Conservation Genetics

, Volume 19, Issue 2, pp 397–408 | Cite as

Genetic variation of complete mitochondrial genome sequences of the Sumatran rhinoceros (Dicerorhinus sumatrensis)

  • Cynthia C. Steiner
  • Marlys L. Houck
  • Oliver A. Ryder
Research Article

Abstract

The Sumatran rhinoceros (Dicerorhinus sumatrensis) is the smallest and one of the most endangered rhinoceros species, with less than 100 individuals estimated to live in the wild. It was originally divided into three subspecies but only two have survived, D. sumatrensis sumatrensis (Sumatran subspecies), and D. s. harrissoni (Bornean). Questions regarding whether populations of the Sumatran rhinoceros should be treated as different management units to preserve genetic diversity have been raised, particularly in light of its severe decline in the wild and low breeding success in captivity. This work aims to characterize genetic differentiation between Sumatran rhinoceros subspecies using complete mitochondrial genomes, in order to unravel their maternal evolutionary history and evaluate their status as separate management units. We identified three major phylogenetic groups with moderate genetic differentiation: two distinct haplogroups comprising individuals from both the Malay Peninsula and Sumatra, and a third group from Borneo. Estimates of divergence time indicate that the most recent common ancestor of the Sumatran rhinoceros occurred approximately 360,000 years ago. The three mitochondrial haplogroups showed a common divergence time about 80,000 years ago corresponding with a major biogeographic event in the Sundaland region. Patterns of mitochondrial genetic differentiation may suggest considering Sumatran rhinoceros subspecies as different conservation units. However, the management of subspecies as part of a metapopulation may appear as the last resource to save this species from extinction, imposing a conservation dilemma.

Keywords

Mitogenomes Phylogenetics Genetic structure Divergence time Critically endangered species 

Notes

Acknowledgements

This work was possible thanks to the contribution of Julie Fronczek, Marisa Korody, and Suellen Charter generating the Sumatran rhinoceros fibroblast cell lines. Inclusion of the rhinoceros samples from Sabah, D. s. harrisoni, was made possible through BORA (Bornean Rhino Alliance) and the Leibnitz Institute of Zoo and Wildlife Medicine. We thank Alfred Roca and Jessica Brandt for helpful discussion and comments on the manuscript. Funding was obtained from an anonymous donor to San Diego Zoo Global.

Supplementary material

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Supplementary material 1 (DOCX 11 KB)
10592_2017_1011_MOESM2_ESM.pptx (209 kb)
Supplementary material 2 (PPTX 209 KB)
10592_2017_1011_MOESM3_ESM.docx (24 kb)
Supplementary material 3 (DOCX 24 KB)

