Biological response to climate change in the Arctic Ocean: the view from the past
The Arctic Ocean is undergoing rapid climatic changes including higher ocean temperatures, reduced sea ice, glacier and Greenland Ice Sheet melting, greater marine productivity, and altered carbon cycling. Until recently, the relationship between climate and Arctic biological systems was poorly known, but this has changed substantially as advances in paleoclimatology, micropaleontology, vertebrate paleontology, and molecular genetics show that Arctic ecosystem history reflects global and regional climatic changes over all timescales and climate states (103–107 years). Arctic climatic extremes include 25 °C hyperthermal periods during the Paleocene-Eocene (56–46 million years ago, Ma), Quaternary glacial periods when thick ice shelves and sea ice cover rendered the Arctic Ocean nearly uninhabitable, seasonally sea-ice-free interglacials and abrupt climate reversals. Climate-driven biological impacts included large changes in species diversity, primary productivity, species’ geographic range shifts into and out of the Arctic, community restructuring, and possible hybridization, but evidence is not sufficient to determine whether or when major episodes of extinction occurred.
KeywordsArctic Ocean Paleoclimate Marine mammal phylogeny Arctic ecosystems Molecular clock
Today’s Arctic climate is warming faster than most other regions and losing summer sea-ice cover at historically unprecedented rates [27, 186]. This pattern of “Arctic amplification” is due to the changes in albedo , heat exchange between the atmosphere and ocean and other processes [146, 172] that are consistent with paleoclimate evidence for elevated polar temperatures during past warm periods [21, 126]. In addition to sea-ice decline, concerns exist about other climate-related processes that affect Arctic Ocean environments, such as submarine methane release , glacier melting , greater riverine discharge , marine ecosystem shifts , changes in biological productivity [9, 198], habitat loss and extinction , and carbon cycling [5, 180].
Instrumental and observational records are too short to fully evaluate the long-term effects of climate change on Arctic ecosystems, but two disparate fields—paleoclimatology and molecular genetics—now provide a unique context for assessment of climate change in the Arctic. In contrast to model simulations of future climatic and ecosystem change, paleoclimatology and genetics look back in time, using geochronology, physical, geochemical and paleoecological proxy methods, and DNA-based molecular clock analyses. Here we assess marine ecosystem response to past climate changes using an integrated approach based on Arctic sediment records of past intervals of warmth, orbital-scale glacial-interglacial cycles, and abrupt climate transitions coupled with DNA-based phylogenetic reconstructions and fossil records of polar vertebrate lineages. Although all parts of Arctic marine ecosystems cannot be studied, our study involves a wide variety of taxonomic groups and several key biological metrics of Arctic ecosystems including biodiversity, primary productivity, biogeography (range expansion and contraction) and hybridization. We address the fundamental question: does climate change cause large-scale loss of biodiversity through species’ extinctions (α diversity) or rearrangement of species abundances within local communities, geographic range shifts (β diversity) [52, 65], or ecosystem restructuring [28, 76].
Advances in Arctic paleoclimatology
Rapid advances have also come from the development of sediment proxy methods used to reconstruct environmental conditions and biological, chemical and physical processes influenced by climate (Supplementary Table 2). Examples used in the following discussion of Arctic climate and ecosystem evolution include micropaleontological records of benthic and pelagic communities, proxies of sea-ice cover, sediment transport, marine biological productivity, ocean temperature, salinity, dissolved oxygen and circulation, and ice sheet and ice shelf activity.
Cenozoic climate in the Arctic
ACEX researchers also investigated key climatic and ecosystem events including the Paleocene-Eocene Thermal Maximum (PETM), an ~170,000-year long warm period about 56 Ma when sea-surface temperatures in the Arctic (SST) reached 22 °C . In addition, ACEX recovered sediment from two younger hyperthermal periods—the Eocene Thermal Maximum 2 (ETM2) at 53.5 Ma  and the Azolla horizon ~48.5 Ma . During ETM2 TEX86-derived SST estimates indicate Arctic temperatures reached 25 °C, dinoflagellate cysts document freshwater influx and eutrophication, and palm pollen suggests winter temperatures on adjacent continents exceeded 8 °C. The dominance of the genus Azolla, a free-floating, freshwater fern, and associated microfossils, characterized an ~800,000-year long interval of episodic fresh surface water, a stratified ocean, endemism in silicoflagellates and ebridians , SSTs of 10–14 °C , and intermittent oxygen depletion  (Fig. 2d, f). During Paleocene-Eocene hyperthermal events, marine primary productivity in the central Arctic varied greatly with maximum values reaching 50–100 C g m−2 year−1 [106, 181]. These values are comparable to those from today’s highly productive Arctic marginal ice zones  and higher than estimates for the central Arctic Ocean over the last 18 Ma, including today (Fig. 2c).
