Heads up-Four Giraffa species have distinct cranial morphology
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
39700177
PubMed Central
PMC11658530
DOI
10.1371/journal.pone.0315043
PII: PONE-D-24-31082
Knihovny.cz E-zdroje
- MeSH
- biologická evoluce MeSH
- druhová specificita MeSH
- fylogeneze MeSH
- lebka * anatomie a histologie MeSH
- pohlavní dimorfismus MeSH
- žirafy * anatomie a histologie klasifikace MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Giraffe (Giraffa spp.) are among the most unique extant mammals in terms of anatomy, phylogeny, and ecology. However, aspects of their evolution, ontogeny, and taxonomy are unresolved, retaining lingering questions that are pivotal for their conservation. We assembled the largest known dataset of Giraffa skulls (n = 515) to investigate patterns of cranial variability using 3D geometric morphometrics. The results show distinct sexual dimorphism and divergent ontogenetic trajectories of skull shape for the north clade (G. camelopardalis antiquorum, G. c. camelopardalis, G. c. peralta, and G. reticulata) and the south clade (G. giraffa angolensis, G. g. giraffa, G. tippelskirchi tippelskirchi, and G. t. thornicrofti) which was further supported statistically. Discriminant functions found statistically significant cranial shape differences between all four Giraffa species, and in some cases also between subspecies of the same species. Our 3D morphometric analysis shows that the four genetically distinct Giraffa spp. also have distinct cranial morphologies, largely addressable to features of display (ossicones). Our results highlight the importance of focusing future giraffe conservation efforts on each taxon to maintain their unique characteristics and biodiversity in the wild.
CIPb UAM Center for the Integration in Paleobiology Universidad Autónoma de Madrid Madrid Spain
Department of Biological Science University of Cape Town Cape Town South Africa
Department of Biology Unidad de Paleontología Universidad Autónoma de Madrid Madrid Spain
Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Prague Czech Republic
Giraffe Conservation Foundation Windhoek Namibia
Institute of Biochemistry and Biology University of Potsdam Potsdam Germany
Museum für Naturkunde Leibnitz Institute for Evolution and Biodiversity Science Berlin Germany
National Museums of Kenya Nairobi Kenya
Research Institute of Wildlife Ecology University of Veterinary Medicine Vienna Austria
School of Biology and Environmental Science University College Dublin Dublin Ireland
Senckenberg Biodiversity and Climate Research Centre Frankfurt am Main Germany
Zobrazit více v PubMed
Mace G. The role of taxonomy in species conservation. Philos Trans R Soc B 2004; 359: 711–719. doi: 10.1098/rstb.2003.1454 PubMed DOI PMC
Morrison WR III, Lohr JL, Duchen P, Wilches R, Tujillo D, Mair M, et al.. The impact of taxonomic change on conservation: Does it kill, can it save, or is it just irrelevant? Biol Conserv 2009; 142: 3201–3206. doi: 10.1016/j.biocon.2009.07.019 DOI
Costello M, Vanhoorne B, Appeltans W. Conservation of biodiversity through taxonomy, data publication, and collaborative infrastructures. Conserv Biol 2015; 29(4): 1094–1099. doi: 10.1111/cobi.12496 PubMed DOI
Vogel Ely C, de Loreto Bordignon SA, Trevisan R, Boldrini II. Implications of poor taxonomy in conservation. J Nat Conserv 2017; 36: 10–13. doi: 10.1016/j.jnc.2017.01.003 DOI
Schmidt C, Hoban S, Hunter M, Paz-Vinas I, Garroway C. Genetic diversity and IUCN Red List Status. Conserv Biol 2023; 37: c14064. doi: 10.1111/cobi.14064 PubMed DOI
Zachos FE. Species Concepts in Biology: Historical Development, Theoretical Foundations and Practical Relevance. Springer International Publishing; 2016. doi: 10.1007/978-3-319-44966-1 DOI
Murie J. On the horns, viscera and muscles of the giraffe, with a record of the post mortem examination of two specimens killed by a fire. Ann Mag Nat Hist 1872; 9: 177–195.
Thomas O. On the Five-horned Giraffe obtained by Sir Harry Johnston near Mount Elgon. Proc Zool Soc Lond 1901; 2(32): 474–483.
Ridewood WG. Some Observations on the Skull of the Giraffe. Proc Zool Soc Lond 1904; 1: 150–157. doi: 10.1111/j.1469-7998.1904.tb08281.x DOI
Spinage CA. Horns and other bony structures of the skull of the giraffe, and their functional significance. E Afr Wildl J 1968; 6: 53–61.
