期刊论文详细信息
BMC Evolutionary Biology
Revealing the maternal demographic history of Panthera leo using ancient DNA and a spatially explicit genealogical analysis
Greger Larson3  Jacques Cuisin7  Lars Werdelin4  Richard Sabin9  Ian Barnes5  Simon YW Ho8  Beth Shapiro6  Nobuyuki Yamaguchi1  Ross Barnett2 
[1] Department of Biological and Environmental Sciences, Qatar University, Doha, Qatar;Current Address: Centre for GeoGenetics, København Universitet, The Natural History Museum Øster Voldgade, Copenhagen 5-7 DK-1350, Denmark;Durham Evolution and Ancient DNA, Department of Archaeology, Durham University, Durham DH1 3LE, UK;Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, Stockholm SE-10405, Sweden;School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, UK;Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 95064, USA;Muséum National d’Histoire Naturelle, 54 Rue Cuvier, Paris 75005, France;School of Biological Sciences, University of Sydney, Sydney, NSW 2006, Australia;Department of Life Science, Natural History Museum, Cromwell Road, London SW7 5BD, UK
关键词: Phylogeography;    Ancient DNA;    Mitochondrial DNA;    Extinction;    Panthera leo;    Barbary lion;   
Others  :  1084790
DOI  :  10.1186/1471-2148-14-70
 received in 2013-12-18, accepted in 2014-03-13,  发布年份 2014
PDF
【 摘 要 】

Background

Understanding the demographic history of a population is critical to conservation and to our broader understanding of evolutionary processes. For many tropical large mammals, however, this aim is confounded by the absence of fossil material and by the misleading signal obtained from genetic data of recently fragmented and isolated populations. This is particularly true for the lion which as a consequence of millennia of human persecution, has large gaps in its natural distribution and several recently extinct populations.

Results

We sequenced mitochondrial DNA from museum-preserved individuals, including the extinct Barbary lion (Panthera leo leo) and Iranian lion (P. l. persica), as well as lions from West and Central Africa. We added these to a broader sample of lion sequences, resulting in a data set spanning the historical range of lions. Our Bayesian phylogeographical analyses provide evidence for highly supported, reciprocally monophyletic lion clades. Using a molecular clock, we estimated that recent lion lineages began to diverge in the Late Pleistocene. Expanding equatorial rainforest probably separated lions in South and East Africa from other populations. West African lions then expanded into Central Africa during periods of rainforest contraction. Lastly, we found evidence of two separate incursions into Asia from North Africa, first into India and later into the Middle East.

Conclusions

We have identified deep, well-supported splits within the mitochondrial phylogeny of African lions, arguing for recognition of some regional populations as worthy of independent conservation. More morphological and nuclear DNA data are now needed to test these subdivisions.

【 授权许可】

   
2014 Barnett et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150113164336678.pdf 826KB PDF download
20150226230559565.pdf 225KB PDF download
Figure 2. 44KB Image download
Figure 1. 65KB Image download
【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】
  • [1]Mellows A, Barnett R, Dalen L, Sandoval-Castellanos E, Linderholm A, McGovern TH, Church MJ, Larson G: The impact of past climate change on genetic variation and population connectivity in the Icelandic arctic fox. Proc Biol Sci 2012, 279(1747):4568-4573.
  • [2]Dalén L, Nyström V, Valdiosera C, Germonpre M, Sablin M, Turner E, Angerbjörn A, Arsuaga JL, Götherstrom A: Ancient DNA reveals lack of postglacial habitat tracking in the arctic fox. Proc Natl Acad Sci U S A 2007, 104(16):6726-6729.
  • [3]Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK: Considering evolutionary processes in conservation biology. Trends Ecol Evol 2000, 15(7):290-295.