During the interval 48–45 Ma, Arctic SSTs fell by as much as 5–10 °C depending on which proxy method is used [182, 200]. This cooling is coincident with the inception of a winter sea-ice regime seen in ice-rafted debris (IRD)  and sea-ice diatom records  (Fig. 2a). There is also lithological evidence for ephemeral perennial sea ice at times between 47 and 44 Ma  (Fig. 2b). Climate history of the late Eocene, Oligocene and early Miocene is poorly known because one age model calls for a major sedimentary unconformity from 44 to 18 Ma , and another for a condensed zone representing the interval from 36 to 12 Ma . This introduces uncertainty in identifying key Cenozoic cooling events, such as the Eocene/Oligocene transition ~34 Ma, and their biological impacts. There is, nonetheless, evidence for stepwise cooling during the last 18 Ma of the Cenozoic greenhouse-icehouse transition. For example, IRD, mineral, and radiogenic proxies record a shift from a mid-Miocene climatic optimum (~15 Ma) toward a colder climate since about 13 Ma [41, 66, 79, 179].
Early- to mid-Pliocene global climate (5–3 Ma) serves as an important benchmark for understanding modern climate because Pliocene atmospheric CO2 concentrations were near today’s level (400 ppmv, [139, 171]), but global mean annual temperature (MAT) was about 2.5–3 °C higher  and peak sea level ~22 m higher . Pliocene Arctic Ocean summer SSTs were appreciably warmer than modern and seasonally sea-ice-free conditions existed in some regions [108, 121]. Non-marine proxy records from continental sections also point to a warm Pliocene climate in the high latitudes of the northern hemisphere. At Lake El’gygytgyn (Lake “E”) in Siberia summer temperatures were 8 °C warmer than modern  and at Ellesmere Island, Canada, summer and MAT were 11.8 and 18.3 °C higher than today . In addition to periods of warmth, the Pliocene saw continued intensification of Northern Hemisphere glaciations and crossing of climate thresholds at 4 and 2.75 Ma as ice sheets reached Arctic coastlines . Such warm Pliocene conditions allowed a major trans-Arctic migration of mollusks [58, 195], ostracodes , and other groups ~4.5–3.8 Ma when the Bering Strait opened [71, 194]. The direction of this migration was mainly from Pacific-to-Atlantic and probably led to the evolution of some of today’s endemic Arctic species.
Quaternary glacial-interglacial cycles
Although not gaining as much attention as past warm periods, glacial periods in the Arctic and adjacent subarctic deserve special attention because they provide a stark environmental contrast with interglacials and concrete evidence for the resiliency of marine ecosystems in the face of large-scale climate oscillations. Records of the Last Glacial Maximum (LGM, MIS 2, ~24–19 ka) and the penultimate glacial MIS 6 (~150 ka) have excellent age control , broad spatial sediment core coverage, extensive submarine geophysical surveys, and onshore glacial geological mapping. At these times, the Arctic Ocean was reduced to ~50 % of its current area due to the combined effects of a 125 m fall in global sea level (increased ice-sheet volume), which exposed the vast Arctic continental shelves, and the expansion of ice sheets and ice shelves bordering the Arctic Ocean [43, 90, 91, 93, 94]. During glacial maxima, the cryosphere, including ice sheets, ice shelves, glaciers and sea ice, was substantially more extensive than what we see today (Fig. 1). The Laurentide, Innuitian, Eurasian, Barents Sea-Svalbard, and Icelandic Ice Sheets covered large parts of continental regions adjacent to the Arctic Ocean [56, 188], but perhaps as important, extensive ice shelves as thick as 1 km have been identified from submarine glacial landforms mapped using geophysical methods on the Chukchi margin and Yermak Plateau [97, 98, 131, 196], the Lomonosov Ridge and Chukchi Plateau , the Lomonosov Ridge , and the Morris Jesup Rise . During peak glacial conditions, sea ice was so thick during glacial maxima that little or no IRD could be transported to the central basin from continental margins leaving a sediment-starved central Arctic Ocean [150, 153]. Although the thickness of glacial-age sea ice is not known precisely, multiyear sea ice, called paleocrystic ice, thicker than today’s >40 m-thick ice shelves off Ellesmere Island, may have dominated the glacial Arctic Ocean before the main phase of deglaciation began at 15 ka .
