Mitochondrial sequences reveal a clear separation between Angolan and South African giraffe along a cryptic rift valley

BMC Evolutionary Biology

Axel Janke³  Francois Deacon²  Andri Marais⁵  Andy Tutchings⁵  Tobias Bidon⁴  Julian Fennessy¹  Friederike Bock⁴ 

[1] School of Biological Earth and Environmental Studies (BEES), University of New South Wales (UNSW), Sydney 2052, New South Wales, Australia;Department Animal, Wildlife & Grassland Science, University of Free State, Faculty of Natural and Agricultural Sciences, Bloemfontein, South Africa;Goethe University Frankfurt, Institute for Ecology, Evolution & Diversity, Biologicum, Max-von-Laue-Straße 13, Frankfurt am Main, 60439, Germany;Biodiversity and Climate Research Centre (BiK-F) – Ecological Genomics & Senckenberg Gesellschaft für Naturforschung (SGN), Senckenberganlage 25, Frankfurt am Main, 60325, Germany;Giraffe Conservation Foundation, 26 Grasmere Road, Purley, Surrey CR8 1DU, England

关键词: mtDNA;    Phylogeny;    Namibia;    Botswana;    Population genetics;    South African giraffe;    Angolan giraffe;    Giraffa;   

Others  :  1117876
DOI  :  10.1186/s12862-014-0219-7

 received in 2014-09-26, accepted in 2014-10-03,  发布年份 2014

【 摘 要 】

Background

The current taxonomy of the African giraffe (Giraffa camelopardalis) is primarily based on pelage pattern and geographic distribution, and nine subspecies are currently recognized. Although genetic studies have been conducted, their resolution is low, mainly due to limited sampling. Detailed knowledge about the genetic variation and phylogeography of the South African giraffe (G. c. giraffa) and the Angolan giraffe (G. c. angolensis) is lacking. We investigate genetic variation among giraffe matrilines by increased sampling, with a focus on giraffe key areas in southern Africa.

Results

The 1,562 nucleotides long mitochondrial DNA dataset (cytochrome b and partial control region) comprises 138 parsimony informative sites among 161 giraffe individuals from eight populations. We additionally included two okapis as an outgroup. The analyses of the maternally inherited sequences reveal a deep divergence between northern and southern giraffe populations in Africa, and a general pattern of distinct matrilineal clades corresponding to their geographic distribution. Divergence time estimates among giraffe populations place the deepest splits at several hundred thousand years ago.

Conclusions

Our increased sampling in southern Africa suggests that the distribution ranges of the Angolan and South African giraffe need to be redefined. Knowledge about the phylogeography and genetic variation of these two maternal lineages is crucial for the development of appropriate management strategies.

