Advertisement

Journal of Mammalian Evolution

, Volume 22, Issue 1, pp 111–120 | Cite as

One Species or Two? Vicariance, Lineage Divergence and Low mtDNA Diversity in Geographically Isolated Populations of South Asian River Dolphin

  • G. T. Braulik
  • R. Barnett
  • V. Odon
  • V. Islas-Villanueva
  • A. R. Hoelzel
  • J. A. Graves
Original Paper

Abstract

Despite their endangered status, the taxonomic relationship between the two geographically isolated South Asian river dolphin populations has never been comprehensively assessed and remains contentious. Here we present the first dedicated evaluation of the molecular phylogenetic relationship between the Indus (Platanista gangetica minor) and Ganges (Platanista gangetica gangetica) River dolphins using mitochondrial DNA from the control region and cytochrome b, extracted from museum specimens. The 458 bp partial control region sequences from 26 Indus River dolphin samples exhibited no variation. Only six haplotypes were identified in the 31 (18 Indus; 13 Ganges) complete (856 bp) control region sequences obtained, none were shared between subspecies, and there were five fixed differences between them. Similarly low genetic diversity was found in a 541 bp section of the cytochrome b gene (n = 29). The lack of shared haplotypes and fixed differences resulted in Φ ST for the partial control region sequences of 0.932 (p < 0.0001) and FST of 0.843 (p < 0.0001), indicating the long-term absence of gene flow and clear genetic differentiation between the two geographically isolated populations. An externally calibrated molecular clock estimated that Indus and Ganges dolphins diverged around 550,000 years ago (95 % posterior probability 0.13–1.05 million years ago), possibly when dolphins from the Ganges dispersed into the Indus during drainage capture.

Keywords

Molecular phylogeny Taxonomy Platanista gangetica Molecular diversity Systematics River capture 

Notes

Acknowledgments

For facilitating access to museum specimens we would like to thank Doris Moerike: Staatliches Museum für Naturkunde Stuttgart, Richard Sabin: British Museum of Natural History, Martin Milner: Bell-Pettigrew Museum, University of St. Andrews, Mathew Lowe and Robert Asher: Cambridge University Museum of Zoology, Andrew Kitchener and Jerry Herman: National Museums of Scotland, Edinburgh, Uzma Khan: WWF-Pakistan, Kelly Robertson: National Marine Fisheries Service USA, Tom Jefferson and Bill Perrin. We thank Tanya Sneddon for lab assistance at St Andrews, and Darren Parker for guidance on MrBayes. The work was funded by the Whale and Dolphin Conservation Society and the US Marine Mammal Commission. We thank Simon Northridge, Phil Hammond, and Peter Clift for reviewing earlier versions of the manuscript.

Supplementary material

10914_2014_9265_MOESM1_ESM.docx (33 kb)
ESM 1 (DOCX 33 kb)
10914_2014_9265_MOESM2_ESM.pdf (301 kb)
Figure A PCR set up and primers (PDF 301 kb)

