Bottleneck(s) or Metapopulation in Cheetahs

The "cheetah paradigm" proposes that a low leve.l of genetic variation has resulted in a high probability of extinction for this species (O'Brien et al. 1983, 1985, 1987), a connection that has recently been questioned (Caro & Laurenson 1994; Caughley 1994; May 1994; Merola 1994). I do not wish to address this controversy further but to suggest that the extent of genetic variation observed in cheetahs, including the recent minisatellite and microsatellite data, is consistent with the equilibrium heterozygosity expected from the small effective population size that may occur because of metapopulation dynamics, that is, because of extinction and recolonization of habitat patches (Slatkin 1977; Maruyama & Kimura 1980; Hedrick & Gilpin 1996). In other words, a severe, ancient population bottleneck (O'Brien et al 1983) or a series of ancient bottlenecks "over time, over space or both, with small populations being founded and surviving, while the larger parent populations died out" (O'Brien et al. 1987) at the end of Pleistocene (10,000 to 12,000 years ago) are not the only explanations for the observed pattern of genetic variation in cheetahs. It should also be noted that there is no direct fossil evidence in Africa for extinctions (or population bottlenecks) of megafauna in general, or cheetahs in particular, at the end of the Pleistocene, as there is for megafauna in North America. The original genetic data for which the cheetah bottleneck hypothesis was proposed was the low allozyme variation observed in the south African cheetah (Acinonyxjubatusjubatus) (O'Brien et al. 1983). In this initial survey 47 allozyme loci were all monomorphic, whereas in a follow-up study (O'Brien et al. 1987) the average heterozygosity over A. j. jubatus and A. j. raineyi, the east African subspecies, was 0.0072 (see comparisons to other species in Table 1). Heterozygosity for soluble proteins was somewhat lower in cheetahs (0.013) than in humans (0.024) (O'Brien et al. 1983) and heterozygosity for restriction fragment length polymorphisms (RFLPs) in the major histocompatibility complex was lower in cheetahs (0.059) than in humans (0.174) (Yukhi & O'Brien 1990). (In a related study, skin transplants between unrelated individuals were accepted in 11 or 14 attempts [O'Brien et al. 1985]). In contrast, substantial levels of genetic variation have recently been documented in cheetahs for mtDNA, minisatellites, and microsatellites (Menotti-Raymond & O'Brien 1993, 1995). For example, four mtDNA RFLP haplotypes were found in A. j. jubatus, and three different haplotypes were found in A. j. raineyi. The overall mtDNA nucleotide diversity was 0.0018, compared to 0.0035 in pumas (Felis concolor), the cheetah's closest relative. The level of heterozygosity in cheetahs is 0.435 for minisatellites (Menotti-Raymond & O'Brien 1993) and for microsatellites is 0.39 (Menotti-Raymond & O'Brien 1995; see Table 1 for comparisons to other species). Further, when the two cheetah subspecies are compared, 29% of the minisatellite fragments and 44% of the microsatellite alleles are unique to one of the subspecies. Because of the substantial variation observed for mtDNA, minisatellites, and microsatellites, Menotti-Raymond and O'Brien (1993, 1995) suggest that cheetahs have accumulated variation for these markers since the hypothetical bottleneck(s) because of their high mutation rates, whereas the low variation of allozymes remains because of the lower mutation rate for these loci. An alternative to the bottleneck hypothesis for the observed pattern of genetic variation in cheetahs is that cheetahs have a metapopulation structure (Pimm et al. 1989; Gilpin 1991; see also O'Brien 1989). A number of factors, such as prey availability, predators, habitat struc-