At the same time that the LGM Arctic Ocean proper was dominated by thick sea ice and ice shelves, sea ice extended far southward into subarctic regions of the Nordic Seas, the northern North Atlantic and the Bering Sea. Using dinoflagellate cyst assemblages from more than 50 core sites, de Vernal et al.  reconstructed spatial patterns of LGM sea ice, SST and sea-surface salinity from mid-to-high latitudes across the Northern Hemisphere. Among their findings were the presence of mid-latitude sea ice, stronger seasonality, nearshore to offshore SST gradients, and reduced surface salinities. Planktic foraminiferal assemblages and stable isotope values , and epipelagic ostracodes  also indicate southward migration of sea ice into the Nordic Seas and North Atlantic during glacial periods MIS 2, 4, and 6. Similarly, in the southern Bering Sea, LGM sea ice is evident from diatom assemblages .
Biological response to glacial-interglacial cycles
Perhaps the most striking biological manifestations of orbital cycles in the Arctic Ocean and surrounding seas are patterns of microfossil density, species diversity, and assemblage composition, which, when combined with physical and geochemical proxies, provide compelling evidence for ecosystem response to climate change. In contrast to the pre-Miocene sediments in the Arctic, which lack calcareous microfossils [see above], commonly preserved microfossil groups in the Quaternary include benthic and planktic [153, 201]) foraminifera, calcareous nannofossils , and ostracodes . Along Arctic margins and in the Nordic Seas, diatoms , tintinnids (planktic ciliates, ), and dinoflagellates  also occur. In addition to faunal and floral remains, there are indirect proxies of oscillating biological activity, notably organic biomarkers of sea-ice diatoms and phytoplankton  and sediment manganese oxyhydroxide content related to terrestrial input, ice cover, and bioturbation [117, 118].
The density of calcareous microfossils in sediments from central Arctic ridges is directly linked to interglacial and glacial climate regimes and changes in sea-ice cover, surface productivity, sedimentation, and post-depositional processes [12, 119]. It is well established that foraminifera (benthic and planktic) and ostracodes are major components of the sand-sized fraction in interglacial sediments in contrast to near absence in glacial-age sediments [1, 80] (Fig. 3d). In addition to density, microfossil biodiversity is extremely variable in the eastern Arctic, where benthic foraminiferal diversity measured by the Fisher α and Shannon Wiener indices varied several-fold during the last glacial cycle , and in the western Arctic over the last few glacial-interglacial cycles . Mechanisms driving species diversity patterns within the Arctic include the strength of inflowing warm Atlantic water, ice cover and surface productivity.
Microfossil assemblage composition (e.g. β diversity), measured by the relative abundances of environmentally sensitive species and genera, is also a useful measure of ecosystem dynamics. One striking example of climate-driven migration is the Pacific diatom Neodenticula seminae, a species that sediment records show disappeared in the North Atlantic Ocean ~800 ka. It has recently been discovered that this species has migrated back into the North Atlantic and Nordic Seas during the last 2 decades almost certainly in response to higher ocean temperatures allowing inter-oceanic migration [125, 161]. In Arctic cores, biogeographic range shifts occur frequently due to changes in climate and ocean circulation over various timescales. One widely used benthic foraminifera, Epistominella exigua, is a phytodetritus-eating, opportunistic species that dominates modern oceanic frontal zones . Microfossil assemblages with dominant E. exigua indicate seasonally sea-ice-free and/or marginal ice zone conditions that characterized the early-mid Quaternary (~1.5 Ma–300 ka) prior to the development of perennial sea ice. This species is common during warm interglacials MIS 5 (125 ka, the Eemian Interglacial) and MIS 11 (400 ka) but absent during glacial periods .