【 授权许可】

   
2014 Bock et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Fennessy JT: Ecology of desert-dwelling giraffeGiraffa camelopardalis angolensisin northwestern Namibia. In PhD thesis. University of Sydney; 2004.
• [2]Fennessy J: An overview of Giraffe Giraffa camelopardalis taxonomy, distribution and conservation status, with a Namibian comparative and focus on the Kunene Region, Namibia. J Namib Sci Soc 2008, 56:1-16.
• [3]Brisson MJ: ᅟRegnum animale in classes IX. distributum, sive synopsis methodica sistens generalem Animalium distributionem in classes IX, & duarum primarum classium, Quadrupedum scilicet & Cetaceorum, particularem divisionem in Ordines, Sectiones, Genera & Species. Cum brevi cujusque Speciei Descriptione, Citationibus Auctorum de iis tractantium, Nominibus eis ab ipsis & Nationibus impositis, Nominibusque vulgaribus. Lugduni Baravorum: Apud Theodorum Haak; 1762.
• [4]Mitchell G, Skinner JD: On the origin, evolution and phylogeny of giraffes Giraffa camelopardalis. Trans Roy Soc S Afr 2003, 58(1):51-73.
• [5]Lydekker R: On the subspecies of Giraffa camelopardalis. Proc Zool Soc Lond 1904, 74(1):202-229.
• [6]Dagg AI, Foster JB: The Giraffe: Its Biology, Behavior and Ecology. Krieger Publishing Company, Malabar; 1982.
• [7]Fennessy J, Brown D: Giraffa camelopardalis. [http://www.iucnredlist.org/details/9194/0] webciteIUCN Red List of Threatened Species. Version 2014.2 2010. http://www.iucnredlist.org/details/9194/0
• [8]Groves C, Grubb P: Ungulate taxonomy. John Hopkins University Press, Baltimore; 2011.
• [9]Brown DM, Brenneman R, Koepfli KP, Pollinger J, Mila B, Louis EE Jr, Georgiadis N, Grether G, Wayne RK: Extensive population genetic structure in the giraffe. BMC Biol 2007, 5:57-70. BioMed Central Full Text
• [10]Hassanin A, Ropiquet A, Gourmand AL, Chardonnet B, Rigoulet J: Mitochondrial DNA variability in Giraffa camelopardalis: consequences for taxonomy, phylogeography and conservation of giraffes in West and central Africa. C R Biol 2007, 330:265-274.
• [11]Fennessy J, Bock F, Tutchings A, Brenneman R, Janke A: Mitochondrial DNA analyses show that Zambia’s South Luangwa Valley giraffe (Giraffa camelopardalis thornicrofti) is genetically isolated. Afr J Ecol 2013, 51(4):635-640.
• [12]Roca AL, Georgiadis N, O’Brien SJ: Cytonuclear genomic dissociation in African elephant species. Nat Genet 2005, 37(1):96-100.
• [13]Brandt AL, Hagos Y, Yacob Y, David VA, Georgiadis NJ, Shoshani J, Roca AL: The elephants of Gash-Barka, Eritrea: Nuclear and mitochondrial genetic patterns. J Hered 2014, 105(1):82-90.
• [14]Arctander P, Johansen C, Coutellec-Vreto MA: Phylogeography of three closely related African bovids (tribe Alcelaphini). Mol Biol Evol 1999, 16(12):1724-1739.
• [15]Osmers B, Petersen BS, Hartl HB, Grobler JB, Kotze A, Van Aswegen E, Zachos FE: Genetic analysis of southern African gemsbok (Oryx gazella) reveals high variability, distinct lineages and strong divergence from the East African Oryx beisa. Mamm Biol 2012, 11(1):60-66.
• [16]Brenneman RA, Louis EE Jr, Fennessy J: Genetic structure of two populations of the Namibian giraffe, Giraffa camelopardalis angolensis. Afr J Ecol 2009, 47(4):720-728.
• [17]Community conservation in Namibia: a review of communal conservancies, community forests and other CBNRM initiatives. NACSO, Windhoek; 2012.
• [18]Chase M: Dry season fixed-wing aerial survey of elephants and wildlife in northern Botswana. Elephants Without Borders, Kasane, Botswana; 2011.
• [19]Game Count in Bwabwata National Park. Unpublished Data, Windhoek; 2012.
• [20]Moore AE: A reappraisal of epeirogenic flexure axes in southern Africa. S Afr J Geol 1999, 102:363-376.
• [21]Moore AE, Cotterill FPD, Eckardt FD: The evolution and ages of Makgadikgadi palaeo-lakes: consilient evidence from Kalahari drainage evolution. S Afr J Geol 2012, 115:385-413.
• [22]Fennessy J, Brenneman R: Giraffa camelopardalis ssp. rothschildi. [http://www.iucnredlist.org/details/174469/0] webciteIUCN Red List of Threatened Species. Version 2014.2 2010. http://www.iucnredlist.org/details/174469/0
• [23]Petit RJ, Excoffier L: Gene flow and species delimitation. Trends Ecol Evol 2009, 24(7):386-393.
• [24]Funk DJ, Omland KE: Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 2003, 34:397-423.
