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Phylogenetic relationships in southern African Bryde’s whales inferred from mitochondrial DNA: further support for subspecies delineation between the two allopatric populations

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Abstract

Bryde’s whales (Balaenoptera edeni) are medium-sized balaenopterids with tropical and subtropical distribution. There is confusion about the number of species, subspecies and populations of Bryde’s whale found globally. Two eco-types occur off South Africa, the inshore and offshore forms, but with unknown relationship between them. Using the mtDNA control region we investigated the phylogenetic relationship of these populations to each other and other Bryde’s whale populations. Skin, baleen and bone samples were collected from biopsy-sampled individuals, strandings and museum collections. 97 sequences of 674 bp (bp) length were compared with published sequences of Bryde’s whales (n = 6) and two similar species, Omura’s (B. omurai) and sei (B. borealis) whales (n = 3). We found eight haplotypes from the study samples: H1–H4 formed a distinct, sister clade to pelagic populations of Bryde’s whales (B. brydei) from the South Pacific, North Pacific and Eastern Indian Ocean. H5–H8 were included in the pelagic clade. H1–H4 represented samples from within the distributional range of the inshore form. Pairwise comparisons of the percentage of nucleotide differences between sequences revealed that inshore haplotypes differed from published sequences of B. edeni by 4.7–5.5% and from B. brydei by 1.8–2.1%. Ten fixed differences between inshore and offshore sequences supported 100% diagnosability as subspecies. Phylogenetic analyses grouped the South African populations within the Bryde’s-sei whale clade and excluded B. edeni. Our data, combined with morphological and ecological evidence from previous studies, support subspecific classification of both South African forms under B. brydei and complete separation from B. edeni.

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Acknowledgements

Logistics and funding to cover fieldwork and laboratory costs were provided by The Centre for Dolphin Studies, Rufford Foundation, Society for Marine Mammalogy, Mammal Research Institute Whale Unit (University of Pretoria), Sea Mammal Research Unit (University of St Andrews) and several international interns. We thank the staff and students of St Andrews and Stellenbosch University’s molecular labs, in particular Tanya Sneddon, for many hours of laboratory support, and Mike Double from the Australian Marine Mammal Centre for sequencing the sample from Madagascar. A large contribution of samples from the Port Elizabeth and Iziko South African Museum collections greatly increased the sample coverage, as did two samples from stranded Bryde’s whales collected by the Namibian Dolphin Project. Thank you to John Bannister for organising the CITES permit from Australia, and to Curt and Micheline Jenner for inviting GSP on board their research vessel Whale Song and collecting additional samples for this study. The collection and movement of samples was carried out under permits issued by the Department of Environmental Affairs (South Africa), CITES and DEFRA (UK). Finally, thanks to Theoni Photopoulou and Tsamaelo Malebu for assisting with the maps, Maria João Janeiro Silva and Carolin Kosiol for analytical software assistance, and Tim Collins and the reviewers for constructive comments that improved the final version of this paper.

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Authors and Affiliations

  1. Department of Zoology, Nelson Mandela University, PO Box 77000, Port Elizabeth, 6031, South Africa

    Gwenith S. Penry & Victor G. Cockcroft

  2. Sea Mammal Research Unit, Scottish Oceans Institute, University of St Andrews, St Andrews, KY16 8LB, Fife, United Kingdom

    Gwenith S. Penry, Philip S. Hammond & Jeff A. Graves

  3. Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Pretoria, 0028, South Africa

    Gwenith S. Penry, Peter B. Best & Meredith Thornton

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  1. Gwenith S. Penry
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  2. Philip S. Hammond
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  3. Victor G. Cockcroft
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  4. Peter B. Best
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Correspondence to Gwenith S. Penry.

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We dedicate this manuscript to Dr. Peter B. Best who established an impressive foundation of information on the two forms of Bryde’s whale occurring off southern Africa. We are pleased to have molecular support for what he suspected nearly 40 years ago and are eternally grateful for his dedication to South African marine mammal science.

Appendices

Appendix 1

See Table 8.

Table 8 Specimen number, source, type of material, date of collection and location where the sample was collected are given
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Appendix 2

The history of samples 37 and 38, recounted by PBB

A male Bryde’s whale foetus (#37) ca 35 cm long was presented to ISAM as having belonged to T. Haraldsen, ex-captain of the “pirate” whaling catcher-factory ship MV Sierra. As this vessel’s operations were largely concentrated on the offshore population of Bryde’s whales on the west coast of southern Africa (Best 1996), and for security reasons excluded inshore waters on the South African coast, it is highly likely that this specimen originated from the offshore population, and it was treated such in analysis.

On 11 December 1983, a 14.7 m male Bryde’s whale was found floating dead but fresh in Ben Schoeman dock, Table Bay harbour. Its skin was intact and bore a large number of healed oval scars on the peduncle and flanks. There was also a large vertical abrasion about mid-length on the left side, suggestive of a ship strike. It was towed out to sea on the same day, but washed up on 15 December at Koeberg Power station, 40 km to the north. It was measured on 16 December, a testis collected and measured (41.5 × 12.5 × 6 cm) with cestode Phyllobothrium cysts recorded in the blubber, and a section of baleen plates collected before the carcase was buried on the beach. The baleen was presented to the museum in February 1984 and accessioned as ZM 39958 (#38).

The size, scarring and timing all indicate that this was most likely to be a representative of the offshore population that was struck by a ship at sea and carried inadvertently on its bow into the docks. Unfortunately, the baleen was either never labelled or subsequently lost its accession tag, but during a search of the ISAM collection in 2011 a section of unlabelled baleen was found that in description closely matched that of ZM 39958, and this was sampled on that assumption.

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Penry, G.S., Hammond, P.S., Cockcroft, V.G. et al. Phylogenetic relationships in southern African Bryde’s whales inferred from mitochondrial DNA: further support for subspecies delineation between the two allopatric populations. Conserv Genet 19, 1349–1365 (2018). https://doi.org/10.1007/s10592-018-1105-4

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