Geographic and temporal dynamics of a global radiation and diversification in the killer whale

Abstract

Global climate change during the Late Pleistocene periodically encroached and then released habitat during the glacial cycles, causing range expansions and contractions in some species. These dynamics have played a major role in geographic radiations, diversification and speciation. We investigate these dynamics in the most widely distributed of marine mammals, the killer whale (Orcinus orca), using a global data set of over 450 samples. This marine top predator inhabits coastal and pelagic ecosystems ranging from the ice edge to the tropics, often exhibiting ecological, behavioural and morphological variation suggestive of local adaptation accompanied by reproductive isolation. Results suggest a rapid global radiation occurred over the last 350 000 years. Based on habitat models, we estimated there was only a 15% global contraction of core suitable habitat during the last glacial maximum, and the resources appeared to sustain a constant global effective female population size throughout the Late Pleistocene. Reconstruction of the ancestral phylogeography highlighted the high mobility of this species, identifying 22 strongly supported long-range dispersal events including interoceanic and interhemispheric movement. Despite this propensity for geographic dispersal, the increased sampling of this study uncovered very few potential examples of ancestral dispersal among ecotypes. Concordance of nuclear and mitochondrial data further confirms genetic cohesiveness, with little or no current gene flow among sympatric ecotypes. Taken as a whole, our data suggest that the glacial cycles influenced local populations in different ways, with no clear global pattern, but with secondary contact among lineages following long-range dispersal as a potential mechanism driving ecological diversification.

Morphological and ecological evidence for two sympatric forms of Type B killer whale around the Antarctic Peninsula

“…Their morphological and ecological variability likely represents adaptation to distinct foraging niches, and over time might be expected to lead to genetic structuring. Analysis of mitochondrial genomes from a global dataset of killer whales placed Type B whales sampled around the Antarctic Peninsula into a monophyletic mitochondrial lineage, which is a sister clade to the Type C killer whale form found on the other (eastern) side of the Antarctic continent (Morin et al 2015). However, Type B1 and B2 individuals sampled and sequenced to date do not share any mitochondrial haplotypes and appear to form two distinct subclades; they are also significantly differentiated at nuclear loci based on 91 nuclear single-nucleotide polymorphisms (Morin et al 2015), and based on a whole genome comparison (Foote et al in press).…”

“…However, genetic data suggest a relatively recent divergence of the B1 and B2 forms in Antarctica, following the release of habitat after the Last Glacial Maximum (see Morin et al 2015;Foote et al in press). Furthermore, in the NE Pacific, the dietary specializations between the ecotypes (e.g., mammal-eating ''Transients'' and the fish-eating ''Residents'') are well established (Ford et al 1998;Herman et al 2005), but further work is needed to elucidate the prey preferences and ecotypic distinction of B1 and B2 killer whales, and other Antarctic types (de Bruyn et al 2013).…”

Gene–culture coevolution in whales and dolphins

“…Best known are the three North Pacific ecotypes: a salmoneating specialist ecotype known as "residents," a mammaleating specialist or "transient" ecotype, and an "offshore" ecotype, which feeds upon sharks (20). All three ecotypes cluster in distinct mitochondrial and nuclear genome clades (33,34) that diverged a few hundred thousand years ago (35). We have less complete information for the Antarctic, but there appear to be five ecotypes respectively specializing on minke whales (Balaenoptera acutorostrata) (ecotype A), seals (ecotype B1), penguins (ecotype B2), and fish (ecotype C and perhaps ecotype D) (20).…”

“…We have less complete information for the Antarctic, but there appear to be five ecotypes respectively specializing on minke whales (Balaenoptera acutorostrata) (ecotype A), seals (ecotype B1), penguins (ecotype B2), and fish (ecotype C and perhaps ecotype D) (20). These Antarctic ecotypes seem to have diverged more recently than those in the North Pacific, and ecotypes B1, B2, and C, at least, are part of a distinct and relatively shallow Antarctic clade (34,35). The distinctions between the ecotypes have led Morin et al to suggest that they should be considered separate species or subspecies (36), but this proposal has not been formally implemented.…”

“…In fewer than 10,000 generations, killer whales have radiated from a single ancestral lineage to colonize regions from the Arctic to the Antarctic and all waters in between (34,35). Until humans reached Antarctica, killer whales were the most widely distributed mammals and likely were subject to a diverse range of selective pressures associated with different habitats.…”