References

  1. Amato G, Wharton D, Zainuddin ZZ, Powell JR (1995) Assessment of conservation units for the Sumatran rhinoceros (Dicerorhinus sumatrensis). Zoo Biol 14:395–402. doi: 10.1002/zoo.1430140502 CrossRefGoogle Scholar
  2. Ambrose SH (1998) Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans. J Hum Evol 34:623–651. doi: 10.1006/jhev.1998.0219 CrossRefPubMedGoogle Scholar
  3. Anderson-Lederer RM, Linklater WL, Ritchie PA (2012) Limited mitochondrial DNA variation within South Africa’s black rhino (Diceros bicornis minor) population and implications for management. Afr J Ecol 50:404–413. doi: 10.1111/j.1365-2028.2012.01333.x CrossRefGoogle Scholar
  4. Bandelt HJ, Forster P, Ruhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. doi: 10.1093/oxfordjournals.molbev.a026036 CrossRefPubMedGoogle Scholar
  5. Benton MJ, Donoghue PCJ (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53. doi: 10.1093/molbev/msl150 CrossRefPubMedGoogle Scholar
  6. Bird MI, Taylor D, Hunt C (2005) Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quat Sci Rev 24:2228–2242. doi: 10.1016/j.quascirev.2005.04.004 CrossRefGoogle Scholar
  7. Brown SM, Houlden BA (2000) Conservation genetics of the black rhinoceros (Diceros bicornis). Conserv Genet 1:365–370. doi: 10.1023/A:1011579807460 CrossRefGoogle Scholar
  8. Christman J (2010) The Sumatran rhinoceros (Dicerorhinus sumatrensis) international studbook. Disney’s Animal Kingdom, OrlandoGoogle Scholar
  9. Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714. doi: 10.1126/science.1172873 CrossRefPubMedGoogle Scholar
  10. Cozzuol MA, Clozato CL, Holanda EC, Rodrigues FHG, Nienow S, de Thoisy B, Redondo RAF, Santos FR (2013) A new species of tapir from the Amazon. J Mamm 94:1331–1345. doi: 10.1644/12-MAMM-A-169.1 CrossRefGoogle Scholar
  11. Das PK, Borthakur U, Sarma HK, Talukdar BK (2015) Population genetic assessment of extant populations of greater one-horned rhinoceros (Rhinoceros unicornis) in India. Eur J Wildl Res 61:841–851. doi: 10.1007/s10344-015-0960-2 CrossRefGoogle Scholar
  12. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:e214. doi: 10.1186/1471-2148-7-214 CrossRefGoogle Scholar
  13. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. doi: 10.1093/molbev/msi103 CrossRefPubMedGoogle Scholar
  14. Eisenmann V (1992) Origins, dispersals, and migrations of Equus (Mammalia, Perissodactyla). Cour Forsch Inst Senckenberg 153:161–170Google Scholar
  15. Ellis S, Ivy J, Ramono WS (2011) Future directions towards the persistence of the captive Sumatran rhino population. White paper accessed 24 Jan 2011. http://www.rhinoresourcecenter.com/index.php?s=1&act=pdfviewer&id=1404633462&folder=140
  16. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  17. Fernando P, Polet G, Foead N, Ng LS, Pastorini J, Melnick DJ (2006) Genetic diversity, phylogeny and conservation of the Javan rhinoceros (Rhinoceros sondaicus). Conserv Genet 7:439–448. doi: 10.1007/s10592-006-9139-4 CrossRefGoogle Scholar
  18. Foose TJ, van Strien N (1997) Asian rhinos—status survey and conservation action plan. IUCN, GlandGoogle Scholar
  19. George M, Chemnick LG, Cisova D, Gabrisova E, Straril A, Ryder OA (1993) Genetic differentiation of white rhinoceros subspecies: diagnostic differences in mitochondrial DNA and serum proteins. In: Ryder OA (ed) Rhinoceros biology and conservation. Zoological Society of San Diego, San Diego, pp 105–113Google Scholar
  20. Goossens B, Salgado-Lynn M, Rovie-Ryan JJ, Ahmad AH, Payne J, Zainuddin ZZ, Nathan SKSS, Ambu LN (2013) Genetics and the last stand of the Sumatran rhinoceros Dicerorhinus sumatrensis. Oryx 47:340–344. doi: 10.1017/S0030605313000045 CrossRefGoogle Scholar
  21. Groves CP (1967) The rhinoceroses of Southeast Asia. Säugetierkd Mitt 15:221–237Google Scholar
