Worldwide mitochondrial DNA diversity and phylogeography of pilot whales (Globicephala spp.)

Abstract

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 (longfinned 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.

Bucking the trend: genetic analysis reveals high diversity, large population size and low differentiation in a deep ocean cetacean

“…In contrast, high genetic diversity is consistent with long-term stability in population size, whereas low levels of population differentiation suggest connectivity or recent population expansion. As a rule, cetaceans are known to have low genetic diversity in comparison with terrestrial mammals and this is hypothesized to be due to slow mutation rates (Jackson et al, 2009) and demographic factors such as recent population expansion following bottlenecks or behaviour (Oremus et al, 2009).…”

Unexpected patterns of global population structure in melon-headed whales Peponocephala electra

“…Haplotypic diversity in most strata (Table 2) was also higher than is typical for other blackfish (e.g. Amos et al 1993, Oremus et al 2009, Parsons et al 2013, Martien et al 2014. Haplotypic diversity was similar to that observed in smaller delphinids such as spinner dolphins (Oremus et al 2007, Andrews et al 2010, pantropical spotted dolphins Stenella attenuata (Escorza-Trevino et al 2005), and common bottlenose dolphins (Tezanos-Pinto et al 2009, Martien et al 2012, species that also do not exhibit deep mitochondrial divergences.…”

“…To determine whether the magnitude of mtDNA differentiation that we observed among MHW strata was comparable to that for other blackfish, we compared our Φ ST estimates to published estimates for resident killer whales (Parsons et al 2013), false killer whales (Martien et al 2014), long-finned pilot whales (Oremus et al 2009), and short-finned pilot whales (Oremus et al 2009, Van Cise et al 2016 ( Table S2 in the Supplement). We grouped the Φ ST values according to whether they were from comparisons of strata within the same ocean basin or between ocean basins and used Mann-Whitney U-tests to determine whether values were significantly lower in MHWs than in other blackfish.…”

“…Oremus et al 2009, Parsons et al 2013, Martien et al 2014, Van Cise et al 2016). However, our data did not reveal any such pattern.…”

“…For example, the cetacean subfamily Globicephalinae, commonly referred to as 'blackfish,' is comprised of several species of large, dark-colored dolphins, including killer whales Orcinus orca, false killer whales Pseudorca crassidens, pygmy killer whales Feresa attenuata, long-finned pilot whales Globicephala melas, and short-finned pilot whales G. macrorhynchus. Each of these species exhibits strong social structure and deep divergences within the mitochondrial genome, both within and between ocean basins (Bigg et al 1987, Amos et al 1993, Baird et al 2008, Oremus et al 2009, Morin et al 2010a, Parsons et al 2013, Martien et al 2014.…”