karyology, morphology, and behaviour, but these hypotheses share few common elements. Here we investigate erythrocytic allozymes as potential phylogenetic markers, and subject our results to a cladistic analysis. Our study offers little support for the previous models, but suggests instead that the greater galagos andG. alleni form a clade since they share character states for eight of the ten systems examined. The two lesser galago species could not be distinguished using these enzymes, and character states common to them and theallenicrassicaudatus-garnettii clade were found in only four systems. Our resultant cladogram accords well with the rather scant galagine fossil record. The data also show strong concordance with results obtained using highly repeated DNA sequences, which indicate that the galagos form a close-knit genetic group, while the Malagasy lemurids show considerably more inter-taxic variation.

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References

  • Arnaud, J., B. Meier, J. M. Dugoujon, &Y. Rumpler, 1992. Study of the variability of erythrocyte enzymes in captive and wild populations of the black lemur (Eulemur macaco macaco): an indispensable preliminary in captive breeding programmes.Primates, 33: 139–146.

    Article  Google Scholar 

  • Barnicot, N. A. &D. Hewett-Emmett, 1974. Electrophoretic studies on prosimian blood proteins. In:Prosimian Biology,R. D. Martin,G. A. Doyle, &A. C. Walker (eds.), Duckworth, London, pp. 891–902.

    Google Scholar 

  • ————,C. Jolly, E. R. Huehns, &J. Moor-Jankowski, 1964. A carbonic anhydrase variant in the baboon.Nature, 202: 198–199.

    CAS  PubMed  Google Scholar 

  • Barroso, C. M. L., M. P. C. Schneider, M. I. C. Sampaio, &F. M. Salzano, 1990. Esterase D in BrazilianSaguinus midas niger — results and comparison with previous studies in Anthropoidea.Amer. J. Primatol., 22: 215–219.

    Article  Google Scholar 

  • Buettner-Janusch, J. &V. Buettner-Janusch, 1963. Haemoglobins ofGalago crassicaudatus.Nature, 197: 1018–1019.

    CAS  PubMed  Google Scholar 

  • ———— & ————, 1964. Hemoglobins of Primates. In:Evolutionary and Genetic Biology of Primates,J. Buettner-Janusch (ed.), Academic Press, New York, pp. 75–90.

    Google Scholar 

  • ———— & ————, & D. Coppenhaver, 1972. Properties of the hemoglobins of newborn and adult prosimians (Prosimii: Lemuriformes and Lorisiformes).Folia Primatol., 17: 177–192.

    CAS  PubMed  Google Scholar 

  • ————,L. Dame, G. A. Mason, &D. S. Sade, 1974. Primate red cell enzymes: glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase.Amer. J. Phys. Anthropol., 41: 7–14.

    CAS  Google Scholar 

  • ———— &R. C. Wiggins, 1970. Haptoglobins and acid phosphatases ofGalago, Folia Primatol., 13: 166–176.

    CAS  PubMed  Google Scholar 

  • Charles-Dominique, P., 1971. Eco-éthologie des prosimiens du Gabon.Biol. Gabonica, 7: 121–228.

    Google Scholar 

  • Coppenhaver, D. H., J. Buettner-Janusch, M. M. Ehrhardt, &L. K. Duffy, 1986. Prosimian hemoglobins: III. The primary structures of the duplicated α-globin chains ofLemur variegatus.Biochem. Biophys. Acta, 873: 372–378.

    CAS  PubMed  Google Scholar 

  • Crovella, S., J. C. Masters, &Y. Rumpler, 1994. Highly repeated DNA sequences as phylogenetic markers among the Galaginae.Amer. J. Primatol., 32: 177–185.

    Article  CAS  Google Scholar 

  • de Boer, L. E. M., 1973. Cytotaxonomy of the Lorisoidea (Primates:Prosimii): I. Chromosome studies and karyological relationships in the Galagidae.Genetica, 44: 155–193.

    Google Scholar 

  • Duffy, L. K., M. M. Ehrhardt, J. Buettner-Janusch, &D. H. Coppenhaver, 1987. Prosimian hemoglobins: IV. The structural difference responsible for the hemoglobin phenotype ofLemur catta.Amer. J. Primatol., 13: 187–193.

    Article  CAS  Google Scholar 

  • Dugoujon, J. M., J. Arnaud, F. Loirat, S. Hazout, &J. Constans, 1989. Blood markers and genetic evolution in Cercopithecinae.Primates, 30: 403–422.

    Article  Google Scholar 

  • Dutrillaux, B., 1979. Chromosomal evolution in primates: tentative phylogeny fromMicrocebus murinus (prosimians) to man.Ann. Genet., 48: 251–314.

    CAS  Google Scholar 

  • Eaglen, R. H., 1980. The systematics of living Strepsirhini, with special reference to the Lemuridae. Ph.D. thesis, Duke Univ., Durham.

    Google Scholar 

  • Ferguson, A., 1988. Isozyme studies and their interpretation. In:Prospects in Systematics,D. L. Hawksworth (ed.), Clarendon Press, Oxford, pp. 184–201.