  • [4]Lorenzen ED, Nogues-Bravo D, Orlando L, Weinstock J, Binladen J, Marske KA, Ugan A, Borregaard MK, Gilbert MT, Nielsen R, Ho SYW, Goebel T, Graf KE, Byers D, Stenderup JT, Rasmussen M, Campos PF, Leonard JA, Koepfli KP, Froese D, Zazula G, Stafford TW Jr, Aaris-Sorensen K, Batra P, Haywood AM, Singarayer JS, Valdes PJ, Boeskorov G, Burns JA, Davydov SP, et al.: Species-specific responses of Late Quaternary megafauna to climate and humans. Nature 2011, 479(7373):359-364.
  • [5]Lorenzen ED, Heller R, Siegismund HR: Comparative phylogeography of African savannah ungulates. Mol Ecol 2012, 21(15):3656-3670.
  • [6]Nowell K, Jackson P: Wild Cats: Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/SSC Cat Specialist Group; 1996.
  • [7]Mills G, Hofer H: Hyaenas: Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/SSC Hyaena Specialist Group; 1998.
  • [8]Servheen C, Herrero S, Peyton B: Bears: Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/SSC Bear Specialise Group IUCN/SSC Polar Bear Specialist Group; 1999.
  • [9]Sillero-Zubri C, Hoffmann M, Macdonald DW: Canids: Foxes, Wolves, Jackals And Dogs: Status Survey and Conservation Action Plan. Gland, Switzerland and Cambridge, UK: IUCN/SSC Dog Specialist Group; 2004.
  • [10]Ramakrishnan U, Hadly EA: Using phylochronology to reveal cryptic population histories: review and synthesis of 29 ancient DNA studies. Mol Ecol 2009, 18:1310-1330.
  • [11]de Bruyn M, Hoelzel AR, Carvalho GR, Hofreiter M: Faunal histories from Holocene ancient DNA. Trends Ecol Evol 2011, 26:405-413.
  • [12]Miller CR, Waits LP, Joyce P: Phylogeography and mitochondrial diversity of extirpated brown bear (Ursus arctos) populations in the contiguous United States and Mexico. Mol Ecol 2006, 15:4477-4485.
  • [13]Calvignac S, Hughes S, Tougard C, Michaux JR, Thevenot M, Philippe M, Hamdine W, Hanni C: Ancient DNA evidence for the loss of a highly divergent brown bear clade during historical times. Mol Ecol 2008, 17:1962-1970.
  • [14]Yamaguchi N, Cooper A, Werdelin L, MacDonald DW: Evolution of the mane and group-living in the lion (Panthera leo): a review. J Zool 2004, 263:329-342.
  • [15]Turner A, Antón M: The Big Cats and Their Fossil Relatives. New York: Columbia University Press; 1997.
  • [16]Bauer H, Van Der Merwe S: Inventory of free-ranging lions Panthera leo in Africa. Oryx 2004, 38(1):26-31.
  • [17]Schnitzler AE: Past and present distribution of the North African-Asian lion subgroup: a review. Mammal Rev 2011, 41(3):220-243.
  • [18]IUCN Red List of Threatened Species [http://www.iucnredlist.org webcite]
  • [19]Barnett R, Yamaguchi N, Barnes I, Cooper A: Lost populations and preserving genetic diversity in the lion Panthera leo: Implications for its ex situ conservation. Conserv Genet 2006, 7(4):507-514.
  • [20]Bertola LD, van Hooft WF, Vrieling K, Uit de Weerd DR, York DS, Bauer H, Prins HHT, Funston PJ, de Haes HA U, Leirs H, van Haeringen WA, Sogbohossou Tumenta EPN, de Iongh HH: Genetic diversity, evolutionary history and implications for conservation of the lion (Panthera leo) in West and Central Africa. J Biogeography 2011, 38(7):1356-1367.
  • [21]Henschel P, Azani D, Burton C, Malanda G, Saidu Y, Sam M, Hunter L: Lion status updates from five range countries in West and Central Africa. Cat News 2010, 52(Spring):34-39.
