First insights into past biodiversity of giraffes based on mitochondrial sequences from museum specimens

  • Alice Petzold Institut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, MNHN, CNRS, EPHE, UA, Muséum national d’histoire naturelle, 55 rue Buffon - CP 51 - 75005 Paris
  • Anne-Sophie Magnant Institut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, MNHN, CNRS, EPHE, UA, Muséum national d’histoire naturelle, 55 rue Buffon - CP 51 - 75005 Paris
  • David Edderai 5 chemin du bas d’Anville - 17750 Etaules
  • Bertrand Chardonnet 92210 Saint Cloud
  • Jacques Rigoulet Direction Générale Déléguée aux Musées, Jardins Botaniques et Zoologiques, Muséum national d’histoire naturelle, 57 rue Cuvier - 75005 Paris
  • Michel Saint-Jalme Centre d’Ecologie et des Sciences de la Conservation, UMR 7204 MNHN CNRS-UPMC, Muséum national d’histoire naturelle - 75005 Paris
  • Alexandre Hassanin Institut de Systématique, Évolution, Biodiversité (ISYEB), Sorbonne Université, MNHN, CNRS, EPHE, UA, Muséum national d’histoire naturelle, 55 rue Buffon - CP 51 - 75005 Paris http://orcid.org/0000-0002-4905-8540
Keywords: Giraffa, ancient DNA, Zarafa, conservation genetics, Pleistocene

Abstract

Intensified exploration of sub-Saharan Africa during the 18th and 19th centuries led to many newly described giraffe subspecies. Several populations described at that time are now extinct, which is problematic for a full understanding of giraffe taxonomy. In this study, we provide mitochondrial sequences for 41 giraffes, including 19 museum specimens of high importance to resolve giraffe taxonomy, such as Zarafa from Sennar and two giraffes from Abyssinia (subspecies camelopardalis), three of the first southern individuals collected by Levaillant and Delalande (subspecies capensis), topotypes of the former subspecies congoensis and cottoni, and giraffes from an extinct population in Senegal. Our phylogeographic analysis shows that no representative of the nominate subspecies camelopardalis was included in previous molecular studies, as Zarafa and two other specimens assigned to this taxon are characterized by a divergent haplogroup, that the former subspecies congoensis and cottoni should be treated as synonyms of antiquorum, and that the subspecies angolensis and capensis should be synonymized with giraffa, whereas the subspecies wardi should be rehabilitated. In addition, we found evidence for the existence of a previously unknown subspecies from Senegal (newly described in this study), which is now extinct. Based on these results, we propose a new classification of giraffes recognizing three species and 10 subspecies. According to our molecular dating estimates, the divergence among these taxa has been promoted by Pleistocene climatic changes resulting in either savannah expansion or the development of hydrographical networks (Zambezi, Nile, Lake Chad, Lake Victoria).

A correction has been published: Petzold A., Magnant A.-S., Edderai D., Chardonnet B., Rigoulet J., Saint-Jalme M. & Hassanin A. 2020. First insights into past biodiversity of giraffes based on mitochondrial sequences from museum specimens – Corrigendum. European Journal of Taxonomy 717: 1–2. https://doi.org/10.5852/ejt.2020.717.1093

References

Allin M. 1999. Zarafa: a Giraffe’s True Story, from Deep in Africa to the Heart of Paris. Walker and Co., New York.

Ansell W.F.H. 1968. Artiodactyla (Excluding the Genus Gazella). In: Meester J.A. (ed.) Preliminary Identification Manual for African Mammals: 152–160. Smithsonian Institution, Washington.

Baker R.J. & Bradley R.D. 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87: 643–662. https://doi.org/10.1644/06-MAMM-F-038R2.1

Baker S.W. 1880. Exploration du Haut Nil: récit d’un Voyage dans l’Afrique centrale. Librairie Hachette, Paris.

Bandelt H.J., Forster P. & Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16 (1): 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Baum D.A. & Shaw K.L. 1995. Genealogical perspectives on the species problem. In: Hoch P.C. & Stephenson A.G. (eds) Experimental and Molecular Approaches to Plant Biosystematics: 289–303. Missouri Botanical Garden, Saint Louis.