• [25]Part 5: Order Artiodactyla, Suborder: Ruminatia, Infraorder: Pecora, Family: Giraffidae, Genus: Giraffa Trans Zool Soc London 1965, 30:139-168.
• [26]Zink RM, Barrowclough GF: Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 2008, 17(9):2107-2121.
• [27]Harris JM: Family Giraffidae, Koobi Fora Research Project. In The Fossil Ungulates: Geology, Fossil Artiodactyls, and Palaeoenvironments. Clarendon Press, Oxford; 1991:93-138. [Harris JM (Series Editor): The Fossil Ungulates: Geology, Fossil Artiodactyls, and Palaeoenvironments, vol 3]
• [28]Hailer F, Kutschera VE, Hallström BM, Klassert D, Fain SR, Leonard JA, Arnason U, Janke A: Nuclear Genomic Sequences Reveal that Polar Bears Are an Old and Distinct Bear Lineage. Science 2012, 336(6079):344-347.
• [29]Won YJ, Hey J: Divergence Population Genetics of Chimpanzees. Mol Biol Evol 2005, 22:297-307.
• [30]Perini FA, Russo CAM, Schrago CG: The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism. J Evol Biol 2010, 23(2):311-322.
• [31]Pamilo P, Nei M: Relationships between gene trees and species trees. Mol Biol Evol 1988, 5(5):568-583.
• [32]Vrba ES: The fossil record of African antelopes (Mammalia, Bovidae) in relation to human evolution and paleoclimate. In Paleoclimate and Evolution with emphasis on Human Origins. 1005 edition. Edited by Vrba ES, Denton GH, Partridge TC, Burckle LH. Yale University Press, New Haven; 1995:385-424.
• [33]Lorenzen ED, Heller R, Siegismund HR: Comparative phylogeography of African savannah ungulates. Mol Ecol 2012, 21:3656-3670.
• [34]Leblanc MJ, Leduc C, Stagnitti F, Van Oevelen PJ, Jones C, Mofor LA, Razack M, Favreau G: Evidence for Megalake Chad, north-central Africa, during the Late Quaternary from satellite data. Palaeogeogr Palaeoclimatol Palaeoecol 2006, 230:230-242.
• [35]Ciofolo I, Le Pendu Y: Seasonal movements of giraffe in Niger. J Trop Ecol 1999, 15(3):341-353.
• [36]Cotterill FPD: The evolutionary history and taxonomy of theKobus lechespecies complex of south-central Africa in the context of palaeo-drainage dynamics. In PhD thesis. University of Stellenbosch; 2006.
• [37]Mvondo F, Dauteuil O, Guillocheau F: The Fish River canyon (Southern Namibia): A record of Cenozoic mantle dynamics? C R Geoscience 2011, 343:478-485.
• [38]Lorenzen ED, Siegismund HR: No suggestion of hybridization between the vulnerable black-faced impala (Aepyceros melampus petersi) and the common impala (A. m. melampus) in Etosha National Park, Namibia. Mol Ecol 2004, 13(10):3007-3019.
• [39]Plowman A (Ed): Geomorphological influences on vicariant evolution in some African mammals in the Zambezi basin: some lessons for conservation In Proceedings of an International Symposium on Duiker and Dwarf Antelope in Africa. Fürth, Filander Verlag; 2003:11-58.
• [40]Vrba ES (Ed): The recognition concept of species In Species and speciation. Transvaal Museum Monograph, Pretoria; 1985:21-29.
• [41]Pusey A: Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 1987, 2:295-299.
• [42]Bidon T, Janke A, Fain SR, Eiken HG, Hagen SB, Saarma U, Hallström BM, Lecomte N, Hailer F: Brown and polar bear Y chromosome reveal extensive male-biased gene flow within brother lineages. Mol Biol Evol 2014, 31(6):1353-1363.
• [43]Toews DP, Brelsford A: The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 2012, 21(16):3907-3930.
• [44]Seutin G, White BN, Boag PT: Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 1991, 69:82-90.
• [45]Sambrook J, Fritch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York; 1989.
• [46]Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen Van Vuuren V, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A: Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasitheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 2012, 335:32-50.
• [47]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882.
• [48]Clement M, Posada D, Crandall K: TCS: a computer program to estimate gene genealogies. Mol Ecol 2000, 9(10):1657-1660.
• [49]Librado P, Rozas J: DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [50]Excoffier L, Lischer HEL: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 2010, 10:564-567.
• [51]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.
• [52]Jobb G, Von Haeseler A, Strimmer K: TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics.BMC Evol Biol 2004, 4:18.
• [53]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing.Nature Methods 2012, 9(8):772.