Molecular genetic analysis suggests that extant lion populations derive from several Pleistocene refugia in East and Southern Africa (324,000–169,000 years ago), which expanded during the Late Pleistocene (100,000 years ago) into Central and North Africa and into Asia. During the Pleistocene/Holocene transition (14,000–7,000 years), another expansion occurred from southern refugia northwards towards East Africa, allowing population interbreeding. In particular, the lions of the Serengeti Ecosystem appear to descend from three distinct populations that admixed in the past thousand years.

Population genetics and effects of inbreeding

Lions in the Ngorongoro Crater form a small and naturally isolated population. In 1962, the Crater lions suffered an epizootic that reduced the population to nine females and one male; seven males apparently immigrated into the Crater in 1964-1965, and only one additional male has moved into the Crater in the past 45 years. By 1975, the population had recovered to 75–125 animals, but subsequently dropped to 29 in 1998 and 32 in 2003, and there has been considerable variance in the reproductive success of both sexes. The Crater was likely colonized by lions from the Serengeti ecosystem, and the Crater lions showed a significant lack of genetic diversity compared to the much larger Serengeti lion population by the 1980s. Computer simulations suggest that the Crater population may have passed through previous bottlenecks before 1962 and that the level of heterozygosity in the breeding population has likely been declining since the mid-1970s.

The Asiatic lions in the Gir Forest Sanctuary in the state of Gujarat, India, descend from a population totaling fewer than 250 individuals by the 19th century. The Gir lions show far lower levels of genetic diversity than the Crater lions, suggesting a drastic population bottleneck followed by even more intense inbreeding than in Ngorongoro. Many studies of inbreeding in livestock and laboratory animals have shown that reduced heterozygosity can adversely affect spermatogenesis, ovulation and perinatal mortality and morbidity. Comparing reproductive profiles of male lions from the Serengeti, Ngorongoro Crater and Gir Forest, sperm abnormalities were most common in the most inbred populations.

In comparisons between the two Tanzanian populations, the Crater males had fewer seminiferous tubules with spermiogenesis and fewer spermatids per seminiferous tubular cross-section than Serengeti lions; interstitial areas were greater in Crater lions, suggesting that proportionately less testicular area was occupied by seminiferous tubules in Crater males. However, basal serum luteinizing hormone (LH) or follicle-stimulating hormone (FSH) concentrations were similar between locations, as was GnRH-stimulated LH release and basal and GnRH-stimulated testosterone secretion. Seminal quality in the Crater population was poor in adult and young adult animals and was unrelated to alterations in pituitary or testicular function. In summary, only seminal quality in adult male lions was affected by location.

The reproductive-endocrine system of Crater females appears functionally normal compared with their Serengeti counterparts. Basal serum cortisol and basal and GnRH-induced gonadotrophin secretion were similar between Serengeti and Ngorongoro females. After ACTH stimulation, serum cortisol increased two- to threefold over baseline values and the response was unaffected by location. ACTH-induced increases in serum cortisol had no effect on subsequent basal or GnRH-stimulated LH or FSH secretion. There were no differences between Serengeti and Crater lions in mean serum progesterone, oestradiol or prolactin concentrations, nor was hormone secretion influenced differently by GnRH or ACTH treatment.

Genetic management

Many surviving populations of wild lions live in fragmented habitats with little opportunity for genetic exchange, thus risks of inbreeding are likely to increase throughout Africa. In the Hluhluwe-iMfolozi Park (HiP), a small, enclosed reserve in South Africa, a large lion Panthera leo population arose from a founder group of five individuals in the 1960s. The HiP lion population went through a persistent decline and showed indications of inbreeding depression. To restore the genetic variation of the inbred HiP lion population, new lions were translocated into the existing population. Translocated females formed stable associations and established enduring pride areas with other translocated lionesses. The translocated male coalition was also successful in gaining and maintaining residence in a pride. Litter size and cub survival was about twice as high for pairings involving at least one translocated parent than for pairings of two native lions. It is therefore possible to infuse new genes rapidly and successfully into a small, isolated lion population.

Elsewhere in South Africa, more than 30 small, enclosed game reserves have reintroduced lions over the last two decades, now totaling more than 500 individuals. The risks of inbreeding in these fenced, isolated populations may be compounded by a lack of management guidelines. A population of 11 founder lions Panthera leo was reintroduced to Madikwe Game Reserve in 1995 and subsequently became a source for reestablishing other populations. When lion density was low, females first gave birth at a significantly younger age and produced larger litters, resulting in a high population growth rate, which decreased significantly as lion density in Madikwe reached an apparent carrying capacity of 61 lions. Only four lineages were reintroduced into Madikwe, founder males were related to founder females, and since 1997, only one male lineage maintained tenure for over 9 years, resulting in breeding with direct relatives. Interventionist management to limit lion population growth and inbreeding involved translocations, trophy hunting and culling of subadults, yet inbreeding started only 5 years after reintroduction. This study illustrates the need for founder populations of reintroduced species to be as large and genetically diverse as possible, and thereafter new genetic material should be supplemented and lions in separate reserves should be managed as metapopulations.