The evolutionary history of extinct and living lions

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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.

Abstract

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.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A

Journal ID (hwp): pnas

Journal ID (pmc): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Print): 19 May 2020

Publication date (Electronic): 4 May 2020

Publication date PMC-release: 4 May 2020

Volume: 117

Issue: 20

Pages: 10927-10934

Affiliations

[1] ^aInstitute of Evolutionary Biology (UPF-CSIC) , PRBB, 08003 Barcelona, Spain;

[2] ^bSection for Evolutionary Genomics, The GLOBE Institute, Faculty of Health and Medical Sciences, University of Copenhagen , 1353 Copenhagen, Denmark;

[3] ^cInstitute of Tropical Biodiversity and Sustainable Development, University Malaysia Terengganu , 21030 Kuala Nerus, Terengganu, Malaysia;

[4] ^dSchool of Medical and Dental Sciences, Institute of Microbiology and Infection, University of Birmingham , B15 2TT Edgbaston, Birmingham, United Kingdom;

[5] ^eBGI-Shenzhen , 518083 Shenzhen, China;

[6] ^fNorwegian University of Science and Technology (NTNU) University Museum , 7012 Trondheim, Norway;

[7] ^gBGI Education Center, University of Chinese Academy of Sciences , 518083 Shenzhen, China;

[8] ^hYukon Palaeontology Program, Department of Tourism and Culture, Government of Yukon , Y1A 2C6 Whitehorse, Yukon, Canada;

[9] ⁱZoological Institute, Russian Academy of Sciences , 199034 St. Petersburg, Russia;

[10] ^jLaboratory of Genomics and Molecular Biology, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS) , Porto Alegre, RS 90619-900, Brazil;

[11] ^kInstituto Nacional de Ciência e Tecnologia - Ecologia Evolução e Conservação da Biodiversidade (INCT-EECBio) , Goiânia, GO 74690-900, Brazil;

[12] ^lInstituto Pró-Carnívoros , Atibaia, SP 12945-010, Brazil;

[13] ^mCenter for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park , Front Royal, VA 22630;

[14] ⁿThe Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution , Suitland, MD 20746-2863;

[15] ^oWalter Reed Army Institute of Research , Silver Spring, MD 20910;

[16] ^pInterdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto , 4450-208 Porto, Portugal;

[17] ^qDepartment of Biology, Faculty of Sciences, University of Porto , 4169-007 Porto, Portugal;

[18] ^rCentre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, Asian Institute of Medicine, Science and Technology (AIMST) , 08100 Bedong, Kedah, Malaysia;

[19] ^sThe Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and the History of Art, University of Oxford , OX1 3QY Oxford, United Kingdom;

[20] ^tJames D. Watson Institute of Genome Science , 310008 Hangzhou, China;

[21] ^uLaboratory of Genomic Diversity, Center for Computer Technologies, ITMO (Information Technologies, Mechanics and Optics) University , 197101 St. Petersburg, Russia;

[22] ^vGuy Harvey Oceanographic Center Halmos College of Natural Sciences and Oceanography, Nova Southeastern University , Ft. Lauderdale, FL 33004;

[23] ^wSection for GeoGenetics, The GLOBE Institute, Faculty of Health and Medical Sciences, University of Copenhagen , 1350 Copenhagen, Denmark;

[24] ^xSection for Ecology and Evolution, Department of Biology, Faculty of Science, University of Copenhagen , 2100 Copenhagen, Denmark;

[25] ^yState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences , 650223 Kunming, China;

[26] ^zCentre Nacional d'Anàlisi Genòmica, Centre for Genomic Regulation (CNAG-CRG), The Barcelona Institute of Science and Technology , 08028 Barcelona, Spain;

[27] ^aaInstitució Catalana de Recerca i Estudis Avançats (ICREA) , 08003 Barcelona, Spain;

[28] ^bbInstitut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona , Edifici ICTA-ICP, 08193 Cerdanyola del Vallès, Barcelona, Spain

Author notes

²To whom correspondence may be addressed. Email: lgdchief@ 123456gmail.com , tomas.marques@ 123456upf.edu , tgilbert@ 123456sund.ku.dk , or nobuyuki.yamaguchi@ 123456umt.edu.my .

Contributed by Stephen J. O’Brien, March 14, 2020 (sent for review November 11, 2019; reviewed by Jeffrey M. Good and Cristiano Vernesi)

Author contributions: M.d.M., R.B., N.Y., S.J.O., T.M.-B., and M.T.P.G. designed research; M.d.M., R.B., M.S.-V., N.Y., M.-H.S.S., S.S.T.M., C.C., Shanlin Liu, C.G., J.Z., G.Z., E.E., K.-P.K., W.E.J., G.L., H.Y., S.J.O., G.Z., T.M.-B., and M.T.P.G. performed research; C.G., J.Z., G.B., T.S.-P., H.Y., S.J.O., A.J.H., and G.Z. contributed new reagents/analytic tools; M.d.M., R.B., M.S.-V., N.Y., F.G.V., M.L.Z.M., Shiping Liu, M.D.M., E.E., A.A., S.G., S.J.O., and M.T.P.G. analyzed data; M.d.M., R.B., N.Y., S.J.O., T.M.-B., and M.T.P.G. wrote the paper; and G.B. contributed samples.

Reviewers: J.M.G., University of Montana; and C.V., Fondazione Edmund Mach.

¹M.d.M. and R.B. contributed equally to this work.