Oceanographic drivers of population differentiation in Indo-Pacific bottlenose (Tursiops aduncus) and humpback (Sousa spp.) dolphins of the northern Bay of Bengal

Abstract

The Bay of Bengal is one of the most productive ecosystems in the northern Indian Ocean and it harbours a rich community of cetaceans, including Indo-Pacific bottlenose (Tursiops aduncus) and humpback (Sousa spp.) dolphins. The taxonomy of these genera has been controversial, but within the Indian Ocean both seem to be divided into phylogenetically discrete units that range from the east to the west. Within the Sousa genus, S. plumbea is distributed in the western Indian Ocean while S. chinensis is distributed in the eastern Indian and western Pacific Ocean. T. aduncus has a discontinuous distribution throughout the Indo-Pacific Ocean and two different phylogenetic units are known to exist, one along the eastern African coast and another one in the eastern Indian and west Pacific Ocean. In this study we investigate the phylogeography of Indo-Pacific humpback and bottlenose dolphins in the northern Bay of Bengal. We sequenced the mitochondrial DNA control region for 17 bottlenose and 15 humpback dolphins and compared the results with previously published sequences within each genus. In both cases, we found that Bangladesh dolphins are genetically different from neighbouring populations. While the Bangladesh T. aduncus seem to be more closely related to the African T. aduncus form than the Pacific form, Sousa spp. seem to be more closely related to individuals from Australia. The genetic uniqueness of these populations has important evolutionary implications, due to their isolation, coastal distribution in a geographic cul-de-sac characterized by an extreme infusion, redistribution and recycling of biological productivity, and conservation implications since their survival is threatened in particular by fatal interactions with fisheries. We suggest that the particular and extreme oceanographic conditions found in the Bay of Bengal may be driving speciation in these dolphins and other marine megafauna.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Allen SJ, Bryant K, Kraus R, Loneragan N, Kopps A, Brown A, Gerber L, Krützen M (2016) Genetic isolation between coastal and fishery-impacted, offshore bottlenose dolphin (Tursiops spp.) populations. Mol Ecol. doi:10.1111/mec.13622

    PubMed  Google Scholar 

  2. Amaral AR, Beheregaray LB, Bilgmann K, Boutov D, Freitas L, Robertson KM, Sequeira M, Stockin KA, Coelho MM, Moeller LM (2012) Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (Genus Delphinus). PLoS ONE 7:e31482

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Ansmann IC, Parra GJ, Lanyon JM, Seddon JM (2012) Fine-scale genetic population structure in a mobile marine mammal: inshore bottlenose dolphins in Moreton Bay, Australia. Mol Ecol 21:4472–4485

    Article  PubMed  Google Scholar 

  4. Baker CS, Perry A, Bannister JL, Weinrich MT, Abernethy RB, Calambokidis J, Lien J, Lambertsen RH, Ramírez JU, Vasquez O, Clapham PJ, Alling A, O’Brien SJ, Palumbi SR (1993) Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc Natl Acad Sci USA 90:8239–8243

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  Article  PubMed  Google Scholar 

  6. Benzie JAH, Ballment E, Forbes AT, Demetriades NT, Sugama K, Haryanti Moria S (2002) Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol Ecol 11(12):2553–2569

    CAS  Article  PubMed  Google Scholar 

  7. Bilgmann K, Moller LM, Harcourt RG, Gibbs SE, Beheregaray LB (2007) Genetic differentiation in bottlenose dolphins from South Australia: association with local oceanography and coastal geography. Mar Ecol-Prog Ser 341:265–276

    CAS  Article  Google Scholar 

  8. Braulik GT, Findlay K, Cerchio S, Baldwin R (2015) Assessment of the conservation status of the indian ocean humpback dolphin (Sousa plumbea) Using the IUCN red list criteria. Adv Mar Biol 72:119–141

