Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Phylogenetic analysis of mtDNA sequences suggests revision of humpback dolphin (Sousa spp.) taxonomy is needed

Céline H. Frère A E , Peter T. Hale B , Lindsay Porter C , Victor G. Cockcroft D and Merel L. Dalebout A

A School of Biological, Earth and Ecological Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

B School of Integrative Biology, University of Queensland, Brisbane, Qld 4072, Australia.

C Worldwide Fund for Nature, 1 Tramway Path, Central, Hong Kong.

D Centre for Dolphin Studies, PO Box 1856, Plettenberg Bay, South Africa 6600.

E Corresponding author. Email: c.frere@uq.edu.au

Marine and Freshwater Research 59(3) 259-268 http://dx.doi.org/10.1071/MF07120
Submitted: 25 June 2007  Accepted: 3 March 2008   Published: 30 April 2008

Abstract

Humpback dolphins (Sousa spp.) have a wide distribution in the tropical Atlantic and Indo-Pacific Oceans and a confused taxonomy. Morphological assessments suggest three species groupings – Sousa teuszii (eastern Atlantic), Sousa plumbea (western Indo-Pacific), and Sousa chinensis (eastern Indo-Pacific) – but most taxonomies recognise only two species – S. chinensis (Indo-Pacific), and S. teuszii (Atlantic). To investigate phylogenetic relationships, mitochondrial DNA control region sequences (338 base pairs) from 72 Sousa representing three populations in the Indo-Pacific (South Africa: S. plumbea, n = 23; China: S. chinensis, n = 19; and Australia: S. chinensis, n = 28), and S. teuszii in the Atlantic (Mauritania, n = 2) were generated. All three Indo-Pacific populations formed robust, monophyletic clades with high bootstrap (BS) and Bayesian posterior probability (BPP) scores. Surprisingly, humpback dolphins from South Africa and China formed a strongly-supported clade with the Atlantic S. teuszii (BS 63%, BPP 0.92) to the exclusion of animals from Australia. Genetic divergence between animals from China and Australia (DA = 8.4% ± 2.47%) was greater than between China and South Africa (DA = 5.1% ± 1.80%). These results strongly suggest that Australian humpback dolphins are not S. chinensis but may represent a distinct species in their own right.

Additional keywords: Australia, Delphininae, Hong Kong, phylogeography, South Africa, speciation.


References

Akaike H. (1973). Information theory and an extension of the maximum likelihood principle. In ‘Second International Symposium on Information Theory’. pp. 267–281. (Akademiai Kiado: Budapest.)

Anon.  (2000). ‘Whale and dolphin conservation in the Great Barrier Reef Marine Park: policy document.’ (The Great Barrier Reef Marine Park Authority: Townsville, Queensland.)

Baker C. S., and Medrano-Gonzalez L. (2002). World-wide distribution and diversity of humpback whale mitochondrial DNA lineages. In ‘Cell and Molecular Biology of Marine Mammals’. (Ed. C. J. Pfeiffer.) pp. 84–99. (Krieger Publishing: Malabar, FL.)

Bannister J. L., Kemper C. M., and Warneke R. M. (1996). ‘The Action Plan for Australian Cetaceans.’ (Australian Nature Conservation Agency: Canberra, Australian Capital Territory.)

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

Beasley I.Robertson K. M.Arnold P.2005Description of a new dolphin, the Australian snubfin Orcaella heinsohni sp. n. (Cetacea, Delphinidae).Marine Mammal Science21365400doi:10.1111/J.1748-7692.2005.TB01239.X

Caballero S.Trujillo F.Vianna J. A.Barrios-Garrido H.Montiel M. G.et al.2007Taxonomic status of the genus Sotalia: Species level ranking for “tucuxi” (Sotalia fluviatilis) and “costero” (Sotalia guianensis) dolphins.Marine Mammal Science23358386doi:10.1111/J.1748-7692.2007.00110.X

Cockcroft V. G., and Smith-Goodwin J. (2002). ‘The phylogeny of the humpback dolphins Genus Sousa.’ Report to the Scientific Committee of the International Whaling Commission (IWC SC/54/SM23). The Red House, Cambridge.

Cockcroft V. G., Leatherwood S., Goodwin J., and Porter L. J. (1997). ‘The phylogeny of humpback dolphins Genus Sousa: insights through mtDNA analyses.’ Report to the Scientific Committee of the International Whaling Commission (SC/49/SM25). The Red House, Cambridge.

