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Genetic Basis for Species Vulnerability in the Cheetah

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Genetic Basis for Species Vulnerability in the Cheetah was probably provided by the variation 7. J. M. Franklin, D. M. Sangster, J. W. Lydon, in Meeting of the Institute on Lake Superior Geol- 75th Anniversary Volume, Economic Geology, ogy, G. L. LaBerge, Ed. (Institute of Lake in the carbon content of continental crust P. Sims, Ed. (Economic Geology, Lancaster, Superior Geology, Wausau, Wise, 1984), pp. Pa., 1981), pp. 485-627. 17-18 (abstract). available for partial melting. Through its 8. F. Mendelsohn, Ed., Geology of the Northern 18. D. E. Roberts and G. R. T. Hudson, Econ. oxygen-carbon energy storage cell, the Rhodesian Copperbelt (McDonald, London, Geol. 78, 799 (1983). 1961); A. Francois, in Gisements Stratiform et 19. E. S. O'DriscoU, in Australasian Institute of biomass has influenced the patterns of Provinces Cuprifères, P. Bartholomè, Ed. (So- Mining and Metallurgy Broken Hill Conference nearly all the ore metals, except perhaps ciété Géologique de Belgique, Liege, 1974), pp. (Australasian Institute of Mining and Metallur- 79-101. gy, Sydney, 1983), pp. 29-47; Pet. Explor. Soc. those of chromium, nickel, and titanium. 9. P. G. Söhnge, Geol. Soc. S. Afr. Spec. Publ. Aust. 1, 11 (1982). (1964), pp. 367-382. 20. G. N. Phillips and D. L. Groves, /. Geol. Soc. References and Notes 10 L. B. Gustafson and N. Williams, in 75th Anni- Aust. 30, 25 (1983). versary Volume, Economie Geology, P. Sims, 21. D. A. Pretorius, in 75th Anniversary Volume, 1. A chart listing individual deposits by type and Ed. (Economie Geology, Lancaster, Pa., 1981), Economic Geology, P. Sims, Ed. (Economic age may be found in C. Meyer, in 75th Anniver- pp. 139-178. Geology, Lancaster, Pa., 1981), pp. 117-138. sary Volume, Economic Geology, P. Sims, Ed. 11 S. R. Titley, Ed., Advances in Geology of the 22. J. T. Nash et al., ibid., pp. 63-116. (Economic Geology, Lancaster, Pa., 1981), p. Porphyry Copper Deposits (Univ. of Arizona 23. C. Meyer and J. J. Hemley, in Geochemistry of 12. Press, Tucson, 1982); I. M. Guilbert and J. D. Hydrothermal Ore Deposits, H. L. Barnes, Ed. 2. First-cycle magma is derived from the partial Lowell, Trans. Can. Inst. Min. Metallurg. TI, (Holt, Rinehart, Winston, New York, 1967), pp. melting of mantle; second-cycle magma from the 105 (1974). 166-235. partial melting of rock from first-cycle magma, 12. J. D. Lowell, Econ. Geol. 69, 601 (1974). 24. B. W. Chappel and A. J. R. White, Pac. Geol. 8, for example, oceanic crust; third-cycle magma 13. V. F. HoUister, Geology of the Porphyry Copper 173 (1974); S. Ishihara, J. Min. Geol. Soc. Jpn. from the melting of continental crust. Deposits of the Western Hemisphere (Special 21, 293 (1977). 3. T. P. Thayer, Geol. Assoc. Can, Spec. Pap. 14 Publication, American Institute of Mining and 25. This article incorporates important suggestions (1976), p. 211; A. J. Naldrett and L. J. Cabri, Metallurgical Engineers, New York, 1978). made by a reviewer. V. B. Meyer assisted with Econ. Geol. 71, 1131 (1976). 14. H. L. James and P. K. Sims, Econ. Geol. 68,913 editorial work and prepared the manuscript. I 4. P. Cotterill, Econ. Geol. Monogr. 4 (1969). (1973). am grateful to both, but especially to Editor P. 5. R. Woodall and G. A. Travis, in Proceedings of 15. P. Cloud, Trans. Geol. Soc. S. Afr. 79, 1 (1976) H. Abelson for his interest over the years in the 9th Congress (Commonwealth Mining and (Alex du Toit Memorial Lecture). resource appraisal, stimulating papers, wise edi- Metallurgical Congress, London, 1969), vol. 2, 16. S. Moorbath, R. K. O'Nions, R. J. Pankhurst, torials, and compilations on energy and minerals pp. 517-533. Nature (London) 245, 138 (1973). which awakened the interest of a wider constitu- 6. N. Herz, Science 164, 944 (1969). 17. S. A. Hauk and E. W. Kendall, in 30th Annual ency than geologists ordinarily reach. both anatomy and behavior from the other genera in the Felidae {5-7). Chee- tahs, the world's swiftest sprinters, have a number of cursorial adaptations that make high-speed pursuit (up to 112 Genetic Basis for Species km/hour) possible (5): long, slender legs; enlarged respiratory, cardiovascular, and adrenal capacities; specialized mus- Vulnerability in the Cheetah cles for high acceleration; and semire- tractile claws (5, 6). Because of its swift S. J. O'Brien, M. E. Roelke, L. Marker, A. Newman and elusive character, demographic esti- C. A. Winkler, D. Meltzer, L. Colly, J. F. Evermann mates of wild cheetahs vary considera- bly (from 1,500 to 25,000 animals) {8-11). M. Bush, D. E. Wildt Most animals are restricted to two re- maining wild populations in southern and eastern Africa, where the population density is less than one animal per 6 km'^ Over 1000 animal species, many of vid's deer, the Mongolian wild horse, (9). This low density can be partially them mammaüan, have been recognized and the European bison), but other spe- explained by the cheetah's solitary na- by the Convention of International Trade cies (such as clouded leopards, pen- ture, for, unlike the