Belon du Mans P. 1553. Les Observations de plusieurs Singularitez et Choses memorables trouvees en Grece, Asie, Iudée, Egypte, Arabie et autres Pays estranges. Corrozet et Canellat, Paris. https://doi.org/10.5962/bhl.title.127374

Bercovitch F.B. & Berry P.S. 2010. Ecological determinants of herd size in the Thornicroft’s giraffe of Zambia. African Journal of Ecology 48 (4): 962–971. https://doi.org/10.1111/j.1365-2028.2009.01198.x

de Blainville H.M.D. 1864. Ostéographie: ou, Description iconographique comparée du Squelette et du Système dentaire des Mammifères récents et fossiles pour servir de base à la Zoologie et à la Géologie. Vol. 4: Quaternatès. JB Baillière et fils, Paris.

Bock F., Fennessy J., Bidon T., Tutchings A., Marais A., Deacon F. & Janke A. 2014. Mitochondrial sequences reveal a clear separation between Angolan and South African giraffe along a cryptic rift valley. BMC Evolutionary Biology 14 (1): 219. https://doi.org/10.1186/s12862-014-0219-7

Boddaert P. 1784. Camelopardalis giraffa. Elenchus Animalium Vol. 1: Systems Quadrupedia. C.R. Hake, Rotterdam.

Bostock J. & Riley H.T. 1855. Pliny the Elder: The Natural History. Taylor and Francis, London.

Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C.H., Xie D., Suchard M.A., Rambaut A. & Drummond A.J. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10 (4): e1003537. https://doi.org/10.1371/journal.pcbi.1003537

Brisson M.J. 1762. Regnum Animale in Classes IX.: Distributum, sive Synopsis methocica: Sistens generalem Animalium distributionem in Classes IX, & duarum primarum Classium, Quadrupedum scilicet & Cetaceorum, particularem divisionem in Ordines, Sectiones, Genera & Species. Theodorum Haak, Leiden. https://doi.org/10.5962/bhl.title.40361

Brown D.M., Brenneman R.A., Koepfli K.P., Pollinger J.P., Milá B., Georgiadis N.J., Edward Jr. E.L., Grether G.F., Jacobs D.K. & Wayne R.K. 2007. Extensive population genetic structure in the giraffe. BMC Biology 5 (1): 57. https://doi.org/10.1186/1741-7007-5-57

Bryden H.A. 1899. Great and Small Game of Africa: An Account of the Distribution, Habits, and Natural History of the Sporting Mammals, with Personal Hunting Experiences. R. Ward, London.

Ciofolo I. & Le Pendu Y. 2013. Giraffa camelopardalis. In: Kingdon J. & Hoffman M. (eds) Mammals of Africa. Vol. 6: Pigs, Hippopotamuses, Chevrotain, Giraffes, Deer and Bovids: 98–110. Bloomsbury Publishing, London.

Combes E. & Tamisier M. 1838. Voyage en Abyssinie, dans les Pays des Galla, de Choa et d’ifat, précédé d’une Excursion dans l’Arabie-Heureuse et accompagné d’une de ces diverses contrées. L. Dessart, Paris.

Dagg A.I. 1962. The subspeciation of the giraffe. Journal of Mammalogy 43 (4): 550–552. https://doi.org/10.2307/1376925

Dagg A.I. 1971. Giraffa camelopardalis. Mammalian Species 5: 1–8. https://doi.org/10.2307/3503830

Dagg A.I. & Foster J.B. 1976. The Giraffe: its Biology, Behaviour, and Ecology. Van Nostrand Reinhold Company, New York.

Dagg A.I. 2014. Giraffe: Biology, Behaviour and Conservation. Cambridge University Press, Cambridge.

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature methods 9 (8): 772–772. https://doi.org/10.1038/nmeth.2109

Delalande P.A. 1822. Précis d’un Voyage au cap de Bonne-Esperance : fait par ordre du Gouvernement. A. Belin, Paris.

Donoghue M.J. 1985. A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 1985: 172–181.

Drummond A.J., Suchard M.A., Xie D. & Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29 (8): 1969–1973. https://doi.org/10.1093/molbev/mss075

Duvernoy M. 1844. Sur une mâchoire de girafe fossile découverte à Issoudun. Notes communiqués au L’Academie de Science, 1843.

East R. 1998. African Antelope Database. IUCN / SSC Antelope Specialist Group, Gland. Available from https://portals.iucn.org/library/efiles/documents/ssc-op-021.pdf [accessed 27 Jul. 2020].