Dalebout M. L.Mead J. G.Baker C. S.Baker A. N.van Helden A. L.2002A new species of beaked whale Mesoplodon perrini sp. n. (Cetacea: Ziphiidae) discovered through phylogenetic analyses of mitochondrial DNA sequences.Marine Mammal Science18577608doi:10.1111/J.1748-7692.2002.TB01061.X

Dalebout M. L.Baker C. S.Mead J. G.Cockcroft V. G.Yamada T. K.2004A comprehensive and validated molecular taxonomy of beaked whales, Family Ziphiidae.The Journal of Heredity95459473doi:10.1093/JHERED/ESH054Pubmed Abstract

Davis J. I.Nixon K. C.1992Populations, genetic variation and the delimitation of phylogenetic species.Systematic Biology41421435doi:10.2307/2992584

Davis L. G., Dibner M. D., and Battey J. F. (1986). ‘Basic Methods in Molecular Biology.’ (Elsevier: New York.)

Frère H. C. (2002). ‘Molecular Taxonomy and Population Genetic Processes in the Genus Sousa.’ Honours Thesis, University of Queensland, Brisbane.

Goodwin J. A. (1997). ‘A molecular genetic assessment of the population structure and variation of two inshore dolphin genera on the east coast of South Africa.’ PhD Thesis, Rhodes University, Grahamstown, South Africa.

Hillis D. M.Bull J. J.1993An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis.Systematic Biology42182192doi:10.2307/2992540

Hoelzel A. R.Hancock J. M.Dover G. A.1991Evolution of the cetacean mitochondrial D-loop region.Molecular Biology and Evolution8475493Pubmed Abstract

Holloway J. D., and Hall R. (1998). SE Asian geology and biogeography: an introduction. In ‘Biogeography and Geological Evolution of SE Asia’. (Eds R. Hall and J. D. Holloway.) pp. 1–23. (Backhuys Publishers: Leiden, the Netherlands.)

Huelsenbeck J. P.Ronquist F.2001MRBAYES: Bayesian inference of phylogenetic trees.Bioinformatics (Oxford, England)17754755doi:10.1093/BIOINFORMATICS/17.8.754Pubmed Abstract

IWC2006Appendix 3: Classification of the order Cetacea (whales, dolphins and porpoises).Journal of Cetacean Research and Management8512

Jefferson T. A.2000Population Biology of the Indo-Pacific hump-backed dolphin in Hong Kong Waters.Wildlife Monographs144165


Jefferson T. A.Karczmarski L.2001Sousa chinensis.Mammalian Species65519
doi:10.1644/1545-1410(2001)655<0001:SC>2.0.CO;2

Jefferson T. A.Van Waerebeek K.2004Geographic variation in skull morphology of humpback dolphins (Sousa spp.).Aquatic Mammals30317doi:10.1578/AM.30.1.2004.3

Kumar S.Tamura K.Nei M.2004MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment.Briefings in Bioinformatics5150163doi:10.1093/BIB/5.2.150Pubmed Abstract

Larson A. (1989). The relationship between speciation and morphological evolution. In ‘Speciation and its Consequences’. (Eds D. Otte and J. A. Endler.) pp. 579–598. (Sinauer Associates: Sunderland, MA.)

Le Duc R. G.Perrin W. F.Dizon A. E.1999Phylogenetic relationships among the delphinid cetaceans based on full cytochrome b sequences.Marine Mammal Science15619648doi:10.1111/J.1748-7692.1999.TB00833.X

Lydekker R.1901Notice of an apparently new estuarine dolphin from Borneo.Proceedings of the Zoological Society of London18891

Maddison W. P., and Maddison D. R. (1992). ‘MacClade (Release version 3.04): Analysis of Phylogeny and Character Evolution.’ (Sinauer Associates: Sunderland, MA.)

May-Collado L.Agnarsson I.2006Cytochrome b and Bayesian inference of whale phylogeny.Molecular Phylogenetics and Evolution38344354
doi:10.1016/J.YMPEV.2005.09.019Pubmed Abstract

Milinkovitch M. C., Le Duc R., Tiedemann R., and Dizon A. (2002). Applications of molecular data in cetacean taxonomy and population genetics with special emphasis on defining species boundaries. In ‘Marine Mammals: Biology and Conservation’. (Eds P. G. H. Evans and J. A. Raga.) pp. 325–359. (Kluwer Academic-Plenum Publishers: Dordrecht, NY.)

Moritz C. (1994). Defining ‘evolutionary significant units’ for conservation. Tree 9, 373–375.

Nei M. (1987). ‘Molecular Evolutionary Genetics.’ (Columbia University Press: New York.)

Osbeck P. (1765). ‘Reise nach Ostindien und China.’ (Koppe: Rostock, Germany.)

Parra G. J. (2005). ‘Behavioural ecology of Irrawaddy, Orcaella brevirostris (Owen in Gray, 1866), and Indo-Pacific humpback dolphins, Sousa chinensis (Osbeck, 1765), in northeast Queensland, Australia: a comparative study.’ PhD Thesis, James Cook University, Cairns, Australia.

Parra G., and Ross G. J. B. (2008). Humpback dolphins. In ‘Encyclopedia of Marine Mammals’. 2nd edn. (Eds W. F. Perrin, B. Wursig and J. G. M. Thewissen.) (Academic Press: San Diego, CA.)