  • [22]Mace GM: The role of taxonomy in species conservation. Trans R Soc B 2004, 359(1444):711-719.
  • [23]Barnett R, Yamaguchi N, Barnes I, Cooper A: The origin, current diversity, and future conservation of the modern lion (Panthera leo). Proc R Soc Lond B 2006, 273(1598):2159-2168.
  • [24]Barnett R, Shapiro B, Barnes I, Ho SYW, Burger J, Yamaguchi N, Higham TFG, Wheeler HT, Rosendahl W, Sher A, Sotnikova M, Kuznetsova T, Baryshnikov G, Martin LD, Harington CR, Burns JA, Cooper A: Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and late Pleistocene reduction in genetic diversity. Mol Ecol 2009, 18(8):1668-1677.
  • [25]Yamaguchi N, Kitchener AC, Driscoll CA, Macdonald DW: Divided infraorbital foramen in the lion (Panthera leo): its implications for colonisation history, population bottlenecks, and conservation of the Asian lion (P.l.persica). Contrib Zoology 2009, 78(2):77-83.
  • [26]Mazak JH: Geographical variation and phylogenetics of modern lions based on craniometric data. J Zoology 2010, 281(3):194-209.
  • [27]Dubach J, Patterson BD, Briggs MB, Venzke K, Flamand J, Stander P, Scheepers L, Kays RW: Molecular genetic variation across the southern and eastern ranges of the African lion, Panthera leo. Conserv Genet 2005, 6:15-24.
  • [28]Antunes A, Troyer JL, Roelke ME, Pecon-Slattery J, Packer C, Winterbach C, Winterbach H, Hemson G, Frank L, Stander P, Siefert L, Driciru M, Funston PJ, Alexander KA, Prager KC, Mills G, Wildt D, Bush M, O'Brien SJ, Johnson WE: The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics. PLoS Genet 2008, 4(11):e1000251.
  • [29]Dubach JM, Briggs MB, White PA, Ament BA, Patterson BD: Genetic perspectives on “Lion Conservation Units” in Eastern and Southern Africa. Conserv Genet 2013, 14(4):741-755.
  • [30]Hemmer H: Untersuchungen zur Stammesgeschichte der Pantherkatzen (Pantherinae), Teil III: Zur Artgeschichte des Löwen Panthera (Panthera) leo (Linnaeus 1758). Veroffentlichungen der Zoologischen Staatssammlung Munchen 1974, 17:167-280.
  • [31]Black S, Yamaguchi N, Harland A, Groombridge J: Maintaining the genetic health of putative Barbary lions in captivity: an analysis of Moroccan Royal Lions. Eur J Wildl Res 2009, 56:21-31.
  • [32]Edwards CJ, Suchard MA, Lemey P, Welch JJ, Barnes I, Fulton TL, Barnett R, O’Connell TC, Coxon P, Monaghan N, Valdiosera CE, Lorenzen ED, Willerslev E, Baryshnikov GF, Rambaut A, Thomas MG, Bradley DG, Shapiro B: Multiple hybridizations between ancient brown and polar bears and an Irish origin for the modern polar bear matriline. Curr Biol 2011, 21:1251-1258.
  • [33]Barnett R, Yamaguchi N, Shapiro B, Sabin R: Ancient DNA analysis indicates the first English lions originated from North Africa. Contrib Zoology 2008, 77(1):7-16.
  • [34]Rohland N, Hofreiter M: Ancient DNA extraction from bones and teeth. Nat Protoc 2007, 2(7):1756-1762.
  • [35]Burger J, Rosendahl W, Loreille O, Hemmer H, Eriksson T, Götherstrom A, Hiller J, Collins MJ, Wess T, Alt KW: Molecular phylogeny of the extinct cave lion Panthera leo spelaea. Mol Phylogenet Evol 2004, 30(3):841-849.