Fennessy J. & Marais A. 2018. Giraffa camelopardalis ssp. antiquorum. The IUCN Red List of Threatened Species 2018: e.T88420742A88420817. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T88420742A88420817.en

Fennessy J., Bock F., Tutchings A., Brenneman R. & Janke A. 2013. Mitochondrial DNA analyses show that Zambia’s South Luangwa Valley giraffe (Giraffa camelopardalis thornicrofti) are genetically isolated. African Journal of Ecology 51 (4): 635–640. https://doi.org/10.1111/aje.12085

Fennessy J., Bidon T., Reuss F., Kumar V., Elkan P., Nilsson M. A., Vamberger M., Fritz U. & Janke A. 2016. Multi-locus analyses reveal four giraffe species instead of one. Current Biology 26 (18): 2543–2549. https://doi.org/10.1016/j.cub.2016.07.036

Fennessy J., Marais A., & Tutchings A. 2018. Giraffa camelopardalis ssp. peralta. The IUCN Red List of Threatened Species 2018: e.T136913A51140803. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T136913A51140803.en

Geoffroy Saint-Hilaire É. 1827. Quelques considérations sur la giraffe. Annales des Sciences naturelles 11: 210–223.

Goudie A.S. 2005. The drainage of Africa since the Cretaceous. Geomorphology 67 (3–4): 437–456. https://doi.org/10.1016/j.geomorph.2004.11.008

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W. & Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59 (3): 307–321. https://doi.org/10.1093/sysbio/syq010

Happold D.C.D. 1969. The present distribution and status of the giraffe in West Africa. Mammalia 33 (3): 516–521. https://doi.org/10.1515/mamm.1969.33.3.516

Happold D.C.D. 1978. Giraffe south of the Niger-Benue River system. Zeitschrift für Säugetierkunde 43 (4): 239–242.

Harris J.M. 1991. The Fossil Ungulates: Geology, Fossil Artiodactyls, and Palaeoenvironments. Clarendon Press, Oxford.

Hassanin A., Ropiquet A., Gourmand A.L., Chardonnet B. & Rigoulet J. 2007. Mitochondrial DNA variability in Giraffa camelopardalis: consequences for taxonomy, phylogeography and conservation of giraffes in West and central Africa. Comptes Rendus Biologies 330 (3): 265–274. https://doi.org/10.1016/j.crvi.2007.02.008

Hassanin A., Delsuc F., Ropiquet A., Hammer C., Van Vuuren B.J., Matthee C., Ruiz-Garcia M., Catzeflis F., Areskoug V., Nguyen T.T. & Couloux A. 2012. Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. Comptes Rendus Biologies 335 (1): 32–50. https://doi.org/10.1016/j.crvi.2011.11.002

Hasselquist F. 1757. Iter Palaestinum eller Resa til Heliga Landet forrattad ifran ar 1749 til 1752. Laurentius Salvius, Stockholm. https://doi.org/10.5962/bhl.title.112563

Henderson D.M. & Naish D. 2010. Predicting the buoyancy, equilibrium and potential swimming ability of giraffes by computational analysis. Journal of Theoretical Biology 265 (2): 151–159. https://doi.org/10.1016/j.jtbi.2010.04.007

Jardine W. 1835. The Natural History of the Ruminating Animals, containing Deer, Antilopes, Camels & c. W. H. Lizars, Edinburgh. https://doi.org/10.5962/bhl.title.131528

Johnson T.C., Kelts K. & Odada E. 2000. The Holocene history of Lake Victoria. Ambio 29 (1): 2–11. https://doi.org/10.1579/0044-7447-29.1.2

Joly N. & Lavocat A. 1845. Recherches historiques, zoologiques, anatomiques et paléontologiques sur la Giraffe (Camelopardalis giraffa, Gmélin). V. Berger-Levrault, Boulogne-Billancourt.

Kingdon J. 1997. The Kingdon Field Guide to African Mammals. Academic Press, London.

Knottnerus-Meyer T. 1910. Eine neue Giraffe aus dem südlichen Abessinien. Zoologischer Anzeiger 35: 797–800.

Leigh J.W. & Bryant D. 2015. PopArt: full‐feature software for haplotype network construction. Methods in Ecology and Evolution 6 (9): 1110–1116. https://doi.org/10.1111/2041-210X.12410

Lesson R.P. 1842. Nouveau tableau du Règne animal: Mammifères. Arthus Bertrand, Paris.

Levaillant F. & de La Borde J.-B. 1790. Partie Méridionale de l’Afrique depuis le Tropique du Capricorne jusqu’au Cap de Bonne Espérance contenant les Pays des Hottentots, des Cafres et de quelques autres Nations. Available from https://gallica.bnf.fr/ark:/12148/btv1b55011014j/f2.item.r=Levaillant%20carte%20meridionale%20de%20l’afrique%20Levaillant [accessed 24 Jul. 2020].