As discussed above, ice shelves and thick sea ice covered the glacial Arctic Ocean, and, as a consequence, species were forced to migrate southward into extra-Arctic regions on a large scale. We can track the range expansion and contraction of sea-ice and marginal ice zone species because the ecology of several groups is well known from large, pan-Arctic surface sediment databases. In the case of dinoflagellates, fossil assemblages are used to estimate months of sea ice cover in subarctic seas [48, 49]. The epipelagic ostracode species Acetabulastoma arcticum, which today lives as a parasite on sea-ice dwelling species of the amphipod Gammarus, is also a useful sea-ice proxy in the Arctic and adjacent seas . As expected from its ecology, this species occurs only in glacial age sediments (MIS 2, 4 and 6) in cores from the Nordic Seas and North Atlantic.
There is also evidence in the Arctic for two well-known global climate transitions involving changes in the pattern of orbital glacial-interglacial cycles—the Mid-Pleistocene Transition between 1.2 Ma and 700 ka , and the mid-Brunhes Event ~450–400 ka . Importantly, both climate transitions involved changes in Arctic sea-ice ecosystems. For example, the mid-Pleistocene transition, a shift from 41 to 100-kyr glacial-interglacial cycles, is characterized by faunal turnover (including regional extinctions) in Arctic foraminifera and ostracodes and reduced marine productivity. These signal a change from a seasonally ice-free to mostly perennial sea-ice cover during interglacial periods . Globally, the mid-Brunhes Event coincides with the glacial termination between MIS 12 and MIS 11 (~450–400 ka) after which interglacial periods had smaller continental ice sheets, higher sea level, warmer temperatures, and higher atmospheric CO2 concentrations. MIS 11 was an exceptionally warm interglacial, notable because, whereas atmospheric CO2 concentrations (~280 ppmv) and orbital insolation were similar to those of the Holocene interglacial, global sea level was higher than today, perhaps due to the collapse of parts of the Antarctic Ice Sheet [84, 160, 165]. Arctic sediments from the Northwind, Mendeleev, and Lomonosov Ridges show that during MIS 11, there was no summer sea ice and SSTs reached 8–10 °C . Warm Arctic Ocean summers during MIS 11 are also evident in the Nordic seas and the subpolar North Atlantic [15, 100], in Lake “E” sediments  and from terrestrial pollen in cores off southern Greenland . Subsequent interglacial and interstadial periods (MIS 9, 7, 5 and 3) also experienced, at least at times, summer sea-ice-free conditions [133, 137].
In sum, the contrast between glacial and interglacial oceanic environmental conditions in the Arctic and subarctic reflects frequent biogeographic marine ecosystem shifts of several thousand kilometers supporting the view that climate change alters β diversity but does not cause the systematic loss of species.
Abrupt, suborbital climate transitions
Changes in the dominant species in benthic foraminifer assemblages occurred on the Yermak Plateau and Barents Sea slope during stadial-interstadial events. These changes suggest a more than twofold change in marine productivity (from 30 to >60 g C m−2 year−1) (Fig. 4a) . On the Laptev Sea margin, changes in dominant benthic foraminiferal species occur over a century or less at the onset and termination of H1 and the YD. Decreases in planktic foraminiferal stable isotope values during the YD up to 1 per mil are known from the Beaufort and Laptev Seas and the Mendeleev Ridge [6, 157, 177]. Faunal and isotopic proxies signify complex hydrological changes in the surface and subsurface Arctic Ocean caused by freshwater influx probably from multiple catastrophic glacial lake drainage episodes  and changes in the strength of inflowing Atlantic water. It is worth noting that other types of catastrophic events disrupted Arctic marine ecosystems, such as mega-iceberg discharges caused by Eurasian Ice Sheet surge and collapse, which scoured the seafloor in the Kara-Barents Seas [95, 131, 152] and central Arctic as far back as 500,000 ka . Space limits our discussion to the Arctic Ocean proper, but suborbital millennial-scale events also caused frequent marine ecosystem reorganizations in the Nordic Seas during the last glacial-interglacial cycle [14, 78].
