Analysis of new fossil material of Protarctos abstrusus from the North America High Arctic shows that, although ecomorphologically similar to the modern North American black bear (Ursus americanus), P. abstrusus represents a basal ursine. The most prominent cranial features of P. abstrusus are its relatively short rostrum, flat forehead above the orbit, and high sagittal crest that extends posteriorly and overhangs the occipital condyles (Fig. 9), characters that generally signal primitive status within Ursinae. P. abstrusus appears to have been an isolated immigration event from Eurasia to North America, separate from Ursus, representing a time of Asian-North American high latitude floral and faunal interchange32, when the high-latitude forests of Asia and North America were connected across the Beringian isthmus.

Figure 9 Artist restoration of lateral view of skull and lower jaw of Protarctos abstrusus based on a composite of partial skull (CMN 54380) and right dentary (CMN 52078-B). Missing bones (ascending ramus, mandibular condyle, and angular process) are based on living black bears. Missing teeth (I2-3, P1-3, i2-3, p1-3, and m3) are restored based on their alveoli. The stage of wear on the lower teeth is drawn to match with those of the upper teeth. Art by Xiaoming Wang. Full size image

The American black bear, by contrast, appears in the North America fossil record in the Early Pleistocene as a result of an independent dispersal event from Eurasia. Fossil records of true American black bear, Ursus americanus Pallas, range from Irvingtonian to late Rancholabrean44,45. From the Irvingtonian age, Brown46 described abundant materials from the Conard Fissure, Arkansas, which he referred to U. americanus. Gidley47 named Ursus (Euarctos) vitabilis from the Cumberland Cave, Maryland, which was later referred to Euarctos vitabilis 48. By late Rancholabrean black bears appear widespread throughout North America49. Several species or subspecies of late Pleistocene black bears have been named, which were sometimes confused with brown bears because of overlap in size and pronounced sexual dimorphism50,51, such as Ursus optimus from late Pleistocene McKittrick brea deposits of southern California52, which was determined by Graham53 to be a brown bear. Graham53 concluded that only one species, Ursus americanus, is valid throughout the Pleistocene with late Pleistocene fossil forms being larger than their living descendants, suggesting continuity of the black bear linage in North America, as was also pointed out earlier by Kurtén54.

Within Ursinae, P. abstrusus represents a stage of dental evolution that is intermediate in its specialization for ingesting plants, and significantly less than modern bears - polar bears being an exception, showing evolutionary reversal toward increased carnivory. The evolutionary history of ursines is generally characterized by a shift in dental specialization from carnivory to increased omnivory, with the posteriormost molars of more recent forms being more elongate, and wrinkled, allowing for more crushing surface (Table S2). Although, morphologically, P. abstrusus is less specialized than modern bears, the presence of dental caries suggests the diet of this 3.5 million-year-old transitional form already included a significant carbohydrate component.

Dental evidence from the beaver pond site P. abstrusus appears to be from two individuals, including an apparent young adult, and both show dental caries, suggesting their diets included high amounts of fermentable carbohydrates early in their lives. Simple sugars, such as glucose and fructose, are readily metabolized by many bacteria found in the oral biofilm into various acids. These acids demineralize enamel and dentin and may lead to dental caries55. Cariogenicity is highly correlated to the amount56,57 and frequency58,59 of sugar intakes. The type of sugar consumed and associated dental caries are also found to differ. Despite their high sugar content, raw fruits by themselves are not always implicated for cariogenicity, although high frequency (up to 17 times a day) may induce caries60. In humans, there is convincing evidence that free-sugar consumption of more than four times a day or more than 6–10% energy intake will increase incidents of dental caries57. Historically in humans, increase in prevalence of dental caries has generally been associated with dietary shifts, linked with a reduction of nomadic lifestyles61, the development of agriculture in Neolithic populations, and even more so with industrialization62.