Levaillant F. 1797. Second Voyage dans l’Intérieur de l’Afrique par le Cap de Bonne-Espérance, dans les années 1783–1785 (Vol. 2). B. Le Francq, Bruxelles. https://doi.org/10.5962/bhl.title.125944

Linnaeus C. 1758. Systema Naturae per Regna Tria Naturae. Editio decima reformata, Tomus I. Regnum Animale. Laurentius Salvius, Stockholm.

Lydekker R. 1903. Local variation in the Giraffe. In: Animal Life and the World of Nature. Vol. 2: 78–84. Hutchinson & Co, London.

Lydekker R. 1904. On the Subspecies of Giraffa camelopardalis. Proceedings of the Zoological Society of London 74: 202–227. https://doi.org/10.1111/j.1469-7998.1904.tb08288.x

Lydekker R. 1911. Two undescribed giraffes. Nature 87: 484. https://doi.org/10.1038/087484c0

Lydekker R. 1914. Catalogue of the Ungulate Mammals in the British Museum. British Museum, London.

MacClintock D. 1973. A Natural History of Giraffes. Charles Scribner’s Sons, New York.

Malte-Brun C. & Malte-Brun V.A. 1839. Nouvelles Annales des Voyages. A. Pihan de la Forest, Paris.

Matschie P. 1898. Einige anscheinend noch nicht beschriebene Säugetiere aus Afrika. Sitzungsbericht Gesellschaft Naturforschender Freunde zu Berlin 1898: 75–81.

McCorquodale W.H. 1898. Giraffe from the Niger Territories. Nature 57: 389–390. https://doi.org/10.1038/057389c0

de Menocal P.B. 2004. African climate change and faunal evolution during the Pliocene–Pleistocene. Earth and Planetary Science Letters 220 (1–2): 3–24. https://doi.org/10.1016/S0012-821X(04)00003-2

Moore A.E., Cotterill F.P.D. & Eckardt F.D. 2012. The evolution and ages of Makgadikgadi palaeo-lakes: consilient evidence from Kalahari drainage evolution south-central Africa. South African Journal of Geology 115 (3): 385–413. https://doi.org/10.2113/gssajg.115.3.385

Muller Z., Bercovitch F., Brand R., Brown D., Brown M., Bolger D., Carter K., Deacon F., Doherty J.B., Fennessy J., Fennessy S., Hussein A.A., Lee D., Marais A., Strauss M., Tutchings A. & Wube T. 2018. Giraffa camelopardalis (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2018: e.T9194A136266699. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T9194A136266699.en

Nežerková P., Verner P.H. & Antonínová M. 2004. The conservation programme of the western giant eland (Taurotragus derbianus derbianus) in Senegal–Czech Aid Development Project. Gazella 31: 87–182.

Noack T. 1908. Die Giraffe des Sambesi-Gebietes. Zoologischer Anzeiger 33 (11): 354–356.

Ogilby W. 1837. On the generic characters of ruminants. Proceedings of the Zoological Society of London 1836: 131–139.

Petzold A. & Hassanin A. 2020. A comparative approach for species delimitation based on multiple methods of multi-locus DNA sequence analysis: A case study of the genus Giraffa (Mammalia, Cetartiodactyla). PloS ONE 15 (2): e0217956. https://doi.org/10.1371/journal.pone.0217956

Rambaut A. & Drummond A.J. 2007. TreeAnnotator. Program and documentation distributed by the author. Available from http://beast.bio.ed.ac.uk/TreeAnnotator [accessed 25 Jul. 2020].

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67 (5): 901–904. https://doi.org/10.1093/sysbio/syy032

Ray J. 1693. Synopsis Methodica Animalium quadrupedum et serpentini Generis. Smith & Walford, London.

Rhoads S.N. 1896. Mammals collected by Dr. A. Donaldson Smith during his expedition to Lake Rudolf, Africa. Proceedings of the Academy of Natural Sciences of Philadelphia 1896: 517–546.

Rigoulet J. 2012. Histoire de Zarafa, la girafe de Charles X. Bulletin de l’Académie vétérinaire de France 165: 169–176. https://doi.org/10.4267/2042/48205

Roeder P., Mariner J. & Kock R. 2013. Rinderpest: the veterinary perspective on eradication. Philosophical Transactions of the Royal Society B: Biological Sciences 368 (1623): 20120139. https://doi.org/10.1098/rstb.2012.0139

Rohland N. & Hofreiter M. 2007. Ancient DNA extraction from bones and teeth. Nature Protocols 2 (7): 1756–1762. https://doi.org/10.1038/nprot.2007.247

Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029

Rüppell E. 1826. Atlas zu der Reise im nördlichen Afrika. HL Brönner, Frankfurt am Main. https://doi.org/10.5962/bhl.title.53779

Salze Mr. 1827. Observations faites sur la Girafe envoyée au Roi par le Pacha d’Égypte. Mémoires du Muséum d’histoire naturelle 14: 68–84.

von Schreber J.C.D. 1784. Die Säugthiere in Abbildungen nach der Natur mit Beschreibungen. Palm’sche Verlagsbuchhandlung, Erlangen.