    Google Scholar 

  • Fooden, J. &S. M. Lanyon, 1989. Blood-protein allele frequencies and phylogenetic relationships inMacaca: a review.Amer. J. Primatol., 17: 209–241.

    Article  Google Scholar 

  • Geibel, O., H. Ritter, &J. Schmitt, 1973. Transspecific variability of carbonic anhydrase I in primates.Humangenetik, 19: 331–334.

    CAS  PubMed  Google Scholar 

  • Hillis, D. M. 1984. Misuse and modification ofNei's genetic distance.Syst. Zool., 33: 238–240.

    Google Scholar 

  • Hopkinson, D. A., J. S. Coppock, M. F. Mühlemann, &Y. H. Edwards, 1974. The detection and differentiation of the products of the human carbonic anhydrase loci, CAI and CAII, using fluorogenic substrates.Ann. Human Genet., 38: 155–162.

    CAS  Google Scholar 

  • ————,M. A. Mestriner, J. Cortner, &H. Harris, 1973. Esterase D: a new human polymorphism.Ann. Human Genet., 37: 119–137.

    CAS  Google Scholar 

  • Kömpf, J., H. Ritter, &J. Schmitt, 1971. Zur transspezifischen Variabilität der Glucose-6-Phosphatdehydrogenase (E.C.: 1.1.1.49) der Primaten.Humangenetik, 11: 342–344.

    PubMed  Google Scholar 

  • Lewontin, R. C., 1989. Inferring the number of evolutionary events from DNA coding sequence differences.Mol. Biol. Evol., 6: 15–32.

    CAS  PubMed  Google Scholar 

  • Lucotte, G., 1979. Génétique des populations, spéciation et taxonomie chez les babouins: II. Similitudes génétique comparées entre différentes espèces:Papio papio, P. anubis, P. cynocephalus etP. hamadryas basées sur les données du polymorphisme des enzymes erythrocytaires.Biochem. Syst. Ecol., 7: 245–251.

    CAS  Google Scholar 

  • ————, 1983. Bases génétiques de la spéciation et de la taxonomie chez les babouins.Biochem. Syst. Ecol., 11: 145–158.

    Google Scholar 

  • Mason, G. A. &J. Buettner-Janusch, 1977. Codominant autosomal inheritance of polymorphic red cell acid phosphatases of lemurs and some properties of the enzymes.Biochem. Genet., 15: 487–507.

    Article  CAS  PubMed  Google Scholar 

  • Masters, J., 1988. Speciation in the greater galagos (Prosimii: Galaginae): review and synthesis.Biol. J. Linn. Soc., 34: 149–174.

    Google Scholar 

  • ———— &D. S. Dunn, 1988. Distribution of erythrocytic allozymes in two sibling species of greater galago [Galago crassicaudatus E. Geoffroy 1812 andG. garnettii (Ogilby 1838)].Amer. J. Primatol., 14: 235–245.

    Article  Google Scholar 

  • Meireles, C. M. M., M. I. C. Sampaio, H. Schneider, &M. P. C. Schneider, 1992. Protein variation, taxonomy and differentiation in five species of marmosets (genusCallithrix Erxleben, 1777).Primates, 33: 227–238.

    Article  Google Scholar 

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

    Google Scholar 

  • Molez, N. 1976. Adaptation alimentaire du galago d'Allen aux milieux forestiers secondaires.La Terre et la Vie, 30: 210–228.

    Google Scholar 

  • Nash, L. T., S. K. Bearder, &T. R. Olson, 1989. Synopsis of galago species characteristics.Int. J. Primatol., 10: 57–79.

    Google Scholar 

  • Nei, M., 1972, Genetic distance between populations.Amer. Naturalist, 106: 283–292.

    Article  Google Scholar 

  • ————, 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals.Genetics, 89: 583–590.

    Google Scholar 

  • Novacek, M. J., 1992. Mammalian phylogeny: shaking the tree.Nature, 356: 121–125.

    Article  CAS  PubMed  Google Scholar 

  • Nute, P. E., V. Buettner-Janusch, &J. Buettner-Janusch, 1969. Genetic and biochemical studies of transferrins and hemoglobins ofGalago.Folia Primatol., 10: 276–287.

    CAS  PubMed  Google Scholar 

  • Olson, T. R., 1979. Studies on aspects of the morphology of the genusOtolemur. Ph.D. thesis, Univ. of London, London.

    Google Scholar 

  • Prakash, S., R. C. Lewontin, &J. L. Hubby, 1969. A molecular approach to the study of genic heterozygosity in natural populations: IV. Patterns of genic variation in central, marginal, and isolated populations ofDrosophila pseudoobscura.Genetics, 61: 841–858.

    CAS  PubMed  Google Scholar 

  • Riley, M. A., 1989. Nucleotide sequence of the Xdh region inDrosophila pseudoobscura and an analysis of the evolution of synonymous codons.Mol. Biol. Evol., 6: 33–52.