Spinage CA. Giraffid Horns. Nat 1970; 227: 735–736. doi: 10.1038/227735a0 PubMed DOI
Spinage CA. The median ossicone of Giraffa camelopardalis. J Zool, Lond 1993; 230: 1–5. doi: 10.1111/j.1469-7998.1993.tb02667.x DOI
Solounias N. Anatomy and Evolution of the Giraffe: Parts Unknown. Cambridge Scholars Publishing; 2022.
Mitchell G, Skinner JD. On the origin, evolution and phylogeny of giraffes Giraffa camelopardalis. Trans R Soc S Afr 2003; 58(1): 51–73. doi: 10.1080/00359190309519935 DOI
Solounias N. Family Giraffidae. In: Prothero D, Foss SE, editors. The Evolution of Artiodactyls. The Johns Hopkins University Press; 2007. pp. 257–277.
Ríos M, Sánchez I, Morales J. A new giraffid (Mammalia, Ruminantia, Pecora) from the late Miocene of Spain, and the evolution of the sivathere-samothere lineage. PLoS ONE 2017; 12(11): e0185378. doi: 10.1371/journal.pone.0185378 PubMed DOI PMC
Singer R, Boné E. Modern Giraffes and the Fossil Giraffids of Africa. Ann S Afr Mus 1960; 45(4): 375–548
Seymour RS. Patterns of Subspecies Diversity in the Giraffe, Giraffa camelopardalis (L. 1758): Comparison of Systematic Methods and Their Implications for Conservation Policy. Ph. D thesis, University of Kent. 2001. doi: 10.22024/UniKent/01.02.86053 DOI
Lydekker R. Local variation in the giraffe. Animal Life and the World of Nature 1903; 2: 76–84.
Lydekker R. The Angola Giraffe. Anim Life World Nat 1903; 2: 121–122.
Lydekker R. On the subspecies of Giraffa camelopardalis. Proc Zool Soc Lond 1904; 74: 202–229. doi: 10.1111/j.1469-7998.1904.tb08288.x DOI
Lydekker R. Two undescribed giraffes. Nat 1911; 87: 484–484. doi: 10.1038/087484c0 DOI
Groves C, Grubb P. Ungulate Taxonomy. The Johns Hopkins University Press; 2011. doi: 10.56021/9781421400938 DOI
Dagg AI. Giraffa camelopardalis. Mamm Spec 1971; 5: 1–8. doi: 10.2307/3503830 DOI
Mitchell G. The origins of the scientific study and classification of giraffes. Trans R Soc S Afr 2009; 64: 1–13. doi: 10.1080/00359190909519234 DOI
Seymour RS. The taxonomic history of giraffe–a brief review. Giraffa 2012; 6(1): 5–9.
Dagg AI. Giraffe: Biology, Behaviour, and Conservation. Cambridge University Press; 2014. doi: 10.1017/CBO9781139542302 DOI
Shorrocks B. The Giraffe: Biology, ecology, evolution and behaviour. John Wiley & Sons; 2016.
Fennessy J, Bidon T, Reuss F, Kumar V, Elkan P, Nilsson M, et al.. Multi-locus Analyses Reveal Four Giraffe Species Instead of One. Curr Biol 2016; 26: 2543–2549. doi: 10.1016/j.cub.2016.07.036 PubMed DOI
Fennessy J, Winter S, Reuss F, Kumar V, Nilsson MA, Vamberger M, et al.. Response to “How many species of giraffe are there?”. Curr Biol 2017; 27: R137–137. doi: 10.1016/j.cub.2016.12.045 PubMed DOI
Winter S, Fennessy J, Janke A. Limited introgression supports division of giraffe into four species. Ecol Evol 2018; 8: 10156–10165. doi: 10.1002/ece3.4490 PubMed DOI PMC
Petzold A, Hassanin A. 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 2020; 15(2): e0217956. doi: 10.1371/journal.pone.0217956 PubMed DOI PMC
Petzold A, Magnant A-S, Edderai D, Chardonnet B, Rigoulet J, Saint-Jalme M, et al.. First insights into past biodiversity of giraffes based on mitochondrial sequences from museum specimens. Eur J Taxon 2020; 703: 1–33. doi: 10.5852/ejt.2020.703 DOI
Coimbra R, Winter S, Kumar V, Koepfli K-P, Gooley R, Dobrynin P, et al.. Whole-genome analysis of giraffe supports four distinct species. Curr Biol 2021; 31: 2929–2938. doi: 10.1016/j.cub.2021.04.033 PubMed DOI
Coimbra R, Winter S, Mitchell B, Fennessy J, Janke A. Conservation Genomics of Two Threatened Subspecies of Northern Giraffe: The West African and the Kordofan Giraffe. Genes 2022; 13(221): 1–14. doi: 10.3390/genes13020221 PubMed DOI PMC
Coimbra R, Winter S, Muneza A, Fennessy S, Otiende M, Mijele D, et al.. Genomic analysis reveals limited hybridisation among three giraffe species in Kenya. BMC Biol 2023; 21: 215. doi: 10.1186/s12915-023-01722-y PubMed DOI PMC
Bertola LD, Quinn L, Hanghøj K, Garcia-Erill G, Rasmussen MS, Balboa RF, et al.. Giraffe lineages are shaped by major ancient admixture events. Curr Biol 2024; 34: 1–11. doi: 10.1016/j.cub.2024.02.051 PubMed DOI