In bears, carbohydrate intake may account for the appearance of dental caries (Tables S3 and S4), and may also be related to sedentary behavior, particularly for northern bears which hibernate. Northern black bears hibernate five to seven months, and survive better if they have high fat reserves63. In bears, the optimal diet for production of fat reserves appears to be one of high-energy carbohydrates (e.g., fruits) and low in protein. High-latitude berries (such as bearberry) often have a wide, circumpolar distribution and can be found in a variety of northern habitats including forest, woodland, wetland and tundra habitats64. Black bears and grizzly bears in boreal forest eat berry fruits in the autumn, but some fruits, such as cranberry and bearberry, frequently remain on the vine over winter and are important to bears coming out of hibernation in the early spring65,66,67. Bearberry (Arctostaphylos uva-ursi) fruits are relished and highly important to black bear in Pelly River Valley of Yukon Territory66. Berries are found in nearly 80% of bear scats collected during the fall period and consistently represent a large component of black bear diet in Alaska, with blueberries (Vaccinium uliginosum) being the most common65. However, fruit intake may be mitigated by factors such as fruit abundance and body size. For example, larger bodied bears appear to tend toward carnivory, as they are less efficient than smaller bears at exploiting small fruits68. These factors may underlie the high variation observed in caries prevalence seen among populations of modern black bears (Table S3).

Floral macrofossils from the Beaver Pond shows a diversity of berries would have been available to U. abstrusus, including Empetrum nigrum (crowberry), Vaccinium sp. (e.g., blueberry, lingonberry), Rubus idaeus (raspberry)69, and their abundance may have been enhanced following forest fires, which is evident at this site33. Therefore berries may have constituted a component of the Beaver Pond bear’s diet, particularly during the peak seasons, and their high sugar and acid contents could have resulted in the observed pronounced dental caries. The bear’s habitat may also have included honeybees, but this is speculative. The genus Apis includes honeybees that are today the basis of the honey industry. The genus appears to have originated in Europe dispersing into Asia, Africa as well as North America70. In North America the fossil record of this lineage is represented by a single species (Apis nearctica) from the Miocene (13 MA) of Nevada71. The most likely route that the Apis lineage took to arrive in North America would have been via the Bering Isthmus70, which was present throughout the Neogene until ~5–7 Ma;72. This land connection would have allowed for the existence of expansive high-latitude terrestrial continuity, spanning the northern reaches of the Eurasian and North American continents. Thus Apis in North America may have originally inhabited this Arctic biome before dispersing southward into the mid-latitudes of North America. In which case, the polar P. abstrusus may have had opportunity to supplement its diet with honey.

Aside from the Beaver Pond site fossil bear, all other basal ursines are known from the northern mid-latitudes (30–40° N) of Eurasia and North America (Fig. 1, and Supplementary Information). The lack of fossil bears in the intervening latitudes reflects the scarcity of northern Neogene vertebrate fossil sites in these regions. Thus, the discovery of the Beaver Pond site P. abstrusus at 78°N fills a substantial geographical gap. The finding also shows that early ursines were adapted to northern forests with snowy winters. Moreover, the Beaver Pond site bear is a small-bodied bear with dental caries and associated with a polar forest, rich in seasonal fruits (Fig. 10), suggesting that the northern populations of P. abstrusus likely consumed large amounts of sugar-rich foods in the fall, a pattern consistent with preparation for hibernation seen in modern bears. If so, the Beaver Pond site bear represents the earliest known, and most primitive bear, to have hibernated. Modern ursid hibernators include high latitude/altitude Asian black bears (U. thibetanus), northern American black bears (U. americanus), all brown bears (U. arctos), and female polar bears (U. maritimus)73. Also, the fossil species of cave bears (U. spelaeus and U. deningeri) are inferred to have hibernated74. All living bears also employ a reproductive strategy of embryonic diapause (delayed implantation) with implicit adaptive value of reducing the cost of reproduction by truncating embryonic development and of optimizing birth season at the most appropriate time75. Furthermore, these reproductive cycles may regulate metabolism by facilitating earlier entry of pregnant females into winter-dormancy state75,76. In the context of the phylogeny of modern bears the northern americanus-arctos-spelaeus-maritimus clade appears to have acquired hibernation from a single ancestor. The case for Asian black bear is ambiguous because its nearest relatives are not known to hibernate; namely the sloth bear (Melursus) of India, the sun bear (Helarctos) of Southeast Asia. The early diverging spectacled bear (Tremarctos) of South America is also a non-hibernator (Fig. 6). If the northern adapted Beaver Pond bear was a hibernator, then hibernation can be traced to the ancestor of all modern bears. This would imply that the Asian black bear retains the primitive condition, and the Eurasian ancestor of the spectacled bear, which would have passed through cold Beringian habitat when it first immigrated to North America77, also employed hibernation as part of its repertoire for winter survival. In this evolutionary scenario modern non-hibernating bears, are interpreted to have secondarily lost this trait, in association with adaptation to warmer habitats.