  22. Groves CP, Fernando P, Robovsky J (2010) The sixth rhino: a taxonomic re-assessment of the critically endangered northern white rhinoceros. PLoS ONE 5(4):e9703. doi: 10.1371/journal.pone.0009703 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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. Syst Biol 59:307–321. doi: 10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  24. Havmøller RG, Payne J, Ramono W, Ellis S, Yoganand K, Long B, Dinerstein E, Williams AC, Putra RH, Gawi J, Talukdar BK, Burgess N (2016) Will current conservation responses save the critically endangered Sumatran rhinoceros Dicerorhinus sumatrensis? Oryx 50:355–359. doi: 10.1017/S0030605315000472 CrossRefGoogle Scholar
  25. Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE 8(5):e62992. doi: 10.1371/journal.pone.0062992 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ho SYW, Shapiro B (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11:423–434. doi: 10.1111/j.1755-0998.2011.02988.x CrossRefPubMedGoogle Scholar
  27. Houck ML, Ryder OA, Vahala J, Kock RA, Oosterhuis JE (1994) Diploid chromosome number and chromosomal variation in the white rhinoceros (Ceratotherium simum). J Hered 85:30–34. doi: 10.1093/oxfordjournals.jhered.a111387 PubMedGoogle Scholar
  28. Houck ML, Ryder OA, Kumamoto AT, Benirschke K (1995) Cytogenetics of the Rhinocerotidae. Verh Berl Erkrank Zootiere 37:25–32Google Scholar
  29. Lane CS, Chorn BT, Johnson TC (2013) Ash from the Toba supereruption in Lake Malawi shows no volcanic winter in East Africa at 75 ka. Proc Natl Acad Sci USA 110:8025–8029. doi: 10.1073/pnas.1301474110 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Librado P, Rozas J (2009) DnaSP ver. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinform Appl Note 25:1451–1452. doi: 10.1093/bioinformatics/btp187 CrossRefGoogle Scholar
  31. Louys J (2007) Limited effect of the Quaternary’s largest super-eruption (Toba) on land mammals from Southeast Asia. Quat Sci Rev 26:3108–3117. doi: 10.1016/j.quascirev.2007.09.008 CrossRefGoogle Scholar
  32. Miller PS, Lees C, Ramono W, Purwoto A, Rubianto A, Sectionov Talukdar B, Ellis S (2015) Population viability analysis for the Sumatran rhino in Indonesia. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, MNGoogle Scholar
  33. Morales JC, Andau PM, Supriatna J, Zainuddin Z-Z, Melnick DJ (1997) Mitochondrial DNA variability and conservation genetics of the Sumatran rhinoceros. Conserv Biol 11:539–543. doi: 10.1046/j.1523-1739.1997.96171.x CrossRefGoogle Scholar
  34. Nardelli F (2014) The last chance for the Sumatran rhinoceros? Pachyderm 55:43–53Google Scholar
  35. Orlando L, Leonard JA, Thenot A, Laudet V, Guerin C, Hänni C (2003) Ancient DNA analysis reveals woolly rhino evolutionary relationships. Mol Phylogenet Evol 28:485–499. doi: 10.1016/S1055-7903(03)00023-X CrossRefPubMedGoogle Scholar
  36. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PLF, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas A-S, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AMV, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KAS, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MTP, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E (2013) Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499:74–78. doi: 10.1038/nature12323 CrossRefPubMedGoogle Scholar
  37. Parson W, Strobl C, Huber G, Zimmermann B, Gomes SM, Souto L, Fendt L, Delport R, Langit R, Wootton S, Lagace R, Irwin J (2013) Evaluation of next generation mtGenome sequencing using the Ion Torrent Personal Genome Machine (PGM). Forensic Sci Int Genet 7:543–549. doi: 10.1016/j.fsigen.2013.06.003 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi: 10.1093/molbev/msn083 CrossRefPubMedGoogle Scholar
  39. Prothero D, Schoch R (1989) The evolution of perissodactyls. Oxford University Press, New YorkGoogle Scholar
  40. Rambaut A, Drummond AJ (2007) Tracer [computer program]. http://beast.bio.ed.ac.uk/tracer
  41. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi: 10.1093/bioinformatics/btg180 CrossRefPubMedGoogle Scholar
  42. Roth TL (2003) Breeding the Sumatran rhinoceros (Dicerorhinus sumatrensis) in captivity: behavioral challenges, hormonal solutions. Horm Behav 44:31. doi: 10.1016/S0018-506X(03)00068-0 Google Scholar