Pratt DM, Anderson VH. Population, distribution, and behaviour of giraffe in the Arusha National Park. Tanzania. J Nat Hist 1982; 16: 481–489. doi: 10.1080/00222938200770381 DOI
Pratt DM, Anderson VH. Giraffe social behaviour. J Nat Hist 1985; 19: 771–781. doi: 10.1080/00222938500770471 DOI
Dagg AI. Sexual differences in giraffe skulls. Mammalia 1965; 29: 610–612. doi: 10.1515/mamm.1965.29.4.610 DOI
Fedorov A, Beichel R, Kalpathy-Cramer J, Finet J, Fillion-Robin J-C, Pujol S, et al.. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Resonance Imag 2012; 30: 1323–1341. doi: 10.1016/j.mri.2012.05.001 PubMed DOI PMC
Corporation Stratovan. Stratovan Checkpoint [Software]. Version 2024.03.20. Mar 20, 2024. Available from: https://www.stratovan.com/products/checkpoint
Baken E, Collyer M, Kaliontzopoulou A, Adams D. geomorph v4.0 and gmShiny: enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Method Ecol Evol 2021; 12: 2355–2363. doi: 10.1111/2041-210X.13723 DOI
Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 2011; 11: 353–357. doi: 10.1111/j.1755-0998.2010.02924.x PubMed DOI
Hammer Ø, Harper D, Ryan D. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electr 2001; 4(1): 1–9. Available from: http://palaeo-electronica.org/2001_1/past/issue1_01.htm.
Institute for Data Analysis and Visualization (IDAV), All rights reserved. Wiley, David F. Copyright 2002–2005. Landmark. Version: 3,0,0,6.
Revell L. phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things). PeerJ 2024; 12: e16505. doi: 10.7717/peerj.16505 PubMed DOI PMC
Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. Version 3.81. 2023; Available from: http://www.mesquiteproject.org.
Hall‐Martin AJ. Dentition and age determination of the giraffe Giraffa camelopardalis. J Zool 1976; 80: 263–289. doi: 10.1111/j.1469-7998.1976.tb04678.x DOI
Dagg AI. The subspeciation of the giraffe. J Mammal 1962; 43: 550–552. doi: 10.2307/1376925 DOI
Weston EM. Evolution of ontogeny in the hippopotamus skull: Using allometry to dissect developmental change. Biol J Linnean Soc 2003; 80: 625–638. doi: 10.1111/j.1095-8312.2003.00263.x DOI
Martino R, Zanolli C, Fidalgo D, Pandolfi L. Talking heads: disentangling the shape changes of the large extant hippopotamus during its ontogenetic development. Integrative Zool 2024. doi: 10.1111/1749-4877.12850 PubMed DOI
Ansell WFH. Artiodactyla (excluding the genus Gazella). In: Meester JAJ, Setzer HW, editors. The Mammals of Africa: An Identification Manual. Smithsonian Institution; 1971. pp. 12–14.
Krumbiegel I. Die Giraffe (Giraffa camelopardalis). A. Ziemsen Verlag; 1971.
Brown DM, Brenneman RA, Koepfli K-P, Pollinger JP, Milá B, Georgiadis NJ, et al.. Extensive population genetic structure in the giraffe. BMC Biol 2007; 5: 57. doi: 10.1186/1741-7007-5-57 PubMed DOI PMC
Brown MB, Fennessy J, Crego RD, Fleming CH, Alves J, Brandlová K, et al.. Ranging behaviours across ecological and anthropogenic disturbance gradients: a pan-African perspective of giraffe (Giraffa spp.) space use. Proc R Soc B 2023; 290: 20230912. doi: 10.1098/rspb.2023.0912 PubMed DOI PMC
Hassanin A, Ropiquet A, Gourmand A, Chardonnet B, Rigoulet J. Mitochondrial DNA variability in Giraffa camelopardalis: consequences for taxonomy, phylogeography and conservation of giraffes in West and central Africa. Comptes Rendus Biologies 2007; 330: 265–274. doi: 10.1016/j.crvi.2007.02.008 PubMed DOI
Thomassen HA, Freedman AH, Brown DM, Buermann W, Jacobs DK. Regional Differences in Seasonal Timing of Rainfall Discriminate between Genetically Distinct East African Giraffe Taxa. PLoS ONE 2013; 8(10): e77191. doi: 10.1371/journal.pone.0077191 PubMed DOI PMC
Bock F, Fennessy J, Bidon T, Tutchings A, Marais A, Deacon F, et al.. Mitochondrial sequences reveal a clear separation between Angolan and South African giraffe along a cryptic rift valley. BMC Evol Biol 2014; 14: 219. doi: 10.1186/s12862-014-0219-7 PubMed DOI PMC
Ciofolo I, Le Pendu Y. Giraffa camelopardalis. In: Kingdon JS, Hoffmann M, editors. The Mammals of Africa. Academic Press, Amsterdam; 2013. pp. 96–110.