lion, the cheetah in Endangered Species as being threat- guins, and condors) have done very usually avoids family groups {8, 11). In ened by extinction (7). Although 1000 poorly under captive propagation condi- addition, cheetah cubs appear to suffer seems a large number, it probably repre- tions (4). The reasons for success or severe mortality (estimated at as high as sents a minor part of a larger process (2, failure in these programs are obscure, 70 percent) due to disease susceptibility, 3). Myers (2) estimated that, of the 5 to since scientists and curators have almost maternal neglect, and insufiflcient de- 10 million living biological species, as none of the necessary background infor- fense against predators (72). many as 1 million probably will become mation for species that are threatened or In 1971 the National Zoological Gar- extinct by the turn of the century. At the rare (2). dens of South Africa initiated a compre- present accelerating rate of extinction, There are 37 species in the cat family hensive program for the propagation of this translates to losing one species ev- (Felidae), and all except the domestic cat cheetahs in captivity (75). In 1981 40 ery hour. Many large mammals already are considered threatened or endangered semen samples from 18 cheetahs were have become extinct in the wild and (7). The cheetah {Acinonyx jubatus) is collected, examined, and compared to survive today only under managed the single surviving species of the genus the semen of domestic cats {14). Sperma- breeding programs in zoological parks Acinonyx and is considered by most tax- tozoal concentrations in ejaculates were and wildlife preserves (4). The acceler- onomists to be markedly divergent in ten times less in cheetahs than in domes- ated rate of habitat destruction has led to the prospect that in the next century S. J. O'Brien, A. Newman, and C. Winkler are in the Section of Genetics, National Cancer Institute, Frederick, Maryland 2I70I. M. E. Roelke and L. Marker are with Wildlife Safari, Winston, Oregon 97496. D. virtually all exotic wildlife will be man- Meltzer is in the Department of Physiology, Faculty of Veterinary Science, Onderstepoart 0110, Republic of aged in captive breeding programs. Sev- South Africa. L. Colly is with the Johannesburg Zoological Gardens, Johannesburg, Republic of South Africa. J. F. Evermann is in the College of Veterinary Medicine, Washington State University, Pullman eral programs have been successful 99164. M. Bush and D. E. Wildt are with the National Zoological Park, Smithsonian Institution, Washington, (most notably those involving Père Da- D.C. 20008. 1428 SCIENCE, VOL. 227 tic cats, and an average of 71 percent of Fig. 1: (i) as Rails and colleagues (17) noninbred matings of cheetahs, which is all cheetah spermatozoa were morpho- have described, inbred oflFspring of zoo not surprising in light of the genetic logically abnormal, compared to 29 per- species in general have consistently status of the species (75). If the cheetah cent in cats. Comparable abnormalities greater juvenile mortality than their non- is as monomorphic for those loci that were observed in semen collected from inbred zoo counterparts; (ii) cheetah contribute to congenital defects or lethal- cheetahs in zoos in the United States. In mortality from noninbred matings occurs ity as it is for biochemical loci, then a parallel study in which over 200 iso- at the high end of the distribution, with inbreeding would probably not lead to zyme and cellular protein loci of 55 only two species (reindeer and dik-dik) the expression of any more deleterious South African cheetahs were analyzed, having higher noninbred mortality; and recessive alíeles than would be observed the population was found to contain 10 to (iii) there is no significant difference be- in genetically variable outbred popula- 100 times less genetic variation than oth- tween infant mortalities from inbred and tions. er mammalian species (15). Both the genetic and reproductive data cast the cheetah in a status reminiscent of highly inbred mice or livestock and prompted Summary. A population genetic survey of over 200 structural loci previously us to hypothesize that the species experi- revealed that the South African cheetah [Acinonyx jubatus jubatus) has an extreme enced a severe population bottleneck in paucity of genetic variability, probably as a consequence of a severe population its recent evolutionary history (75). The bottleneck in its recent past. The genetic monomorphism of the species is here possible consequences of such genetic extended to the major histocompatibility complex, since 14 reciprocal skin grafts uniformity would include high species between unrelated cheetahs were accepted. The apparent consequences of such vulnerability because such circum- genetic unlfonnity to the species include (I) great difficulty In captive breeding, (11) a stances not only allow expression of high degree of juvenile mortality in captivity and In the wild, and (ill) a high frequency deleterious recessive alíeles but also hm- of spermatozoal abnonnalities in ejaculates.
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