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(Panthera Leo Ssp.) Reveals Three Distinct Taxa and a Late Pleistocene Reduction in Genetic Diversity

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(Panthera Leo Ssp.) Reveals Three Distinct Taxa and a Late Pleistocene Reduction in Genetic Diversity Molecular Ecology (2009) 18, 1668–1677 doi: 10.1111/j.1365-294X.2009.04134.x PhylogeographyBlackwell Publishing Ltd of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity ROSS BARNETT,* BETH SHAPIRO,† IAN BARNES,‡ SIMON Y. W. HO,§ JOACHIM BURGER,¶ NOBUYUKI YAMAGUCHI,** THOMAS F. G. HIGHAM,†† H. TODD WHEELER,‡‡ WILFRIED ROSENDAHL,§§ ANDREI V. SHER,¶¶,‡‡‡‡ MARINA SOTNIKOVA,*** TATIANA KUZNETSOVA,††† GENNADY F. BARYSHNIKOV,‡‡‡ LARRY D. MARTI N,§§§ C. RI CHARD HARI NGTON,¶¶¶ JAMES A. BURNS**** and ALAN COOPER†††† *Department of Zoology, University of Oxford, Oxford OX1 3PS, UK, †Department of Biology, Pennsylvania State University, University Park, PA 16801, USA, ‡Department of Biology, University College London, London WC1E 6BT, UK, §Centre for Macroevolution and Macroecology, School of Botany and Zoology, Australian National University, Canberra, ACT 0200, Australia, ¶Institute of Anthropology, Mainz University, 55099 Mainz, Germany, **Department of Biological and Environmental Sciences, University of Qatar, PO Box 2713, Doha, Qatar, ††Research Laboratory for Archaeology, University of Oxford, Oxford OX1 3QJ, UK, ‡‡George C. Page Museum of La Brea Discoveries, Los Angeles, CA 90036, USA, §§Reiss-Engelhorn-Museen, D-68159 Mannheim, Germany, ¶¶Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071 Moscow, Russia, ***Geological Institute, Russian Academy of Sciences, 119017 Moscow, Russia, †††Palaeontological Department, Geological Faculty, Moscow State University, 119899 Moscow, Russia, ‡‡‡Zoological Institute, Russian Academy of Sciences, 199034 St Petersburg, Russia, §§§Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USA, ¶¶¶Canadian Museum of Nature (Palaeobiology), Ottawa, ON, Canada K1P 6P4, ****Quaternary Palaeontology, Royal Alberta Museum, Edmonton, AB, Canada T5N 0M6, ††††School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia Abstract Lions were the most widespread carnivores in the late Pleistocene, ranging from southern Africa to the southern USA, but little is known about the evolutionary relationships among these Pleistocene populations or the dynamics that led to their extinction. Using ancient DNA techniques, we obtained mitochondrial sequences from 52 individuals sampled across the present and former range of lions. Phylogenetic analysis revealed three distinct clusters: (i) modern lions, Panthera leo; (ii) extinct Pleistocene cave lions, which formed a homogeneous population extending from Europe across Beringia (Siberia, Alaska and western Canada); and (iii) extinct American lions, which formed a separate population south of the Pleistocene ice sheets. The American lion appears to have become genetically isolated around 340 000 years ago, despite the apparent lack of significant barriers to gene flow with Beringian populations through much of the late Pleistocene. We found potential evidence of a severe population bottleneck in the cave lion during the previous interstadial, sometime after 48 000 years, adding to evidence from bison, mammoths, horses and brown bears that megafaunal popu- lations underwent major genetic alterations throughout the last interstadial, potentially presaging the processes involved in the subsequent end-Pleistocene mass extinctions. Keywords: American lion, ancient DNA, Beringia, cave lion, extinction, megafauna Received 3 October 2008; revision received 6 January 2009; accepted 15 January 2009 Introduction Correspondence: Ross Barnett, E-mail: [email protected]; Lions currently survive only in parts of Africa and India, Alan Cooper, Australian Centre for Ancient DNA, School of Earth yet as recently as the late Pleistocene (LP), large and and Environmental Sciences, University of Adelaide, Adelaide, morphologically diverse forms of lion were distributed SA 5005, Australia. E-mail: [email protected] ‡‡‡‡Deceased. across the Northern Hemisphere. Lions survived in Europe, © 2009 Blackwell Publishing Ltd PHYLOGEOGRAPHY OF PLEISTOCENE LIONS 1669 Fig. 1 Pleistocene lion distribution and sample origin. Colours correspond to commonly cited population subdivisions (e.g. Baryshnikov & Boeskorov 2001). Numbers refer to particular samples used in this analysis (Table 1). northern Asia, and North America until around 11 000 bp number of distinct species or the extent of overlap of their (Fig. 1), when they disappeared as part of the end-Pleistocene distributions (for a comprehensive overview of the taxonomy megafaunal mass extinctions (Martin & Steadman 1999). of pantherine cats, please refer to Burger et al. 2004). Human hunting and/or environmental alteration, and