References

  1. Anderson J (1879) Anatomical and Zoological Researches: Comprising an Account of the Zoological Results of the Two Expeditions to Western Yunnan in 1868 and 1875 and a Monograph of the Two Cetacean genera Platanista and Orcella. Bernard Quaritch, Piccadilly, LondonGoogle Scholar
  2. Arnason U, Gullberg A, Gretarsdottir S, Ursing B, Janke A (2000) The mitochondrial genome of the sperm whale and a new molecular reference for estimating eutherian divergence dates. J Mol Evol 50(6): 569–578PubMedGoogle Scholar
  3. Arnason U, Gullberg A, Janke A (2004) Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene 333: 27–34PubMedCrossRefGoogle Scholar
  4. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48PubMedCrossRefGoogle Scholar
  5. Barnes LG, Doming DP, Ray CE (1985) The status of studies on fossil marine mammals. Mar Mammal Sci 1: 15–53CrossRefGoogle Scholar
  6. Blyth E (1859) On the rorqual of the Indian Ocean, with notices of other cetals, and of the sirenia or marine pachyderms. J Asiatic Soc Bengal 28: 481–498Google Scholar
  7. Burbank DW, Derry LA, France-Lanord C (1993) Reduced Himalayan sediment production 8 Myr ago despite an intensified monsoon. Nature 364: 48–50CrossRefGoogle Scholar
  8. Burridge CP, Craw D, Waters JM (2006) An empirical test of freshwater vicariance via river capture. Mol Ecol 16: 1883–1895CrossRefGoogle Scholar
  9. Cassens I, Vicario S, Waddell GV, Balchowsky H, Van Belle D, Ding W, Fan C, Mohan LRS, Simoes-Lopes PC, Bastida R, Meyer A, Stanhope MJ, Milinkovitch MC (2000) Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proc Natl Acad Sci USA 97: (21) 11343–11347PubMedCentralPubMedCrossRefGoogle Scholar
  10. Clift PD, Blusztajn J (2005) Reorganisation of the western Himalayan river system after five million years ago. Nature 438: 1001–1003PubMedCrossRefGoogle Scholar
  11. Clift PD, Carter A, Giosan L, Durcan J, Duller GaT, Macklin MG, Alizai A, Tabrez AR, Danish M, Vanlaningham S and Fuller DQ (2012) U-Pb zircon dating evidence for a Pleistocene Sarasvati River and capture of the Yamuna River. Geology 40(3): 211–214Google Scholar
  12. Committee on Taxonomy (2013) List of marine mammal species and subspecies. Society for Marine Mammalogy, www.marinemammalscience.org, consulted on 26 Oct 2013
  13. Darriba D, Taboada GL, Doallo R, Posada D ( 2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772PubMedCrossRefGoogle Scholar
  14. De Monte T, Pilleri G (1979) Cetacean haematology 1: haemoglobin. Investigations on Cetacea 10: 277–287Google Scholar
  15. Dornburg A, Brandley MC, Mcgowen MR, Near TJ (2012) Relaxed clocks and inferences of heterogeneous patterns of nucleotide substitution and divergence time estimates across whales and wolphins (Mammalia: Cetacea). Mol Biol Evol 29(2): 721–736PubMedCrossRefGoogle Scholar
  16. Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214PubMedCentralPubMedCrossRefGoogle Scholar
  17. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resources 10: 564–567CrossRefGoogle Scholar
  18. Gachal GS (2001) Aspects of the environmental ecology and an introduction to the molecular genetics of the Indus River dolphin (Platanista minor). PhD Thesis, School of Bioscience, Cardiff University, Cardiff, UKGoogle Scholar
  19. Gilpin ME, Soule ME (1986) Minimum viable populations: processes of species extinction. In: Soule ME (ed) Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates Inc., Sunderland, MassachusettsGoogle Scholar
  20. Hamilton H, Caballero S, Collins AG, Brownell JRL (2001) Evolution of river dolphins. Proc R Soc London 268: 549–556CrossRefGoogle Scholar
  21. Ho SYW, Saarma U, Barnett R, Haile J, Shapiro B (2008) The effect of inappropriate calibration: three case studies in molecular ecology. PLoS ONE 3(2): e1615PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kasuya T (1972) Some informations on the growth of the Ganges dolphin with a comment on the Indus dolphin. Sci Rep Whales Res Inst 24: 87–108Google Scholar
  23. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, Mcwilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948PubMedCrossRefGoogle Scholar
  24. Lebeck HHJ (1801) Delphinus gangeticus beschrieben von Heinrich Julius Lebeck zu Trankenbar. Der Gesellschaft Naturforschender Freunde zu Berlin Neue Schriften 3: 280–282Google Scholar
  25. McGowen MR, Spaulding M, Gatesy J (2009) Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogen Evol 53: 891–906CrossRefGoogle Scholar
  26. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9: 373–375PubMedCrossRefGoogle Scholar
  27. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76: 5269–5273Google Scholar
  28. Nikaido M, Matsuno F, Hamilton H, Brownell JRL, Cao Y, Ding W, Zuoyan Z, Shedlock AM, Fordyce RE, Hasegawa M, Okado N (2001) Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA 98(13): 7384–7389Google Scholar
  29. Owen (1853) Descriptive Catalogue of the Osteological Series Contained in the Museum of the Royal College of Surgeons. Volume II. Mammalia Placentalia. Taylor and Francis, LondonGoogle Scholar
