Population genetics of Ice Age brown bears

Abstract

The major climatic changes that occurred toward the end of the late Pleistocene had an important influence on the evolution and distribution of extant taxa. However, the genetic consequences of these events have been difficult to determine (1–6). The brown bear is a large, Holarctic carnivore whose distribution was dramatically altered by late Pleistocene events. In North America, the brown bear has had a limited history, appearing in eastern Beringia only 50–70,000 years ago and spreading into the contiguous United States about 13,000 years ago (7, 8). Previous research on mitochondrial control region sequences from 317 extant brown bears found that they defined one European (I) and three distinct North American (II, IIIa/IIIb, IV) clades (9) (Figs. ​(Figs.11 and ​and22a). Bears with sequences from the basal and divergent clade II were restricted to the Admiralty, Baranof, and Chichagof (ABC) islands. Sequences from populations in northern Canada and Alaska fell in a clade comprising two closely related groups (IIIa and IIIb), whereas populations in southern Canada and the contiguous United States belonged to a southern clade (IV). Of 22 localities surveyed, none had sequences from more than one clade, with one exception, where IIIa and IIIb cooccurred (ref. 9, Fig. ​Fig.22a). Sequences from the western Alaskan clade (IIIa) also were found in Asia and northern and eastern Europe, suggesting a recent connection across the Bering Land Bridge (9, 10).

Figure 1

Maximum likelihood trees of brown bear control region and cytochrome b sequences. For simplicity, we use the clade I–IV nomenclature that was established previously (9), although in our smaller dataset several clades appear paraphyletic, particularly in the less well resolved cytochrome b tree. Extant sequences are in color [W (9), TS (10), TB (11)], and permafrost sequences (P1–P7) are in black. Reliability values (above nodes) and bootstrap percentages (below nodes) with values greater than 50% are indicated. Corrected radiometric dates (12) and reference numbers are as follows: P1, UCR3742/CAMS-51806 (15,370 ± 60 bp); P2, UCR3741/CAMS-51805 (14,980 ± 60 bp); P3, UCR3743/CAMS-54128 (13,760 ± 50 bp); P4, UCR3745/CAMS-54129 (15,680 ± 50 bp); P5, UCR3746/CAMS-54130 (42,850 ± 850); P6, UCR3744/CAMS-51808 (35,970 ± 660); and P7, Beta16162 (36,500 ± 1,150).

Figure 2

Current (A) and past geographic distribution of brown bear control region sequence clades 15,000 (B) and 35,000–45,000 (C) years ago. Locations of modern samples (9) are indicated by triangles. The asterisk indicates a brown bear fossil dated to greater than 40,000 years ago on Prince of Wales Island (16), and no fossils are known in the contiguous United States before 13,000 years. The approximate extent of glacial ice sheets 15,000 ago is superimposed on current continental boundaries in hatching (17).

The recent appearance of brown bears in North America and their division into four genetically distinct populations with highly divergent mitochondrial control region sequences implied separate invasions of North America from long-isolated Old World populations (9, 10). Clade II was postulated to represent the earliest invasion, followed by clades IV and IIIa/IIIb. Furthermore, the precise correspondence between geographic and phylogenetic divisions suggests three evolutionary significant units for conservation (9, 13) (clades II, III, and IV). In contrast, nuclear microsatellite data in Alaskan brown bears do not support long-term genetic isolation of the three Alaskan clades, suggesting the possibility of sex-biased dispersal (14).

Mammalian remains have been recovered from vast permafrost deposits in central Alaska and northwestern Canada as a consequence of placer gold-mine operations (8). More than 100,000 skeletal elements are preserved in collections at the American Museum of Natural History (AMNH), New York, and the Canadian Museum of Nature (CMN), Ottawa. Mitochondrial and nuclear DNA sequences have been amplified from several individual permafrost specimens, and cold conditions are thought to favor DNA survival (15). Therefore, museum collections of permafrost-preserved bones potentially represent an extensive genetic record of mammal populations over the past 50,000 years. To directly record changes in genetic diversity through the late Pleistocene, we examined nine unassociated, permafrost-preserved brown bear bones from localities about 400 km apart, near Fairbanks, Alaska, and Sixtymile, Yukon Territory (Fig. ​(Fig.22a).

Acknowledgments

Abbreviations

Note Added in Proof

Recent studies of permafrost remains have demonstrated that it is possible to amplify single copy nuclear sequences, including nuclear copies of mitochondrial genes (35). The latter is unlikely to be a factor in the current study as several different primer pairs and sequence regions produced consistent results.

Footnotes