Schickh J. 1828. Wiener-Moden-Zeitung und Zeitschrift für Kunst, schöne Literatur und Theater. Anton Strauß sel. Witwe, Wien.

Shorrocks B. 2016. The Giraffe: Biology, Ecology, Evolution and Behaviour. John Wiley & Sons, New Jersey. https://doi.org/10.1002/9781118587430

Sidney J. 1965. The past and present distribution of some African ungulates. Transactions of the Zoological Society of London 30: 139–168.

Stott K.W. & Selsor C.J. 1981. Further remarks on giraffe intergradation in Kenya and unreported marking variations in reticulated and Masai giraffes. Mammalia 45: 261–263.

Swainson W. 1835. A Treatise on the Geography and Classification of Animals. Green Longman, London. https://doi.org/10.5962/bhl.title.25975

Swofford D.L. 2002. PAUP * Phylogenetic Analysis Using Parsimony (* And Other Methods). ver. 4.0b10. Sinauer Associates, Sunderland.

Thomas O. 1898. On a new subspecies of giraffe from Nigeria. Proceedings Zoological Society London 1898: 39–41.

Trouessart L. 1898. Catalogus Mammalium tam viventium quam fossilium. Vol. 4: Tillodontia et Ungulata. Freidlander, Berlin. https://doi.org/10.5962/bhl.title.130824

Vincke X., Hornick J.L., Njikam N.I. & Leroy P. 2005. Gestion de la faune sauvage au Sénégal: comparaison du Parc national du Niokolo Koba et de la Réserve privée de Bandia. Annales de Médecine vétérinaire 149 (4): 232–237.

Vosmaer A. 1787. Description du chameau-leopard (Camelopardalis). P. Meyer and G. Warners, Amsterdam.

Weinland D.F. 1863. Zur Erinnerung an unsere Giraffe. Zoologischer Garten 4: 204–207.

Williams M.A., Adamson D., Prescott J.R. & Williams F.M. 2003. New light on the age of the White Nile. Geology 31 (11): 1001–1004. https://doi.org/10.1130/G19801.1

Wilson D.E. & Mittermeier R.A. 2011. Handbook of the Mammals of the World. Vol. 2: Hoofed Mammals. Lynx Edicions, Barcelona.

Winter S., Fennessy J., Fennessy S. & Janke A. 2018a. Matrilineal population structure and distribution of the Angolan giraffe in the Namib desert and beyond. Ecological Genetics and Genomics 7: 1–5.

https://doi.org/10.1016/j.egg.2018.03.003

Winter S., Fennessy J. & Janke A. 2018b. Limited introgression supports division of giraffe into four species. Ecology and Evolution 8 (20): 10156–10165. https://doi.org/10.1002/ece3.4490

de Winton W.D. 1899. On the giraffe of Somaliland (Giraffa camelopardalis reticulata). Annals and Magazine of Natural History 7 (4): 211–212. https://doi.org/10.1080/00222939908678186

Wube T., Doherty J.B., Fennessy J. & Marais A. 2018. Giraffa camelopardalis ssp. camelopardalis. The IUCN Red List of Threatened Species 2018: e.T88420707A88420710. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T88420707A88420710.en.

Yin Q.Z. & Guo Z.T. 2007. Strong summer monsoon during the cool MIS-13. Climate of the Past Discussions 3: 1119–1132. https://doi.org/10.5194/cpd-3-1119-2007

Zabeirou R. 2017. National Survey Report of the West African Giraffe, Niger – August 2017. Giraffe Conservation Foundation and Sahara Conservation Fund, Niamey, Niger.

Published
2020-08-18
How to Cite
Petzold, A., Magnant, A.-S., Edderai, D., Chardonnet, B., Rigoulet, J., Saint-Jalme, M., & Hassanin, A. (2020). First insights into past biodiversity of giraffes based on mitochondrial sequences from museum specimens. European Journal of Taxonomy, (703). https://doi.org/10.5852/ejt.2020.703
Section
Zoology