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Worldwide Mitochondrial DNA Diversity and Phylogeography of Pilot Whales (Globicephala Spp.)

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Worldwide Mitochondrial DNA Diversity and Phylogeography of Pilot Whales (Globicephala Spp.) Biological Journal of the Linnean Society, 2009, 98, 729–744. With 4 figures Worldwide mitochondrial DNA diversity and phylogeography of pilot whales (Globicephala spp.) MARC OREMUS1*, ROSEMARY GALES2, MEREL L. DALEBOUT1,3, NAOKO FUNAHASHI4, TETSUYA ENDO5, TAKAHIRO KAGE6, DEBBIE STEEL1,7 and SCOTT C. BAKER1,7 1School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland, New Zealand 2Resource Management and Conservation Division, DPIW, GPO Box 44, Hobart, Tasmania 7001, Australia 3School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia 4Japan representative, International Fund for Animal Welfare, 1-2-10 Koyama, Higashi Kurume-shi, Tokyo 203-0051, Japan 5Faculty of Pharmaceutical Sciences, Health Sciences University of Hokkaido, 1757 Ishikari-Tobetsu, Hokkaido 061-0293, Japan 6Mie University, 1577 Kurimamachiya-cho, Tsu City, Mie Prefecture, Japan 514-8507 7Marine Mammal Institute and Department of Fisheries and Wildlife, Hatfield Marine Science Center, 2030 SE Marine Science Drive, Oregon State University, Newport, OR 97365, USA Received 25 February 2009; accepted for publication 25 June 2009bij_1325 729..744 Pilot whales (Globicephala spp.) provide an interesting example of recently diverged oceanic species with a complex evolutionary history. The two species have wide but largely non-overlapping ranges. Globicephala melas (long- finned pilot whale; LFPW) has an antitropical distribution and is found in the cold-temperate waters of the North Atlantic and Southern Hemisphere, whereas Globicephala macrorhynchus (short-finned pilot whale; SFPW) has a circumglobal distribution and is found mainly in the tropics and subtropics. To investigate pilot whale evolution and biogeography, we analysed worldwide population structure using mitochondrial DNA (mtDNA) control region sequences (up to 620 bp) from a variety of sources (LFPW = 643; SFPW = 150), including strandings in New Zealand and Tasmania, and whale-meat products purchased on the markets of Japan and Korea. Phylogenetic reconstructions failed to support a reciprocal monophyly of the two species, despite six diagnostic substitutions, possibly because of incomplete lineage sorting or inadequate phylogenetic information. Both species had low haplotype and nucleotide diversity compared to other abundant widespread cetaceans (LFPW, p=0.35%; SFPW, p=0.87%) but showed strong mtDNA differentiation between oceanic basins. Strong levels of structuring were also found at the regional level. In LFPW, phylogeographic patterns were suggestive either of a recent demographic expansion or selective sweep acting on the mtDNA. For SFPW, the waters around Japan appear to represent a centre of diversity, with two genetically-distinct forms, as well as a third population of unknown origin. The presence of multiple unique haplotypes among SFPW from South Japan, together with previously documented morphological and ecological differences, suggests that the southern form represents a distinct subspecies and/or evolutionary significant unit. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 729–744. ADDITIONAL KEYWORDS: biogeography – cetacean – evolution – taxonomy. *Corresponding author. E-mail: [email protected] © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 729–744 729 730 M. OREMUS ET AL. INTRODUCTION Collado & Agnarsson, 2006), although only one or two individuals were used to represent each taxon in these Among cetaceans (whales, dolphins, and porpoises), studies. The two species are widely distributed but limits to gene flow are complex and considered to largely parapatric, except in the North Pacific where be the result of behavioural specializations, social the LFPW is now absent (see below; Fig. 1). There are organization, and historical environmental changes no global estimates of abundance, although several (Hoelzel, 1998). However, because studies of ceta- regional estimates suggest that they are relatively ceans, particularly open-ocean species, are challeng- numerous worldwide (e.g. 778 000 LFPW in Northeast ing, their demography and evolutionary history is Atlantic: Buckland et al., 1993; 160 200 SFPW in often unresolved or incompletely known (Whitehead, Eastern tropical Pacific: Wade & Gerrodette, 1993). Christal & Tyack, 2000; Cipriano, 2002). For the Pilot whales are amongst the most gregarious of family Delphinidae (oceanic dolphins, including pilot cetaceans, often found in groups of up to several whales Globicephala spp.), these issues are further hundred individuals, although the average group size obscured by the relatively recent evolutionary