Solounias N, Danowitz M. Astragalar Morphology of Selected Giraffidae. PLoS ONE 2016; 11(3): e0151310. doi: 10.1371/journal.pone.0151310 PubMed DOI PMC
Lee V, Solounias N. Osteological foot differences between giraffes from distinct geographical locations; a pilot study. Zoologischer Anzeiger 2022; 296: 179–186. doi: 10.1016/j.jcz.2022.01.001 DOI
Hausen N. Computer-aided photographic pelage pattern analysis of Giraffa camelopardalis (Artiodactyla:Giraffidae). M.Sc. Thesis, University of London; 2017.
Mayr E. What Is a Species, and What Is Not? Philos Sci 1996; 63(2): 262–277. doi: 10.1086/289912 DOI
Stankowski S, Ravinet M. Quantifying the use of species concepts. Curr Biol 2021; 31(9): R428–R429. doi: 10.1016/j.cub.2021.03.060 PubMed DOI
Buckley-Beason VA, Johnson WE, Nash WG, Stanyon R, Menninger JC, Driscoll CA, et al.. Molecular Evidence for Species-Level Distinctions in Clouded Leopards. Curr Biol 2006; 16: 2371–2376. doi: 10.1016/j.cub.2006.08.066 PubMed DOI PMC
Yang L, Wei F, Zhan X, Fan H, Zhao P, Huang G, et al.. Evolutionary Conservation Genomics Reveals Recent Speciation and Local Adaptation in Threatened Takins. Mol Biol Evol 2022; 39(6): msac111. doi: 10.1093/molbev/msac111 PubMed DOI PMC
Roca AL, Georgiadis N, Pecon-Slattery J, O’Brien SJ. Genetic evidence for two species of elephant in Africa. Sci 2001; 293(5534): 1473–1477. doi: 10.1126/science.1059936 PubMed DOI
Harding L. Available names for Rangifer (Mammalia, Artiodactyla, Cervidae) species and subspecies. ZooKeys 2022; 1119: 117–151. doi: 10.3897/zookeys.1119.80233 PubMed DOI PMC
Nater A, Mattle-Greminger MP, Nurcahyo A, Nowak MG, de Manuel M, Desai T, et al.. Morphometric, Behavioral, and Genomic Evidence for a New Organutan Species. Curr Biol 2017; 27: 3487–3498. doi: 10.1016/j.cub.2017.09.047 PubMed DOI
Ghiselin MT. A radical solution to the species problem. Syst Zool 1974; 23: 536–544. doi: 10.2307/2412471 DOI
de Queiroz K. Species Concepts and Species Delimitation. Syst Biol 2007; 56(6): 879–886. doi: 10.1080/10635150701701083 PubMed DOI
Grubb P, Groves CP, Dudley JP, Shoshani J. Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2000; 2: 1–4. doi: 10.22237/elephant/1521732169 DOI
Comstock KE, Georgiadis N, Pecon-Slattery J, Roca AL, Ostrander EA, O’Brien SJ, et al.. Patterns of molecular genetic variation among African elephant populations. Mol Ecol 2002; 11: 2489–2498. doi: 10.1046/j.1365-294x.2002.01615.x PubMed DOI
Gobush KS, Edwards CTT, Balfour D, Wittemyer G, Maisels F, Taylor RD. Loxodonta africana (amended version of 2021 assessment). The IUCN Red List of Threatened Species 2022: e.T181008073A223031019. doi: 10.2305/IUCN.UK.2022-2.RLTS.T181008073A223031019.en DOI
Gobush KS, Edwards CTT, Maisels F, Wittemyer G, Balfour D, Taylor RD. Loxodonta cyclotis (errata version published in 2021). The IUCN Red List of Threatened Species 2021: e.T181007989A204404464. doi: 10.2305/IUCN.UK.2021-1.RLTS.T181007989A204404464.en DOI