Abstract
The electrophoretic phenotypes of the two isozymes of red cell carbonic anhydrase, CA I and CA II, are described in nine species of macaque monkeys from southeast Asia and Japan. Twelve phenotypes of CA I, apparently under the control of seven alleles, and five phenotypes of CA II, under the control of three alleles, were found in the different macaque populations studied. Extensive electrophoretic polymorphisms of CA I were found in three species (Macaca nemestrina, Macaca speciosa, and Macaca fuscata), and polymorphisms at the CA II locus were found in Macaca irus, Macaca mulatta, and M. nemestrina. In addition to the electrophoretic polymorphisms at the CA I locus in M. nemestrina, an inherited deficiency of CA I was also discovered in which approximately 30% of the individuals in all populations of M. nemestrina tested showed the deficient phenotype. Although the recessive gene controlling this deficiency appears to be an allele of the CA I locus, it is postulated that the CA I deficiency could also be under the control of a closely linked gene. The comparative data on the extent of genetic variation observed in the two isozymes of red cell carbonic anhydrase in macaques appear to support the concept that CA I has evolved more rapidly than CA II in mammals.
Similar content being viewed by others
References
Barnicot, N. A., Jolly, C., Huehns, E. R., and Moor-Jankowski, J. (1964). A carbonic anhydrase variant in the baboon. Nature 202 198.
Bernstein, I. S. (1966). Naturally occurring primate hybrid. Science 154 1559.
Boyer, S. H., Crosby, E. F., Thurmon, T. F., Noyes, A. N., Fuller, G. F., Leslie, S. E., Shepard, M. K., and Herndon, C. N. (1969). Hemoglobins A and A2 in New World primates: Comparative variation and its evolutionary implications. Science 166 1428.
Derrien, Y., and Laurent, G. (1969). The erythrocyte carbonic anhydrases. Exposés Annuels Biochim. Méd., Ser. 29, p. 167.
Duff, T. A., and Coleman, J. E. (1966). Macaca mulatta carbonic anhydrase. Crystallization and physiochemical and enzymatic properties of two isozymes. Biochemistry 5 2009.
Edsall, J. (1968). The carbonic anhydrases of erythrocytes. Harvey Lectures, Ser. 62, p. 191.
Epstein, C. J., and Schechter, A. N. (1968). An approach to the problem of conformational isozymes. Ann. N.Y. Acad. Sci. 151 85.
Fooden, J. (1964). Rhesus and crab-eating macaques: Integradation in Thailand. Science 143 363.
Fooden, J. (1969). Taxonomy and evolution of the monkeys of Celebes (primates: Cercopithecidae). Bibliotheca Primatologica, No. 10, S. Karger, Basel, New York, pp. 1–148.
Funakoshi, S., and Deutsch, H. F. (1968). Human carbonic anhydrases. I. Isolation and demonstration of isozymes in erythrocytes. J. Biol. Chem. 243 6474.
Funakoshi, S., and Deutsch, H. F. (1969). Human carbonic anhydrases. II. Some physiochemical properties of native isozymes and of similar isozymes generated in vitro. J. Biol. Chem. 244 3488.
Furth, A. J. (1968). Purification and properties of horse erythrocyte carbonic anhydrases. J. Biol. Chem. 243 4832.
Gibbons, B. H., and Edsall, J. T. (1964). Kinetic studies of human carbonic anhydrases B and C. J. Biol. Chem. 239 2539.
Headings, V. E., and Tashian, R. E. (1970a). A radioimmunoassay for quantifying carbonic anhydrase isozymes in crude lysates. Biochem. Genet. 4 285.
Headings, V. E., and Tashian R. E. (1970b). Quantitative genetic variation in carbonic anhydrase isozymes from blood cells and other tissues of the pig-tailed macaque, Macaca nemestrina (submitted for publication).
Kimura, M., and Ohta, T. (1969a). The average number of generations until fixation of a mutant gene in a finite population. Genetics 61 763.
Kimura, M., and Ohta, T. (1969b). The average number of generations until extinction of an individual mutant gene in a finite population. Genetics 63 701.
King, J. L., and Jukes, T. H. (1969). Non-Darwinian evolution. Science 164 788.
Nesturkh, M. (1959). The Origin of Man, Foreign Languages Publishing House, Moscow.
Nyman, P. O., Strid, L., and Westermark, G. (1968). Carboxy-terminal region of human and bovine erythrocyte carbonic anhydrases. I. Amino acid sequences of terminal cyanogen bromide fragments. European J. Biochem. 6 172.
Reed, T. E., and Schull, W. J. (1968). A general maximum likelihood estimation program. Am. J. Human Genet. 20 579.
Salthe, S. N. (1969). Geographic variation of the lactate dehydrogenases of Rana pipiens and Rana palustris. Biochem. Genet. 2 271.
Sandberg, K. (1968). Genetic polymorphism in carbonic anhydrase from horse erythrocytes. Hereditas 60 411.
Sartore, G., Stormont, C., and Grunder, A. A. (1969). Multiple electrophoretic forms of carbonic anhydrase in red cells of domestic cattle (Bos taurus) and American buffalo (Bison bison). Genetics 61 823.
Shows, T. B., and Ruddle, F. H. (1968). Function of the lactate dehydrogenase B gene in mouse erythrocytes: Evidence for control by a regulator gene. Proc. Natl. Acad. Sci. 61 574.
Shows, T. B., Massaro, E. J., and Ruddle, F. H. (1969). Evolutionary evidence for a regulator gene controlling the lactate dehydrogenase B gene in rodent erythroctyes. Biochem. Genet. 3 525.
Tanis, R. J., Tashian, R. E., and Yu, Y.-S. L. (1970). Properties of carbonic anhydrase isozymes isolated from porcine erythrocytes. J. Biol. Chem. 245 6003.
Tashian, R. E. (1965). Genetic variation and evolution of the carboxylic esterases and carbonic anhydrases of primate erythrocytes. Am. J. Human Genet. 17 257.
Tashian, R. E. (1969). The esterases and carbonic anhydrases of human erythrocytes. In Yunis, J. J. (ed.), Biochemical Methods in Red Cell Genetics, Academic Press, New York, pp. 307–336.
Tashian, R. E., Shreffler, D. C., and Shows, T. B. (1968). Genetic and phylogenetic variation in the different molecular forms of mammalian erythrocyte carbonic anhydrases. Ann. N.Y. Acad. Sci. 151 64.
Tucker, E. M., Suzuki, Y., and Stormont, C. (1967). Three new phenotypic systems in the blood of sheep. Vox Sanguinis 13 246.
Author information
Authors and Affiliations
Additional information
Supported by USPHS grant GM-15419 and NSF grants GF-253, GB-7426, and GB-15060 of the U.S.-Japan Cooperative Science and Systemic Biology Programs.
Rights and permissions
About this article
Cite this article
Tashian, R.E., Goodman, M., Headings, V.E. et al. Genetic variation and evolution in the red cell carbonic anhydrase isozymes of macaque monkeys. Biochem Genet 5, 183–200 (1971). https://doi.org/10.1007/BF00485644
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00485644