  30. Pichler FB, Baker CS (2000) Loss of genetic diversity in the endemic Hector’s dolphin due to fisheries-related mortality. Proc R Soc London B 267: 97–102CrossRefGoogle Scholar
  31. Pilleri G (1971) Preliminary analysis of the lipids present in the blubber of Platanista indi and gangetica. Investigations on Cetacea 3: 51–52Google Scholar
  32. Pilleri G, Gihr M (1971) Differences observed in the skulls of Platanista gangetica [Roxburgh, 1801] and indi [Blyth, 1859]. Investigations on Cetacea 3: 13–21Google Scholar
  33. Pilleri G, Gihr M (1976) Osteological differences in the cervical vertebrae of Platanista indi and gangetica. Investigations on Cetacea 7: 105–108Google Scholar
  34. Pilleri G, Marcuzzi G, Pilleri O (1982) Speciation in the Platanistoidea, systematic, zoogeographical and ecological observations on recent species. Investigations on Cetacea 14: 15–46Google Scholar
  35. Reeves RR, Brownell JRL (1989) Susu Platanista gangetica (Roxburgh, 1801) and Platanista minor Owen, 1853. In: Ridgway SH, Harrison RJ (eds) Handbook of Marine Mammals Vol 4: The First Book of Dolphins. Academic Press Ltd., London, pp 66–99Google Scholar
  36. Reeves RR, Perrin WF, Taylor BL, Baker CS, Mesnick SL (eds) (2004) Report of the workshop on the shortcomings of cetacean taxonomy in relation to the needs of conservation and management. NOAA, La Jolla, California, 97 pGoogle Scholar
  37. Rice D (1998) Marine mammals of the world: systematics and distribution. Soc Mar Mammalogy Spec Pub 4: 1–231Google Scholar
  38. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhn S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3): 539–542Google Scholar
  39. Rosel PE, Rojas-Bracho L (1999) Mitochondrial DNA variation in the critically endangered vaquita Phocoena sinus Norris and MacFarland, 1958. Mar Mammal Sci 15(4): 990–1003CrossRefGoogle Scholar
  40. Roxburgh W (1801) An account of a new species of Delphinus, an inhabitant of the Ganges. Asiatick Researches 7: 170–174Google Scholar
  41. Sinha RK, Behera S, Choudhary BC (2010) Conservation action plan for the Gangetic river dolphin 2012–2020. National Ganga River Basin Authority, Ministry of Environment and Forests, India, 38 pGoogle Scholar
  42. Smith BD, Braulik G, Strindberg S, Ahmed B, Mansur R (2006) Abundance of Irrawaddy dolphins (Orcaella brevirostris) and Ganges River dolphin (Platanista gangetica gangetica) estimated using concurrent counts made by independent teams in waterways of the Sundarbans mangrove forest in Bangladesh. Mar Mammal Sci 22(2): 527–547CrossRefGoogle Scholar
  43. Steeman ME, Bebsgaard MB, Fordyce RE, Ho SYW, Rabosky DL, Nielsen R, Rahbek C, Glenner H, Sørensen MV, Willerslev E (2009) Radiation of extant cetaceans driven by restructuring of the oceans. Syst Biol 58(6): 573–585PubMedCentralPubMedCrossRefGoogle Scholar
  44. Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13: 510–524PubMedCrossRefGoogle Scholar
  45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  46. Taylor BL, Rojas-Bracho L (1999) Examining the risk of inbreeding depression in a naturally rare cetacean, the vaquita (Phocoena sinus). Mar Mammal Sci 15(4): 1004–1028CrossRefGoogle Scholar
  47. Verma S, Sinha R, Singh L (2004) Phylogetic position of Platanista gangetica: insights from the mitochondrial cytochrome b and nuclear interphotoreceptor retinoid-binding protein gene sequences. Mol Phylogen Evol 33: 280–288CrossRefGoogle Scholar
  48. Wang JY, Frasier TR, Yang SC, White BN (2008) Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena). Heredity 101: 145–155PubMedCrossRefGoogle Scholar
  49. Waters JM, Craw D, Youngson JH, Wallis GP (2001) Genes meet geology: fish phylogeographic pattern reflects ancient, rather than modern, drainage connections. Evolution 55(9): 1844–1851PubMedCrossRefGoogle Scholar
  50. Xiong Y, Brandley MC, Xu S, Zhou K, Yang G (2009) Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales. BMC Evol Biol 9: (20) doi: 10.1186/1471-2148-1189-1120
  51. Yang DY, Eng B, Waye JS, Dudar JC, Saunders SR (1998) Technical note: improved DNA extraction from ancient bones using silica-based spin columns. Am Phys Anthropol 105: 539–543CrossRefGoogle Scholar
  52. Yang G, Zhou K, Ren W, Ji G, Liu S, Bastida R, Rivero L (2002) Molecular systematics of river dolphins inferred from complete mitochondrial cytochrome-b gene sequences. Mar Mammal Sci 18(1): 20–29CrossRefGoogle Scholar
  53. Zhou X, Xu S, Yang Y, Zhou K, Yang G (2011) Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol Phylogen Evol 61: 255–264CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • G. T. Braulik
    • 1
    • 2
  • R. Barnett
    • 3
  • V. Odon
    • 1
  • V. Islas-Villanueva
    • 1
    • 4
  • A. R. Hoelzel
    • 3
  • J. A. Graves
    • 1
  1. 1.University of St. AndrewsSt. AndrewsUK
  2. 2.Pakistan Wetlands Programme/WWF-PakistanIslamabadPakistan
  3. 3.School of Biological and Biomedical SciencesDurham UniversityDurhamUK
  4. 4.Instituto de Ciencias del Mar y LimnologiaUniversidad Nacional Autonoma de Mexico (UNAM)MéxicoMéxico

Personalised recommendations