    Article  PubMed  Google Scholar 

  9. Chen H, Zhai K, Chen J, Chen Y, Wen H, Chen S, Wu Y (2008) A preliminary investigation on genetic diversity of Sousa chinensis in the Pearl River Estuary and Xiamen of Chinese waters. J Genet Genomics 35:491–497

    CAS  Article  PubMed  Google Scholar 

  10. Chen L, Caballero S, Zhou K, Yang G (2010) Molecular phylogenetics and population structure of Sousa chinensis in Chinese waters inferred from mitochondrial control region sequences. Biochem Syst Ecol 38:897–905

    CAS  Article  Google Scholar 

  11. Committee on Taxonomy (2014) List of marine mammal species and subspecies. Society for Marine Mammalogy, www.marinemammalscience.org. Accessed 12 May 2015

  12. Compagno LJV (2007) Glyphis gangeticus. The IUCN red list of threatened species. e.T9281A12978210. Doi: 10.2305/IUCN.UK.2007.RLTS.T9281A12978210.en

  13. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 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 Resour 10:564–567

    Article  PubMed  Google Scholar 

  15. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  16. Henriques R, Potts WM, Santos CV, Sauer WHH, Shaw PW (2014) Population connectivity and phylogeography of a coastal fish, Atractoscion aequidens (Sciaenidae), across the Benguela current region: evidence of an ancient vicariant event. PLoS ONE 9(2):e87907

    Article  PubMed  PubMed Central  Google Scholar 

  17. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    CAS  Article  PubMed  Google Scholar 

  18. Hussain Z, Acharya G (1994) Mangroves of the Sundarbans, vol 2. IUCN, Bangkok

    Google Scholar 

  19. Islam MS (2003) Perspectives of the coastal and marine fisheries of the Bay of Bengal, Bangladesh. Ocean Coast Manag 46:763–796

    Article  Google Scholar 

  20. Jefferson TA, Rosenbaum HC (2014) Taxonomic revision of the humpback dolphins (Sousa spp.), and description of a new species from Australia. Mar Mamm Sci 30:1494–1541

    Article  Google Scholar 

  21. Jefferson TA, Smith BD (2016) Re-assessment of the conservation status of the Indo-Pacific humpback dolphin (Sousa chinensis) using the IUCN red list criteria. Adv Mar Biol 73:1–26

    Article  PubMed  Google Scholar 

  22. Keyse J, Crandall ED, Toonen RJ, Meyer CP, Treml EA, Riginos C (2014) The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities in the region. Bull Mar Sci 90:47–78

    Article  Google Scholar 

  23. Kopps AM, Ackermann CY, Sherwin WB, Allen SJ, Bejder L, Krützen M (2014) Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins. Proc R Soc B 281:20133245

    Article  PubMed  PubMed Central  Google Scholar 

  24. Li C, Corrigan S, Yang L, Straube N, Harris M, Hofreiter M, White WT, Naylor JP (2015) DNA capture reveals transoceanic gene flow in endangered river sharks. Proc Natl Acad Sci USA 112:13302–13307

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  Article  PubMed  Google Scholar 

  26. Liggins L, Treml EA, Possingham HP, Riginos C (2016) Seascape features, rather than dispersal traits, predict spatial genetic patterns in co-distributed reef fishes. J Biogeogr 43:256–267

    Article  Google Scholar 

  27. Mansur RM, Strindberg S, Smith BD (2012) Mark-resight abundance and survival estimation of Indo-Pacific bottlenose dolphins, Tursiops aduncus, in the swatch-of-no-ground, Bangladesh. Mar Mamm Sci 28:561–578

    Article  Google Scholar 

  28. Mendez M, Rosenbaum HC, Subramaniam A, Yackulic C, Bordino P (2010) Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range. Mol Ecol 19:2212–2228