  43. Ruiz-García M, Vásquez C, Pinedo-Castro MO, Sandoval S, Castellanos A, Kaston F, Thoisy B, Shostell J (2012) Phylogeography of the Mountain Tapir (Tapirus pinchaque) and the Central American Tapir (Tapirus bairdii) and the origins of the three Latin-American tapirs by means of mtCyt-B sequences. In: Anamthawat-Jónsson K (ed) Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems. InTech, Rijeka, pp 83–116Google Scholar
  44. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10. doi:  10.1016/0169-5347(86)90059-5 CrossRefGoogle Scholar
  45. Sankararaman S, Mallick S, Dannemann M, Prüfer K, Kelso J, Pääbo S, Patterson N, Reich D (2014) The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507:354–357. doi: 10.1038/nature12961 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Saragusty J, Diecke S, Drukker M, Durrant B, Friedrich Ben-Nun I, Galli C, Göritz F, Hayashi K, Hermes R, Holtze S, Johnson S, Lazzari G, Loi P, Loring JF, Okita K, Renfree MB, Seet S, Voracek T, Stejskal J, Ryder OA, Hildebrandt TB (2016) Rewinding the process of mammalian extinction. Zoo Biol 35:280–292. doi: 10.1002/zoo.21284 CrossRefPubMedGoogle Scholar
  47. Sharma R, Arora N, Goossens B, Nater A, Morf N, Salmona J, Bruford MW, Van Schaik CP, Krützen M, Chikhi L (2012) Effective population size dynamics and the demographic collapse of Bornean orangutans. PLoS ONE 7(11):e49429. doi: 10.1371/journal.pone.0049429 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Soares P, Trejaut JA, Loo J-H, Hill C, Mormina M, Lee C-L, Chen Y-M, Hudjashov G, Forster P, Macaulay V, Bulbeck D, Oppenheimer S, Lin M, Richards MB (2008) Climate change and postglacial human dispersals in Southeast Asia. Mol Biol Evol 25:1209–1218. doi: 10.1093/molbev/msn068 CrossRefPubMedGoogle Scholar
  49. Steiner CC, Ryder OA (2011) Molecular phylogeny and evolution of the Perissodactyla. Zool J Linnean Soc 163:1289–1303. doi: 10.1111/j.1096-3642.2011.00752.x CrossRefGoogle Scholar
  50. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  51. van Strien NJ, Manullang B, Sectionov IW, Khan MKM, Sumardja E, Ellis S, Han KH, Boeadi Payne J, Bradley ME (2008) Dicerorhinus sumatrensis. The IUCN Red List of Threatened Species 2008: e.T6553A12787457Google Scholar
  52. Vilstrup JT, Seguin-Orlando A, Stiller M, Ginolhac A, Raghavan M, Nielsen SCA, Weinstock J, Froese D, Vasiliev SK, Ovodov ND, Clary J, Helgen KM, Fleischer RC, Cooper A, Shapiro B, Orlando L (2013) Mitochondrial phylogenomics of modern and ancient equids. PLoS ONE 8(2):e55950. doi: 10.1371/journal.pone.0055950 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Willerslev E, Gilbert MTP, Binladen J, Ho SYW, Campos PF, Ratan A, Tomsho LP, da Fonseca RR, Sher A, Kuznetsova TV, Nowak-Kemp M, Roth TL, Miller W, Schuster SC (2009) Analysis of complete mitochondrial genomes from extinct and extant rhinoceroses reveals lack of phylogenetic resolution. BMC Evol Biol 20099:95. doi: 10.1186/1471-2148-9-95 CrossRefGoogle Scholar
  54. Woodruff DS (2010) Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodivers Conserv 19:919–941. doi: 10.1007/s10531-010-9783-3 CrossRefGoogle Scholar
  55. Zielinski GA, Mayewski PA, Meeker LD, Whitlow S, Twickler MS, Taylor K (1996) Potential atmospheric impact of the Toba mega-eruption ∼71,000 years ago. Geophys Res Lett 23:837–840. doi: 10.1029/96GL00706 CrossRefGoogle Scholar
  56. Zschokke S, Armbruster GFJ, Ursenbacher S, Baur B (2011) Genetic differences between the two remaining wild populations of the endangered Indian rhinoceros (Rhinoceros unicornis). Biol Conserv 144:2702–2709. doi: 10.1016/j.biocon.2011.07.031 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Cynthia C. Steiner
    • 1
  • Marlys L. Houck
    • 1
  • Oliver A. Ryder
    • 1
  1. 1.San Diego Zoo Institute for Conservation Research, San Diego Zoo GlobalEscondidoUSA

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