    CAS  PubMed  Google Scholar 

  • Rumpler, Y., J. Couturier, S. Warter, &B. Dutrillaux, 1983. The karyotype ofGalago crassicaudatus is ancestral for Lorisiforms.Folia Primatol., 40: 227–231.

    CAS  PubMed  Google Scholar 

  • ———— &B. Dutrillaux, 1990. Chromosomal evolution and speciation in primates.Cell Biol. Rev., 23: 1–112.

    CAS  Google Scholar 

  • Ruvolo, M., 1983. Genetic evolution in the African guenon monkeys (Primates, Cercopithecinae). Ph.D. thesis, Harvard Univ., Cambridge.

    Google Scholar 

  • ————, 1988. Genetic evolution in the African guenons. In:A Primate Radiation: Evolutionary Biology of the African Guenons,A. Gautier-Hion,F. Bourliere,J.-P. Gautier, &J. Kingdon (eds.), Cambridge Univ. Press, Cambridge, pp. 127–139.

    Google Scholar 

  • Sampaio, M. I. C., M. P. C. Schneider, C. M. L. Barroso, B. T. F. Silva, H. Schneider, F. Encarnacion, E. Montoya, &F. M. Salzano, 1991. Carbonic Anhydrase II in New World monkeys.Int. J. Primatol., 12: 389–402.

    Google Scholar 

  • ————, ————,F. M. Salzano, &C. M. L. Barroso, 1986. Esterase D and Carbonic Anhydrase 2 in a natural population ofCebus apella from Brazil.Primates, 27: 363–367.

    Article  CAS  Google Scholar 

  • Simons, E. L. &Y. Rumpler, 1988.Eulemur: new generic name for species ofLemur other thanLemur catta.C. R. Acad. Sci. Paris, 307: 547–551.

    Google Scholar 

  • Suzuki, D. T., A. J. F. Griffiths, J. H. Miller, &R. C. Lewontin, 1989.An Introduction to Genetic Analysis, 4th ed., W. H. Freeman, New York.

    Google Scholar 

  • Swofford, D. L., 1985.PAUP: Phylogenetic Analysis Using Parsimony, Version 2.4. Illinois Natural History Survey, Champaign, Illinois.

    Google Scholar 

  • Tariverdian, G., H. Ritter, &J. Schmitt, 1971. Zur transspezifischen Variabilität der 6-Phosphogluconate-dehydrogenase (E.C.: 1.1.1.44) der Primaten.Humangenetik, 11: 323–327.

    CAS  PubMed  Google Scholar 

  • Tashian, R. E., 1965. Genetic variation and evolution of the carboxylic esterases and carbonic anhydrases of primate erythrocytes.Amer. J. Human Genet., 17: 257–272.

    CAS  Google Scholar 

  • ————,M. Goodman, V. E. Headings, J. de Simone, &R. H. Ward, 1971. Genetic variation and evolution in the red cell carbonic anhydrase isozymes of macaque monkeys.Biochem. Genet., 5: 183–200.

    Article  CAS  PubMed  Google Scholar 

  • Walker, S. E., C. J. Jolly, &J. F. Oates, 1988. Electrophoretic evidence for the evolutionary position ofCercopithecus erythrogaster andCercopithecus erythrotis.Folia Primatol., 51: 220–226.

    CAS  PubMed  Google Scholar 

  • Wesselman, H. B., 1984. The Omo micromammals: systematics and paleoecology of early man sites from Ethiopia.Contrib. Vert. Evol., 7: 1–219.

    Google Scholar 

  • Zimmermann, E., 1990. Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships.Z. Zool. Syst. Evolut.-forsch., 28: 217–239.

    Google Scholar 

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Author notes

  1. J. C. Masters

    Present address: Department of Anthropology, State University of New York at Stony Brook, 11794-4364, Stony Brook, New York, U. S. A.

  2. R. J. Rayner

    Present address: Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, P.O. Wits, Private Bag 3, 2050, South Africa

  3. H. Ludewick

    Present address: Department of Human Genetics (SAIMR), School of Pathology, University of the Witwatersrand, P.O. Wits, Private Bag 3, 2050, South Africa

  4. E. Zimmermann

    Present address: Deutsches Primatenzentrum GmbH, Kellnerweg 4, D-3400, Göttingen, Germany

  5. N. Molez-Verriere & F. Vincent

    Present address: Laboratorie de Biologie et Physiologie du Comportement, Université Paris X-Nanterre, 200 Avenue de la Republique, 92001, Nanterre Cedex, France

  6. L. T. Nash

    Present address: Department of Anthropology, Arizona State University, Box 872402, 85287-2402, Tempe, Arizona, U. S. A.

Authors and Affiliations

  1. Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, P.O. Wits, Private Bag 3, 2050, South Africa

    J. C. Masters

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Masters, J.C., Rayner, R.J., Ludewick, H. et al. Phylogenetic relationships among the galaginae as indicated by erythrocytic allozymes. Primates 35, 177–190 (1994). https://doi.org/10.1007/BF02382053

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