    CAS  Article  PubMed  Google Scholar 

  29. Mendez M, Subramaniam A, Collins T, Minton G, Baldwin R, Berggren P, Sarnblad A, Amir OA, Peddemors V, Karczmarski L, Guissamulo A, Rosenbaum H (2011) Molecular ecology meets remote sensing: environmental drivers to population structure of humpback dolphins in the Western Indian Ocean. Heredity 107:349–361

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Mendez M, Jefferson TA, Kolokotronis S-O, Kruetzen M, Parra GJ, Collins T, Minton G, Baldwin R, Berggren P, Saernblad A, Amir OA, Peddemors VM, Karczmarski L, Guissamulo A, Smith B, Sutaria D, Amato G, Rosenbaum HC (2013) Integrating multiple lines of evidence to better understand the evolutionary divergence of humpback dolphins along their entire distribution range: a new dolphin species in Australian waters? Mol Ecol 22:5936–5948

    Article  PubMed  Google Scholar 

  31. Möller LM, Beheregaray LB (2001) Coastal bottlenose dolphins from southeastern Australia are Tursiops aduncus according to sequences of the mitochondrial DNA control region. Mar Mamm Sci 17:249–263

    Article  Google Scholar 

  32. Morin PA, LeDuc RG, Robertson KM, Hedrick NM, Perrin WF, Etnier M, Wade P, Taylor BL (2006) Genetic analysis of killer whale (Orcinus orca) historical bone and tooth samples to identify Western U.S. ecotypes. Mar Mamm Sci 22:897–909

    Article  Google Scholar 

  33. Natoli A, Peddemors VM, Rus-Hoelzel A (2004) Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. J Evol Biol 17:363–375

    CAS  Article  PubMed  Google Scholar 

  34. Oremus M, Garrigue C, Tezanos-Pinto G, Baker CS (2015) Phylogenetic identification and population differentiation of bottlenose dolphins (Tursiops spp.) in Melanesia, as revealed by mitochondrial DNA. Mar Mamm Sci 31:1035–1056

    Article  Google Scholar 

  35. Parra GJ, Ross G (2009) The Indo-Pacific humpback dolphin, Sousa chinensis. In: Perrin WF, Wursig B, Theweissen JGM (eds) Encyclopedia of marine mammals. Elsevier Press, New York

    Google Scholar 

  36. Perrin WF (2007) The South Africa species gate. In: Best PB (ed) Whales and dolphins of the Southern Africa Subregion. Cambridge University Press, New York

    Google Scholar 

  37. Saha A, Hauser L, Kent M, Planque B, Neat F, Kirubakaran TG, Huse I, Homrum EI, Fevolden S-E, Lien S, Johansen T (2015) Seascape genetics of saithe (Pollachius virens) across the North Atlantic using single nucleotide polymorphisms. ICES J Mar Sci 72:2732–2741

    Article  Google Scholar 

  38. Sarin MM, Krishaswami S, Dilli K, Somayajulu BLY, Moore WS (1989) Major ion chemistry of the Ganges-Brahmaputra river system: weathering processes and fluxes to the Bay of Bengal. Geochim Cosmochim Ac 53:997–1009

    CAS  Article  Google Scholar 

  39. Sarnblad A, Danbolt M, Dalen L, Amir OA, Berggren P (2011) Phylogenetic placement and population structure of Indo-Pacific bottlenose dolphins (Tursiops aduncus) off Zanzibar, Tanzania, based on mtDNA sequences. Mar Mamm Sci 27:431–448

    Article  Google Scholar 

  40. Selkoe KA, Watson JR, White C, Ben Horin T, Iacchei M, Mitarai S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726

    Article  PubMed  Google Scholar 

  41. Smith BD, Tun MT (2008) A note on the species occurrence, distributional ecology and fisheries management of cetaceans in the Mergui (Myeik) Archipelago, Myanmar. J Cetac Res Manag 10:37–44