Morphological identification is complicated by the climate changes associated with the last glacial maximum presence of shared primitive features (e.g. Sotnikova & (LGM; 22 000–18 000 bp) and the end of the Pleistocene have Nikolskiy 2006), although characteristics such as body size variously been implicated (Barnosky et al. 2004). or the presence/absence of a mane in males have been used In eastern Beringia, a Pleistocene landmass consisting of to suggest taxonomic distinctiveness between geographical present-day Alaska and Canada’s Yukon Territory, genetic regions (e.g. Kurtén 1968; Yamaguchi et al. 2004; Sotnikova, and palaeontological data from large mammal populations Nikolskiy 2006). Pleistocene lions in Europe are usually suggest that a key period of change occurred around referred to as spelaea, while North American lions are given 40 000–21 000 bp, in the period before the LGM (Barnes the designation atrox. However, the status of these groups et al. 2002; Guthrie 2003; Shapiro et al. 2004). Due to their as species or subspecies, and their relationships to each worldwide distribution, genetic analyses of Pleistocene other and to extant Panthera remains unclear (e.g. Simpson lions potentially hold key insights into how megafaunal 1941; Kurtén 1985; Harington 1971; Vereshchagin 1971; carnivore populations responded to environmental changes Kurtén & Anderson 1980; Herrington 1986; Groiss 1996; in different regions. Additionally, a better understanding Turner & Antón 1997; Baryshnikov & Boeskorov 2001; Burger of how and when lion populations went extinct is vital for et al. 2004; Sotnikova, Nikolskiy 2006). reconstructing community-level dynamics during the LP, In this study, the first to examine intraspecific diversity which in turn is fundamental for testing hypotheses about in an extinct Pleistocene felid, we investigate the rela- the cause of the end-Pleistocene extinctions. tionships among the putative lion subspecies. This was All Pleistocene and modern lion specimens are assigned carried out by obtaining mitochondrial DNA sequences to the genus Panthera, but there is little consensus as to the from modern and ancient lions. The evolutionary and © 2009 Blackwell Publishing Ltd 1670 R. BARNETT ET AL. demographic history of the sequences is inferred using Bayesian Markov chain Monte Carlo (MCMC) analyses phylogenetic analysis, and the results are interpreted were then performed using beast (Drummond & Rambaut in the context of environmental changes in the late 2007), first for HVR1 and ATP8 data sets separately, and Pleistocene. then for a smaller, combined analysis consisting of only those samples from which both sequence fragments could be amplified and which were associated with finite radio- Materials and methods carbon dates. For all three data sets, comparison of Akaike More than 200 cortical bone samples were obtained from information criterion scores suggested the HKY85 model museum specimens of modern, Pleistocene, and American of nucleotide substitution. Each beast analysis assumed lions (Table S1, Supporting information). Specimens ranged this substitution model as well as a constant population in age from modern to > 62 000 years. To prevent duplicate size and a strict molecular clock calibrated using the age sampling within a site, either the same skeletal element or of the split between the spelaea and leo groups (with a nor- samples associated with widely separated radiocarbon mal prior mean of 550 000 years, standard deviation 25 000 dates were chosen. DNA extraction was performed as years), based on the first appearance of Panthera leo fossilis described in Barnett et al. (2006) in dedicated ancient DNA (Garcia Garcia 2001; Burger et al. 2004). Demographic and (aDNA) facilities at the University of Oxford. Four evolutionary model parameters were then estimated simul- European lions were also extracted and amplified at Mainz taneously along with the phylogeny, with samples drawn University under similarly stringent conditions (Burger from the posterior every 5000 MCMC steps over a total of et al. 2004). One of the cave lions from Mainz (sample 8 in 5 000 000 steps. The first 500 000 steps were discarded as Table 1) was previously analysed for cytochrome b in an burn-in. Acceptable mixing and convergence to stationar- earlier study showing the phylogenetic position of the cave ity were checked using the program Tracer version 1.4 lion among the Panthera cats (Burger et al. 2004). (Rambaut & Drummond 2007). A ~215-bp fragment of the mitochondrial hypervariable region 1 (HVR1) and a 143-bp fragment of ATP8 were Results polymerase chain reaction (PCR) amplified, and cloned, purified, and sequenced following Barnett et al. (2006). DNA was successfully amplified from 38 LP and 14 Strict aDNA protocols were followed, including the use
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