Holocene climate oscillations
Although smaller in scale than glacial-interglacial cycles, climate variability during the Holocene interglacial period had significant impacts on polar biological systems. There is extensive evidence for an Early Holocene Thermal Maximum (EHTM) ~11–7 ka with regionally variable seasonally sea-ice-free conditions based on circum-Arctic lake and ice core records [101, 187], glacial geology , ocean temperatures , IRD , dinoflagellate assemblages , and sea-ice biomarkers . The EHTM was followed by Neoglacial cooling, which witnessed the development of what we know as the preindustrial, perennial sea-ice-covered Arctic, culminating in the Little Ice Age (LIA, 1400–1900 C.E.). Temporally and spatially variable sea-ice cover throughout the Holocene is among the most notable discoveries of the last decade [170, 193] because it reflects an Arctic Ocean highly sensitive to insolation and unforced climate variability.
Similarly, high-resolution late Holocene records covering the last 1000–2000 years are particularly important because they provide baseline variability to interpret recent trends in sea ice and temperature. Terrestrial [40, 102], marine SST , and sea ice  proxies show natural climate variability during the late Holocene, including the Medieval Climate Anomaly (600–1400 C.E.) and the LIA, as well as anomalous 20th century patterns.
Arctic Ocean marine mammals
Marine mammals are a major component of modern Arctic sea-ice ecosystems [74, 105] and their molecular genetics and paleontology provide insights about past climate changes in the Arctic. The use of molecular sequences of DNA and proteins to infer species’ phylogeny and divergence times (i.e., a molecular clock) is an important aspect of phylogenetics . These analyses, combined with vertebrate fossil evidence, can provide information about the temporal distribution of species, which can be used with paleoclimate data to better understand the Arctic climate-biological relationships, especially for vertebrate lineages (Supplementary Table 3). As we see below, molecular methods are increasingly applied to integrated paleoclimatic-ecosystem studies in the Arctic, so it is important to briefly consider the strengths and limitations.
The molecular approach involves comparison of the amino acid sequences of proteins or nucleic acid sequences (DNA or RNA) in different species [158, 191, 197, 209]. Molecular sequences will diverge by mutation from a common ancestral sequence at some rate, which is the time component of the “clock”. If the rate of sequence divergence is constant, then its extent will be a function of time and the phylogenetic relationships and time of divergence of the sequences can be estimated. If the time of divergence of the sequences is assumed to be equal to the time of divergence of the species, then an estimate of species’ divergence time is obtained. The assumptions of a constant rate of sequence divergence (depending on mutation rate and population genetic factors of selection, population size, migration) and that a sequence divergence reflects the species divergence are key factors affecting the accuracy of molecular clocks. Single gene sequences often do not reflect the species phylogeny so multiple genes or entire genome sequences are needed for robust analyses (e.g., ). DNA from extant animals is typically used to quantify sequence divergence, but ancient DNA (aDNA) from fossil material as old as 0.7 ma can also be used and provide valuable insights .
The accuracy of molecular clocks also depends on the accuracy of a fossil calibration date to identify the divergence time for at least one node of the phylogenetic tree of the taxa considered [7, 87, 124, 143]. Divergence time estimates can be controversial because of potential discrepancies of molecular clocks depending on the genes, calibration points, and models of molecular evolution considered [69, 158, 191, 197].
Case studies of vertebrate phylogeny with fossils and DNA sequences
In the case of Arctic climate change, the divergence time of polar bears (Ursus maritimus) and its sister species, brown bears (U. arctos), is especially relevant because there is concern about reduced summer sea ice habitat, especially for some geographic populations [3, 4, 54, 185]. Polar bears and brown bears are thought to have evolved from a common ancestor during the Pleistocene , and a polar bear fossil from the last interglacial (Eemian) period ~125 ka established this age as their minimum time of divergence [2, 88, 114].
Molecular clock estimates of the divergence time of polar bears and brown bears vary widely depending on the genes used. These include divergence times of 2–3 Ma using proteins , 110–130 ka with mitochondrial DNA (mtDNA, [8, 19, 46, 57, 109, 114, 189, 206, 207], 0.43–1.12 Ma with Y-chromosome DNA sequences  and 0.34–2.0 Ma with nuclear DNA sequences [57, 77, 206]. The most recent analyses of genome sequences estimated the polar bear-brown bear divergence at 340–480 ka , 1.2 Ma [23, 36], and 4–5 Ma .
Due to the inherent uncertainty of molecular clocks, some authors have refrained from applying them to these species [32, 67, 140, 199]. Cahill et al.  note that the molecular divergence times for bear species are relative, not absolute dates because of the uncertainty of the fossil record regarding bear species’ divergences. However, it is reasonable to infer the minimum age of U. maritimus is about 125 ka and more likely somewhat older, between 300 ka and 2 Ma. As discussed above, major climate transitions including the mid-Pleistocene Transition and mid-Brunhes Event occurred during this time frame.