    Google Scholar 

  42. Smith BD, Ahmed B, Mansur R et al (2008) Species occurrence and distributional ecology of nearshore cetaceans in the Bay of Bengal, Bangladesh, with abundance estimates for Irrawaddy dolphins, Orcaella brevirostris and finless porpoises Neophocaena phocaenoides. J Cetac Res Manag 10:37–44

    Google Scholar 

  43. Somayajulu YK, Murty VSN, Sarma YB (2003) Seasonal and inter-annual variability of surface circulation in the Bay of Bengal from TOPEX/Poseidon altimetry. Deep-Sea Res Part II 50:867–880

    Article  Google Scholar 

  44. Sutaria D, Jefferson TA (2004) Records of Indo-Pacific humpback Dolphins (Sousa chinensis, Osbeck, 1765) along the coasts of India and Sri Lanka: an overview. Aquat Mamm 30:125–136

    Article  Google Scholar 

  45. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Unger D, Ittekkot V, Schafer P, Tiemann J, Reschke S (2003) Seasonality and interannual variability of particle fluxes to the deep Bay of Bengal: influence of riverine input and oceanographic processes. Deep-Sea Res Part II 50:897–923

    Article  Google Scholar 

  47. Vogler C, Benzie J, Barber PH, Erdmann MV, Ambariyanto Sheppard C, Tenggardjaja K, Gerard K, Woerheide G (2012) Phylogeography of the crown-of-thorns starfish in the Indian Ocean. PLoS ONE 7(8):e43499

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:153–167

    Article  Google Scholar 

  49. Wang JY, Yang SC (2009) Indo-Pacific bottlenose dolphin, Tursiops aduncus. In: Perrin W, Wursig B, Thewissen J (eds) Encyclopedia of marine mammals. Elsevier Press, New York

    Google Scholar 

  50. Wang JY, Chou LS, White BN (1999) Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Mol Ecol 8:1603–1612

    CAS  Article  PubMed  Google Scholar 

  51. Wiszniewski J, Lusseau D, Moller LM (2010) Female bisexual kinship ties maintain social cohesion in a dolphin network. Anim Behav 80:895–904

    Article  Google Scholar 

  52. Young EF, Belchier M, Hauser L, Horsburgh GJ, Meredith MP, Murphy EJ, Pascoal S, Rock J, Tysklind N, Carvalho GR (2015) Oceanography and life history predict contrasting genetic population structure in two Antarctic fish species. Evol Appl 8:486–509

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research would not have been possible without the dedicated effort of WCS field assistants and our research boat crew especially Musa Kalimullah. Samples for this study were collected under permit from the Ministry of Environment and Forest, Bangladesh. We are grateful to Mr. Yunus Ali, Chief Conservator of Forest, Bangladesh, for his help with obtaining the CITES export permit for the skin samples used in this study as well as the NMFS Marine Mammals Health and Stranding Response Program for their assistance. Funding for this work was provided by the IWC Small Cetacean Conservation Fund Awarded and Ocean Park Conservation Foundation Hong Kong to BDS and HCR. We thank Dr. Paolo Agnelli, Mammals Collection Manager at the Natural History Museum, Zoological Section “La Specola”, University of Florence, Florence, Italy for access to the Andaman specimen and Kelly Robertson (SWFSC) for extracting and sequencing this specimen. A.R. Amaral is supported by a Grant (SFRH/BPD/79002/2011) from the Portuguese Science Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ana R. Amaral.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 525 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amaral, A.R., Smith, B.D., Mansur, R.M. et al. Oceanographic drivers of population differentiation in Indo-Pacific bottlenose (Tursiops aduncus) and humpback (Sousa spp.) dolphins of the northern Bay of Bengal. Conserv Genet 18, 371–381 (2017). https://doi.org/10.1007/s10592-016-0913-7

Download citation

Keywords

  • Genetic structure
  • mtDNA
  • Indo-Pacific humpback dolphin
  • Indo-Pacific bottlenose dolphin
  • Bangladesh