  • [36]Davis BW, Li G, Murphy WJ: Supermatrix and species tree methods resolve phylogenetic relationships amoung the big cats, Panthera (Carnivora: Felidae). Mol Phylogenet Evol 2010, 56(1):64-76.
  • [37]Kim J-H, Antunes A, Luo S-J, Menninger J, Nash WG, O’Brien SJ, Johnson WE: Evolutionary analysis of a large mtDNA translocation (numt) into the nuclear genome of the Panthera genus species. Gene 2006, 366(2):292-302.
  • [38]Rambaut A: Se-Al: Sequence Alignment Editor v2.0a11 Carbon. Oxford: University of Oxford; 1996.
  • [39]Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
  • [40]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29(8):1969-1973.
  • [41]Luo A, Qiao H, Zhang Y, Shi W, Ho SYW, Xu W, Zhang A, Zhu C: Performance criteria for selecting evolutionary models in phylogenetics: a comprehensive study based on simulated datasets. BMC Evol Biol 2010, 10:242. BioMed Central Full Text
  • [42]Sheng G-L, Soubrier J, Liu J, Werdelin L, Llamas B, Thomson VA, Tuke J, Wu L-J, Hou X-D, Chen Q-J, Lai X, Cooper A: Pleistocene Chinese cave hyenas and the recent Eurasian history of the spotted hyena, Crocuta Crocuta. Mol Ecol 2013, 23(3):522-533.
  • [43]Shapiro B, Ho SYW: Ancient hyenas highlight the old problem of estimating evolutionary rates. Mol Eco 2014, 23(3):499-501.
  • [44]Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A: Time-dependent rates of molecular evolution. Mol Ecol 2011, 20(15):3087-3101.
  • [45]Ho SYW, Lanfear R, Phillips MJ, Barnes I, Thomas JA, Kolokotronis S, Shapiro B: Bayesian estimation of substitution rates from ancient DNA sequences with low information content. Syst Biol 2011, 60(3):366-375.
  • [46]García García N: Los Carnivoros de los Yacimientos Pleistocenos de la Sierra de Atapuerca. In Tésis Doctoral Madrid. Spain: Universidad Complutense de Madrid; 2001.
  • [47]Suchard MA, Weiss RE, Sinsheimer JS: Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 2001, 18:1001-1013.
  • [48]Rambaut A, Drummond AJ: Tracer v1.5. 1.5 edn; 2009. http://tree.bio.ed.ac.uk/software/tracer/ webcite
  • [49]Minin VN, Bloomquist EW, Suchard MA: Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol 2008, 25:1459-1471.
  • [50]Gilbert MTP, Bandelt H-J, Hofreiter M, Barnes I: Assessing ancient DNA studies. Trends Ecol Evol 2005, 20(10):541-544.
  • [51]Dupont L: Orbital scale vegetation change in Africa. Quaternary Sci Rev 2011, 30(25–26):3589-3602.
  • [52]De Vivo M, Carmignotto AP: Holocene vegetation change and the mammal faunas of South America and Africa. J Biogeography 2004, 31:943-957.
  • [53]Meadows ME, Chase BM: Pollen Records, Late Pleistocene/Africa. In Encyclopaedia of Quaternary Science. Edited by Elias SA. Elsevier Science Ltd. North Holland; 2007:2606-2613.
  • [54]Cohen AS, Stone JR, Beuning KRM, Park LE, Reinthal PN, Dettmar D, Scholz CA, Johnsor TC, King JW, Talbot MR, Brown ET, Ivory SJ: Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proc Natl Acad Sci U S A 2007, 104(42):16422-16427.
  • [55]Castaneda IS, Mulitza S, Schefuss E, dos Santos RAL, Damste JSS, Schouten S: Wet phases in the Sahara/Sahel region and human migration patterns in North Africa. Proc Natl Acad Sci U S A 2009, 106(48):20159-20163.