Given the dynamic nature of climate-driven habitat changes outlined above, it is important to note that speciation may be accompanied by interbreeding between populations until there is permanent reproductive isolation. Extant populations of polar bears and brown bears have separate gene pools with minimal interbreeding [34, 35, 36, 77, 144], but future interbreeding (i.e., hybridization) is hypothesized if sea-ice declines and polar bears spend more time on land . Past interbreeding in these species is suggested by paraphyletic mtDNA phylogeny in which polar bears and brown bears from Admiralty, Baranof, and Chichagof islands (ABC) in southeast Alaska have haplotypes in a clade separate from other brown bears [32, 35]. In addition, polar bears and ABC brown bears share nuclear alleles [77, 116, 128], including <1 % of the autosomal genome and 6.5 % of the X-chromosome loci , but none of the Y-chromosome . The pattern of genes shared by polar bears and ABC brown bears—maternally inherited mtDNA > X chromosome > autosomes > Y-chromosomes—is consistent with introgressive hybridization of male brown bears mating with female polar bears. This is hypothesized to have occurred about 12 ka when brown bears replaced polar bears during post-glacial colonization of the ABC islands .
Pinniped phylogenies also shed light on the development of the Arctic marine ecosystem. The pinnipeds, which include seals (Phocidae), sea lions (Otariidae), and walruses (Odobenidae), live in Arctic and subarctic seas with seasonal or perennial ice. Seals of the subfamily Phocinae (tribe Phocini) include three closely related genera in the northern hemisphere whose divergence has been estimated with fossil and molecular data relevant to our discussion. This includes the ringed seal (Pusa hispida), a primary prey of polar bears. The genus Pusa has a circumpolar Arctic distribution that in addition to P. hispida in the central Arctic includes Caspian seals (P. caspica) in the Caspian Sea, and Baikal seals (P. sibirica) in (freshwater) Lake Baikal, Siberia. Phoca includes the harbor seal (P. vitulina) in the temperate and subarctic northern hemisphere, and the spotted seal (P. largha) in the subarctic North Pacific Ocean. The gray seal (Halichoerus grypus) occurs in the North Atlantic Ocean.
However, seal classification is not definitive because of close relationships among various groups. For example, harbor seals and spotted seals are sometimes considered conspecific, and some taxonomists suggest that Pusa and Halichoerus could be reclassified as Phoca [45, 86]. This is reflected in equivalent mtDNA divergence (mean sequence divergence 3.36 %) of ringed seals, harbor seals, and gray seals, which has been used as a standard to calibrate a molecular clock for other taxa .
The fossil record shows that ringed seals occurred in the Arctic region during Quaternary interglacial and interstadial periods, including the eastern Beaufort Sea (~42 ka), Greenland (130 ka), and the Chukchi Sea (130 ka, [81, 162]). Phoca (harbor seal or spotted seal) fossils also occur in the Chukchi Sea (115–130 ka, ). This indicates that the oldest fossils of ringed seals and spotted/harbor seals in the Arctic are the same age as the oldest polar bear fossil from the Eemian (MIS 5) interglacial. Even though molecular clock estimates suggest a much older origin of polar bears, the fossil data provide a minimum estimate of their origin and that of ringed and harbor/spotted seals. This confirms that the bears and seals co-existed in the Arctic during MIS 5 and persisted until the present.
Molecular genetic data indicate that the Phocini radiated during the last 1–2 Ma. Analysis of 8935 bp of 16 nuclear genes and mtDNA indicates that Pusa and Phoca split 1.58 Ma; and within Phoca harbor seals and spotted seals split 0.4–1.3 Ma, and within Pusa ringed, Caspian, and Baikal seals split 0.7–1.8 Ma . Analysis of 26,818 bp of 52 nuclear and mtDNA genes indicate Pusa and Phoca split 2.1 Ma; and within Phoca harbor seals and spotted seals split 1.1 Ma, and within Pusa ringed, Baikal, and Caspian seals split 2.0 Ma . The differences in these estimates reflect the different genes and models used, but they also indicate that seal species, including ringed seals, probably existed over much of the Pleistocene and Holocene along with polar bears.
