Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata

Abstract

How do populations of highly mobile species inhabiting open environments become reproductively isolated and evolve into new species? We test the hypothesis that elevated ocean-surface temperatures can facilitate allopatry among pelagic populations and thus promote speciation. Oceanographic modelling has shown that increasing surface temperatures cause localization and reduction of upwelling, leading to fragmentation of feeding areas critical to pelagic species. We test our hypothesis by genetic analyses of populations of two closely related baleen whales, the Antarctic minke whale (Balaenoptera bonaerensis) and common minke whale (Balaenoptera acutorostrata) whose current distributions and migration patterns extent are largely determined by areas of consistent upwelling with high primary production. Phylogeographic and population genetic analyses of mitochondrial DNA control-region nucleotide sequences collected from 467 whales sampled in four different ocean basins were employed to infer the evolutionary relationship among populations of B. acutorostrata by rooting an intraspecific phylogeny with a population of B. bonaerensis. Our findings suggest that the two species diverged in the Southern Hemisphere less than 5 million years ago (Ma). This estimate places the speciation event during a period of extended global warming in the Pliocene. We propose that elevated ocean temperatures in the period facilitated allopatric speciation by disrupting the continuous belt of upwelling maintained by the Antarctic Circumpolar Current. Our analyses revealed that the current populations of B. acutorostrata likely diverged after the Pliocene some 1.5 Ma when global temperatures had decreased and presumably coinciding with the re-establishment of the polar-equatorial temperature gradient that ultimately drives upwelling. In most population samples, we detected genetic signatures of exponential population expansions, consistent with the notion of increasing carrying capacity after the Pliocene. Our hypothesis that prolonged periods of global warming facilitate speciation in pelagic marine species that depend on upwelling should be tested by comparative analyses in other pelagic species.

A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences

“…Periods of global cooling with associated high upwelling intensities were alternated by extended periods of global warming (Zachos et al, 2001) during which upwelling areas (Schmittner, 2005;Fedorov et al, 2013;Ravelo et al, 2004) and related productivity (Diester-Haass et al, 2002;Marlow et al, 2000;Piela et al, 2012;Suto et al, 2012) were reduced. Hence, hypothetically, global warming may have resulted in fragmentation of the habitat of filter feeders, leading to different subpopulations eventually residing in smaller isolated regions, which may have facilitated speciation as suggested for the common minke whale (Balaenoptera acutorostrata) and Antarctic minke whale (B. bonaerensis) (Pastene et al, 2007). Our divergence estimates coincide broadly with several periods of global warming making such a mechanism conceivable for mobulids.…”

“…The upwelling hypothesis has also been proposed for the mysticeti whales, whose early evolution in Southern Oceans coincides with the initiation of the Antarctic Circumpolar Current, and associated high upwellingrelated productivity in this region during the Oligocene (Fordyce, 1980). Pastene et al (2007) suggested that periodic decreases in upwelling intensity through global warming could have facilitated allopatric speciation among pelagic populations of filter feeders. Upwelling has not been a stable phenomenon, but has waxed and waned following changes in the world's climate throughout the ages.…”

Update on the Cetacean Fauna of the Mediterranean Levantine Basin

“…This was confirmed by histopathology, which showed alveolar flooding consistent with aspiration or lung edema, all other tissue structure being within normal limits. Mitochondrial DNA control region sequencing found the male calf to be related to the north Atlantic stock of common minke whale [16]. Two other calf mortalities of unknown cause were investigated.…”

Ommastrephid squids Sthenoteuthis oualaniensis and Dosidicus gigas in the eastern Pacific show convergent biogeographic breaks but contrasting population structures

“…Population differentiation in cetaceans, for example, is frequently driven by opposite reproductive seasonality in northern and southern hemispheres (Hoelzel 1998, Pastene et al 2007). Data on seasonality and location of spawning by D. gigas are sparse but tantalizing.…”