origins is generally around 20 whales (Bernard & Reilly, of this group (LeDuc, Perrin & Dizon, 1999). On the 1994). Their social system is assumed to be matrilin- basis of the fossil record, the Delphinidae appear to eal, with groups consisting of several generations have arisen approximately 11 Mys (Barnes, 1985), of maternally-related individuals (Kasuya & Marsh, and subsequently underwent a rapid radiation, such 1984; Amos, Schlötterer & Tautz, 1993; Heimlich- that there has been comparatively little time for Boran, 1993). They are well-known for their highly diagnostic morphological or genetic characters to cohesive behaviour, allowing them to be herded to evolve between species. shore by a small number of boats during ‘drive–kill’ The two recognized species of the genus Globi- fisheries in the Faroe Islands and Japan. This strong cephala provide an interesting example of a recent and social cohesion is also considered to be the reason complex evolutionary history. The long-finned pilot behind their propensity for mass stranding (Perrin & whale (LFPW; Globicephala melas, Traill 1809) and Geraci, 2002). As with other matrilineal odontocetes the short-finned pilot whale (SFPW; Globicephala (toothed whales), such as the killer whales (Orcinus macrorhynchus, Gray 1846) are widely-distributed, orca) and the sperm whales (Physeter macrcephalus), abundant species of large dolphins (up to 7 m for adult Globicephala spp. reportedly show low diversity at males). Although similar in external appearance, a the maternally-inherited mtDNA (Siemann, 1994; number of features, in particular the shape of the Whitehead, 1998). To date, however, low mtDNA skull, validate the distinctiveness of the two species diversity has only been demonstrated in the North (van Bree, 1971). Phylogenetic analyses of mitochon- Atlantic population of pilot whales (Siemann, 1994). drial DNA (mtDNA) cytochrome b sequences also LFPWs inhabit the cold temperate waters of the supports their species status (LeDuc et al., 1999; May- North Atlantic and the Southern Hemisphere, such North Atlantic n = 70/18 Japan/Korea n = 98/41 eastern North Pacific n = 2/2 Atlantic n = 12/8 South Pacific n = 38/10 Tasmania n = 215/6 New Zealand n = 358/43 Figure 1. Global distribution of Globicephala spp., with number and source locations of samples used in the present study (n, full dataset/adjusted dataset, see text for details). Diagonal strips, long-finned pilot whale (Globicephala melas); dark grey, short-finned pilot whale (Globicephala macrorhynchus). Map taken from Olson & Reilly (2002). © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 729–744 WORLDWIDE mtDNA OF PILOT WHALES 731 that there are two widely-separated, anti-tropical and relationships between the two putative subspe- populations (Fig. 1). On the basis of differences in cies, and (2) for the SFPW, the evolutionary history of colour pattern, populations in the North Atlantic and northern and southern forms around Japan, and their Southern Hemisphere have been described as differ- relationship to populations in other regions. ent species by Rayner (1939). However, Davies (1960) reduced this distinction to the sub-species level, with Globicephala melas melas in the North Atlantic and MATERIAL AND METHODS Globicephala melas edwardii in the Southern Hemi- SAMPLE COLLECTION AND ADDITIONAL SEQUENCES sphere, arguing that the last contact between the two LFPW current subspecies could have occurred only 10 000– A total of 573 tissue samples were collected from 15 000 years ago during the last Pleistocene glacia- whales involved in 19 singleton and 19 mass strand- tion, when equatorial waters were substantially ings (i.e. two or more individuals stranding together cooler. Although LFPWs are now absent in the North that are not mother-calf pairs) around New Zealand Pacific, sub-fossil and fossil skulls identified as this and Tasmania, Australia (Fig. 1; for full details of species have also been found at several archaeological all samples, see Supporting information, Table S1). sites in Japan (dating from the 8th to 12th Centuries, Three additional mtDNA control region haplotypes Kasuya (1975) and Alaska (dating from 3500–2500 representing a total of 70 whales from strandings years BP, Frey, Crockford & Meyer, 2005), suggesting and incidental fisheries takes (by-catch) in the a recent extinction in this ocean basin. North Atlantic were obtained from Siemann (1994) SFPWs range across the tropical and warm- (Genbank numbers U20926–U20928). temperate waters of the Atlantic, Pacific, and Indian Ocean (Fig. 1). In the western North Pacific, off the SFPW coast of Japan, distinct ‘southern’ and ‘northern’ forms A total of 39 tissue samples were collected from SFPW have been described on the basis of morphological, in the South Pacific (New
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