Parra G. J.Corkeron P. J.Marsh H.2006aPopulation sizes, site fidelity and residence patterns of Australian snubfin and Indo-Pacific humpback dolphins: Implications for conservation.Biological Conservation129167180doi:10.1016/J.BIOCON.2005.10.031

Parra G. J.Schick R.Corkeron P. J.2006bSpatial distribution and environmental correlates of Australian snubfin and Indo-Pacific humpback dolphins.Ecography29396406doi:10.1111/J.2006.0906-7590.04411.X

Perrin W. F., Reeves R. R., Dolar M. L. L., Jefferson T. A., Marsh H., Wang J. Y., et al. (Eds) (2005). ‘Report on the Second Workshop on the Biology and Conservation of Small Cetaceans and Dugongs of South-east Asia.’ (Convention on Migratory Species (CMS) Technical Series Publication No. 9, UNEP/CMS Secretariat: Bonn, Germany.)

Pilleri G.Gihr M.1972Contribution to the knowledge of the cetaceans of Pakistan with particular reference to the genera Neomeris, Sousa, Delphinus, and Tursiops, and the description of a new Chinese porpoise (Neomeris asiaorientalis).Investigations on Cetacea4107162

Posada D.2006Modeltest Server: a web-based tool for the statistical selection of models of nucleotide substitutions online.Nucleic Acids Research34W700W703
doi:10.1093/NAR/GKL042Pubmed Abstract

Posada D.Buckley T. R.2004Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests.Systematic Biology53793808doi:10.1080/10635150490522304Pubmed Abstract

Posada D.Crandall K. A.1998MODELTEST: testing the model of DNA subsitution.Bioinformatics Applications Note14817818

Ptacek M. B.2000The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates.Behavioural Processes51111134
doi:10.1016/S0376-6357(00)00123-6Pubmed Abstract

Rannala B.Yang Z.1996Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference.Journal of Molecular Evolution43304311doi:10.1007/BF02338839Pubmed Abstract

Reeves R. R., Smith B. D., Crespo E. A., and Notarbartolo di Sciara G. (2003). ‘Dolphins, Whales and Porpoises: 2002–2010. Conservation Action Plan for the World’s Cetaceans.’ IUCN Cetacean Specialist Group. (IUCN: Gland, Switzerland and Cambridge, UK.)

Reeves R. R., Perrin W. F., Taylor B. L., Baker C. S., and Mesnick S. L. (2004). ‘Report of the Workshop on Shortcomings of Cetacean Taxonomy in Relation to Needs of Conservation and Management, April 30–May 2, 2004. La Jolla, California.’ (NOAA Technical Memorandum, NOAA-TM-NMFS-SWFSC-363: San Diego, CA.)

Rice D. W. (1998). ‘Marine Mammals of the World. Systematics and Distribution.’ (The Society of Marine Mammalogy Special Publication No. 4: Lawrence, KA.)

Rosenbaum H. C.Brownell R. L.JrBrown M. W.Schaeff C.Portway V.et al.2000World-wide genetic differentiation of Eubalaena: questioning the number of right whale species.Molecular Ecology917931802doi:10.1046/J.1365-294X.2000.01066.XPubmed Abstract

Rosenbaum H., Glaberman S., Jefferson T., Collins T., Minton G., Peddemors V., et al. (2002). ‘Phylogenetic Relationships and Population Structure Among Sousa spp. Based on mtDNA Variation.’ (Report to the Scientific Committee of the International Whaling Commission (SC/54/SM34). The Red House, Cambridge.)

Ross G. J. B. (2002). Humpback Dolphins. In ‘Encyclopedia of Marine Mammals’. (Eds W. F. Perrin, B. Wursig and J. G. M. Thewissen.) pp. 585–589. (Academic Press: San Diego, CA.)

Ross G. J. B., Hensohn G. E., and Cockcroft V. G. (1994). Humpback dolphins Sousa chinensis (Osbeck 1765), Sousa plumbea (G. Cuvier 1829), and Sousa teuszii (Kukenthal 1892). In ‘Handbook of Marine Mammals, Volume 5’. (Eds S. H. Ridgeway and R. Harrison.) pp. 24–42. (Academic Press: London.)

Ross G. J. B., Heinsohn G. E., Cockcroft V. G., Parsons E. C. M., Porter L., and Preen A. (1995). ‘Review of the taxonomic status of humpback dolphins, genus Sousa. (UNEP/SEA95/WP19).’ (Paper presented at the Workshop on the Biology and Conservation of Small Cetaceans and Dugongs of Southeast Asia. Dumaguete, Philippines.)

Swofford D. L. (1999). ‘PAUP*: Phylogenetic Analysis using Parsimony *and other phylogenetic reconstruction methods.’ (Sinauer Associates: Sunderland, MA.)



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