The evolutionary history of extinct and living lions

Significance Lions were once the most globally widespread mammal species, with distinct populations in Africa, Eurasia, and America. We generated a genomic dataset that included 2 extinct Pleistocene cave lions, 12 lions from historically extinct populations in Africa and the Middle East, and 6 modern lions from Africa and India. Our analyses show the Pleistocene cave lion as maximally distinct with no evidence of hybridization with other lion groups based on the level of population structure and admixture. We also confirm long-term divisions between other extant lion populations and assess genetic diversity within individual samples. Our work provides views on the complex nature of the global lion species-complex and its evolution and provides conservation data for modern lion regional populations. Lions are one of the world’s most iconic megafauna, yet little is known about their temporal and spatial demographic history and population differentiation. We analyzed a genomic dataset of 20 specimens: two ca. 30,000-y-old cave lions (Panthera leo spelaea), 12 historic lions (Panthera leo leo/Panthera leo melanochaita) that lived between the 15th and 20th centuries outside the current geographic distribution of lions, and 6 present-day lions from Africa and India. We found that cave and modern lions shared an ancestor ca. 500,000 y ago and that the 2 lineages likely did not hybridize following their divergence. Within modern lions, we found 2 main lineages that diverged ca. 70,000 y ago, with clear evidence of subsequent gene flow. Our data also reveal a nearly complete absence of genetic diversity within Indian lions, probably due to well-documented extremely low effective population sizes in the recent past. Our results contribute toward the understanding of the evolutionary history of lions and complement conservation efforts to protect the diversity of this vulnerable species.