High genetic diversity and low differentiation reflect the ecological versatility of the African leopard

Large carnivores are generally sensitive to ecosystem changes because their specialized diet and position at the top of the trophic pyramid is associated with small population sizes. Accordingly, low genetic diversity at the whole-genome level has been reported for all big cat species, including the widely distributed leopard. However, all previous whole-genome analyses of leopards are based on the Far Eastern Amur leopards that live at the extremity of the species’ distribution and therefore are not necessarily representative of the whole species. We sequenced 53 whole genomes of African leopards. Strikingly, we found that the genomic diversity in the African leopard is 2- to 5-fold higher than in other big cats, including the Amur leopard, likely because of an exceptionally high effective population size maintained by the African leopard throughout the Pleistocene. Furthermore, we detected ongoing gene flow and very low population differentiation within African leopards compared with those of other big cats. We corroborated this by showing a complete absence of an otherwise ubiquitous equatorial forest barrier to gene flow. This sets the leopard apart from most other widely distributed large African mammals, including lions. These results revise our understanding of trophic sensitivity and highlight the remarkable resilience of the African leopard, likely because of its extraordinary habitat versatility and broad dietary niche. [Display omitted] •African and Amur leopards have markedly different demographic trajectories•Among big cats, African leopards have the highest genetic diversity•Gene flow on a continent-wide scale maintains low genetic differentiation•Broad dietary and habitat niche likely explain the extraordinary genetic makeup Pečnerová et al. analyze whole-genome data from 53 African leopards and identify genetic features that set the African leopard apart from the Amur leopards, as well as the other big cats. This includes long-term high effective population size and exceptionally high levels of genetic diversity and connectivity.