The walrus (Odobenus rosmarus) also lives in Arctic and subarctic sea-ice-covered regions. Two subspecies are generally recognized, the Atlantic walrus (O. r. rosmarus) in the central Canadian Arctic east to the Kara Sea and the Pacific walrus (O. r. divergens) in the Bering and Chukchi Seas. A population in the Laptev Sea is related to the Pacific walrus [63, 113]. The fossil record shows that the Odobenidae evolved in the mid-Miocene ~16–21 Ma  and O. rosmarus is the only extant species, although up to 14 genera and 20 species lived in the past [47, 81]. Odobenus rosmarus is thought to have migrated from the Atlantic to the Pacific about 600 ka ; walrus fossils in the Bering and Chukchi Seas date to about 130 ka, on Vancouver Island, British Columbia 70 ka Ma, and as far south as California ~270 ka .
Molecular clock estimates suggest the walrus family diverged from the sea lion family (Otariidae) about 15.1–18 Ma [68, 86]. There are no extant taxa for molecular clock comparison of walruses with other Odobenidae, but an estimate of divergence of the Atlantic and Pacific walrus can be made considering their mtDNA divergence of 1–1.6 %  and a rate of pinniped mtDNA evolution of 1.2 %/Ma . These data suggest the Atlantic and Pacific subspecies split sometime between 83 and 133 ka, although there may have been gene flow between the oceans over this time considering the changes in sea-ice conditions described above.
Vertebrate range expansion and contraction during climate changes
Vertebrate paleontology often combined with paleoclimatic and/or molecular genetics provides key information about Arctic mammalian response to climate change. For example, Cooper et al.  recently analyzed genetic (13 events) and paleontological (18 events) megafaunal “transition events” for terrestrial taxa within the context of abrupt climate transitions including Dansgaard-Oeschger events identified in Greenland ice cores and Cariaco Basin sediments. They defined faunal transitions as geographically widespread or global extinctions, or invasions, of species or major clades. The bulk of the evidence indicated terrestrial vertebrates are affected by abrupt climate transitions.
In addition, there have been several studies in which polar bear evolution has been assessed in the context of orbital paleoclimate cycles over the past few million years [23, 46, 57, 77, 128]. If, as DNA and fossil evidence suggests, polar bears and their primary prey, ringed seals and other prey such as walruses, have existed for at least 125 ka and likely hundreds of thousands of years, then they experienced extreme climate conditions of glacial periods as well as partially or completely summer sea-ice-free interglacial periods (MIS 11, MIS 5 and the early Holocene). Microfossil proxy evidence for southward expansion of sea ice during glacial periods implies that vertebrate species that are dependent on sea ice habitat might have also migrated southward into the Nordic and Bering Sea-North Pacific regions.
Several lines of evidence support this idea of frequent geographically extensive range shifts, not only in terrestrial vertebrates , but sea ice based marine mammals as well. First, the close genetic relationships among bear species and among seal species discussed above, including evidence for hybridization, suggests dynamic population shifts. Moreover, large-scale range expansion during glacial periods is evident in the fossil record of vertebrates in extra-Arctic regions . For example, the post-glacial Champlain Sea (13–9 ka, ) of New York, Vermont, and Canada has well-studied Arctic vertebrate faunas that include whales, walruses, brown bears and seals [64, 83]. Likewise, in coastal regions around Alaska, fossil records [31, 85] support molecular genetic data  showing that during the LGM, polar bears and ringed seals ranged as far south as the Gulf of Alaska, considerably south of their current Arctic ranges. In the case of summer sea-ice-free interglacial periods, the presence of winter sea ice habitat, polar bears’ ability to fast during summer , seals ability to use land areas in the absence of sea ice, and the availability of new prey species shifting ranges into the Arctic may have allowed survival during warm periods. Walrus also have an extensive glacial and post-glacial fossil record  including specimens from the paleo-Hudson River Valley on the New York and New Jersey continental shelf dated at ~10.6–11.2 ka .
We are grateful to H. Bauch, J. Donnelly, O. Ingólfsson, M. Jakobsson, L. Polyak, A. Sluijs, R. Spielhagen R. Stein, and D. Willard for input into Arctic paleoclimates and comments on early drafts, and to E. Caverly, L. DeNinno and L. Gemery for graphics. Funded by USGS Climate and Land Use Research and Development Program and the University of Alaska, Fairbanks School of Natural Resources and Extension.
