Gene flow on ice: the role of sea ice and whaling in shaping Holarctic genetic diversity and population differentiation in bowhead whales (Balaena mysticetus)

Abstract

Sea ice is believed to be a major factor shaping gene flow for polar marine organisms, but it remains unclear to what extent it represents a true barrier to dispersal for arctic cetaceans. Bowhead whales are highly adapted to polar sea ice and were targeted by commercial whalers throughout Arctic and subarctic seas for at least four centuries, resulting in severe reductions in most areas. Both changing ice conditions and reductions due to whaling may have affected geographic distribution and genetic diversity throughout their range, but little is known about range-wide genetic structure or whether it differed in the past. This study represents the first examination of genetic diversity and differentiation across all five putative stocks, including Baffin Bay-Davis Strait, Hudson Bay-Foxe Basin, Bering-Beaufort-Chukchi, Okhotsk, and Spitsbergen. We also utilized ancient specimens from Prince Regent Inlet (PRI) in the Canadian Arctic and compared them with modern stocks. Results from analysis of molecular variance and demographic simulations are consistent with recent and high gene flow between Atlantic and Pacific stocks in the recent past. Significant genetic differences between ancient and modern populations suggest PRI harbored unique maternal lineages in the past that have been recently lost, possibly due to loss of habitat during the Little Ice Age and/or whaling. Unexpectedly, samples from this location show a closer genetic relationship with modern Pacific stocks than Atlantic, supporting high gene flow between the central Canadian Arctic and Beaufort Sea over the past millennium despite extremely heavy ice cover over much of this period.

Keywords: Ancient DNA; arctic; cetacean; marine mammal; mitochondrial DNA; whaling.

Figure 1

(a) The full range of bowhead whales across the Arctic (lightly shaded area; Laidre et al. 2008) with sample sizes from region. Italicized names represent data collected in this study. Area inside dotted line shows the location of (b) detailed map of the Canadian Arctic. 1 = McClintock Sound, 2 = Qariaraqyak (PaJS-2) (archeological site from which “PRI” samples were excavated), 3 = Somerset Island, 4 = Prince Regent Inlet, 5 = Fury and Hecla Strait. Also shown are maximum (March – lightest gray) and minimum (September – white) sea-ice extent for 1979 (the earliest year data are available from NSIDC).

Figure 2

Minimum spanning network for bowhead whale haplotypes created using TCS. Size of circle is proportional to number of samples; hatchmarks represent additional segregating sites.

Figure 3

Simulated and empirical pairwise ΦST values between putative populations for m = 0.1. Vertical lines show 95% highest posterior density (HPD) intervals for simulated ΦST values; top and bottom of box indicate 75% HPD intervals and thick horizontal lines show median values for simulations. Dotted horizontal lines show empirically observed pairwise ΦST values. CG = Canada-Greenland (BBDS and HBFB combined). (a) Scenario A; (b) Scenario B; (c) Scenario C; (d) Scenario D (see text for details).

Figure A1

Cartoon representation of demographic scenarios used in simulations (see text). [Boundaries shown below are intended to convey the general geographic location for putative populations, and are not intended in any way to represent the shape or extent of the range of those populations.]