  • [56]Blome MW, Cohen AS, Tryon CA, Brooks AS, Russell J: The environmental context for the origins of modern human diversity: A synthesis of regional variability in African climate 150,000-30,000 years ago. J Hum Evol 2012, 62(5):563-592.
  • [57]Osborne AH, Vance D, Rohling EJ, Barton N, Rogerson M, Fello N: A humid corridor across the Sahara for the migration of early modern humans out of Africa 120,000 years ago. Proc Natl Acad Sci U S A 2008, 105(43):16444-16447.
  • [58]Mashkour M, Monchot H, Trinkaus E, Reyss J, Biglari F, Bailon S, Heydari S, Abdi K: Carnivores and their prey in the Wezmeh cave (Kermanshah, Iran): a late Pleistocene refuge in the Zagros. Int J Osteoarchaeology 2008, 19(6):678-694.
  • [59]Tchernov E, Tsoukala E: Middle Pleistocene (Early Toringian) Carnivore Remains from Northern Israel. Quaternary Res 1997, 48:122-136.
  • [60]Eriksson J, Hohmann G, Boesch C, Vigilant L: Rivers influence the population genetic structure of bonobos (Pan paniscus). Mol Ecol 2004, 13(11):3425-3435.
  • [61]Eizirik E, Kim JH, Menotti-Raymond M, Crawshaw PG, O’Brien SJ, Johnson WE: Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol Ecol 2001, 10(1):65-79.
  • [62]Moritz C: Applications of mitochondrial DNA analysis in conservation- a critical review. Mol Ecol 1994, 3:401-411.
  • [63]O’Brien SJ, Martenson JS, Packer C, Herbst L, Devos V, Joslin P, Ottjoslin J, Wildt DE, Bush M: Biochemical Genetic-Variation in Geographic Isolates of African and Asiatic Lions. Natl Geographic Res 1987, 3(1):114-124.
  • [64]O’Brien SJ, Joslin P, Smith GL III, Wolfe R, Schaffer N, Heath E, Ott-Joslin J, Rawal PP, Bhattacharjee KK, Martenson JS: Evidence for African origins of founders if the asiatic lion species survival plan. Zoo Biol 1987, 6:99-116.
  • [65]Bauer H, de Iongh HH, Princee FPG, Ngantou D: Research needs for lion conservation in West and Central Africa. C R Biologies 2003, 326:S112-S118.
  • [66]Bauer H, Nowell K, Breitenmoser C, Breitenmoser U, Jackson P: Endangered classification for West African lions. Cat News 2004, 41:35-36.
  • [67]Yamaguchi N, Haddane B: The North African Barbary lion and the Atlas Lion Project. Int Zoo News 2002, 49:465-481.
  • [68]Burger J, Hemmer H: Urgent call for further breeding of the relic zoo population of the critically endangered Barbary lion (Panthera leo leo Linnaeus 1758). Eur J Wildl Res 2006, 52:54-58.
  • [69]Driscoll CA, Yamaguchi N, Bar-Gal GK, Roca AL, Luo S, Macdonald DW, O’Brien SJ: Mitochondrial phylogeography illuminates the origin of the extinct Caspian tiger and its relationship to the Amur tiger. PLoS One 2009, 4(1):e4125.
  • [70]Jungius H: Feasibility Study on the Possible Restoration of the Caspian Tiger in Central Asia. WWF; 2010. http://www.wwf.ru/resources/publ/book/eng/460 webcite
  • [71]Tigers could reappear in Kazakhstan under new plan http://wwf.panda.org/?uNewsID=200017 webcite
  • [72]Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) v4.0b10. Sunderland, Massachusetts: Sinauer Associates; 2002.
  • [73]Cracraft J, Feinstein J, Vaughn J, Helm-Bychowski K: Sorting out tiger (Panthera tigris): mitochondrial sequences, nuclear inserts, systematics, and conservation genetics. Anim Conserv 1998, 1:139-150.
  文献评价指标  
  下载次数:25次 浏览次数:13次