- 3.Amstrup SC, Marcot BG, Douglas DC (2007) Forecasting the range-wide status of polar bears at selected times in the 21st century, administrative report, 123 pp, U.S. Geol. Surv., Alaska Sci. Cent., Anchorage, Alaska. Available at http://www.usgs.gov/newsroom/special/polar_bears/
- 4.Amstrup SC, Marcot BG, Douglas DC (2008) A Bayesian network modeling approach to forecasting the 21st century worldwide status of polar bears. In: DeWeaver ET, Bitz CM, Tremblay LB (eds) Arctic sea ice decline: observations, projections, mechanisms, and implications. Geophysical Monograph Series vol 180. AGU, Washington, pp 213–268Google Scholar
- 5.Anderson LG, Tanhua T, Björk G, Hjalmarsson S, Jones EP, Jutterström S, Rudels B, Swift JH, Wåhlstöm I (2010) Arctic ocean shelf–basin interaction: an active continental shelf CO2 pump and its impact on the degree of calcium carbonate solubility. Deep Sea Res Part I Oceanogr Res Pap 57:869–879CrossRefGoogle Scholar
- 10.Backman J, Moran K, McInroy DB, Mayer LA (2006) Arctic coring expedition. In: Proceedings of the integrated ocean drilling program 302. doi: 10.2204/iodp.proc.302.2006
- 11.Backman J, Jakobsson M, Frank M, Sangiorgi F, Brinkhuis H, Stickley C, O’Regan M, Løvlie R, Pälike H, Spofforth D, Gattacecca J, Moran K, King J, Heil C (2008) Age model and core-seismic integration for the Cenozoic Arctic Coring Expedition sediments from the Lomonosov Ridge. Paleoceanography. doi: 10.1029/2007PA001476 Google Scholar
- 19.Bon C, Caudy N, de Dieuleveult M, Fosse P, Philippe M, Maksud F, Beraud-Colomb E, Bouzaid E, Kefi R, Laugier C et al (2008) Deciphering the complete mitochondrial genome and phylogeny of the extinct cave bear in the Paleolithic painted cave of Chauvet. Proc Natl Acad Sci USA 105:17447–17452CrossRefGoogle Scholar
- 21.Brigham-Grette J, Melles M, Minyuk P, Andreev A, Tarasov P, DeConto R, Koenig S, Nowaczyk N, Wennrich V, Rosén P, Haltia E, Cook T, Gebhardt C, Meyer-Jacob C, Snyder J, Herzschuh U (2013) Pliocene warmth, polar amplification and stepped Pleistocene cooling recorded in NE Arctic Russia. Science 340:1421–1427CrossRefGoogle Scholar
- 22.Brinkhuis H, Schouten S, Collinson ME, Sluijs A, Sinninghe Damsté JS, Dickens GR, Huber M, Cronin TM, Onodera J, Takahashi K, Bujak JP, Stein R, van der Burgh J, Eldrett JS, Harding IC, Lotter AF, Sangiorgi F, van Konijnenburg-van Cittert H, de Leeuw JW, Matthiessen J, Backman J, Moran K, The Expedition 302 Scientists (2006) Episodic fresh surface waters in the Eocene Arctic Ocean. Nature 441:606–609CrossRefGoogle Scholar
- 23.Cahill JA, Green RE, Fulton TL, Stiller M, Jay F, Ovsyanikov N, Salamzade R, St John J, Stirling I, Slatkin M, Shapiro B (2013) Genomic evidence for island population conversion resolves conflicting theories of polar bear evolution. PLoS Genet 9:e1003345. doi: 10.1371/journal.pgen.1003345 CrossRefGoogle Scholar
- 25.CCSP (2008) Abrupt Climate Change. A report by the US Climate Change Science Program and the Subcommittee on Global Change Research [Clark, P.U., A.J. Weaver (coordinating lead authors), E. Brook, E.R. Cook, T.L. Delworth, and K. Steffen (chapter lead authors)]. US Geological Survey, Reston, VA, p 459Google Scholar
- 37.Cronin TM (1991) Late Neogene marine ostracoda from Tjörnes, Iceland. J Paleontol 65(5):767–794Google Scholar
- 48.de Vernal A, Hillaire-Marcel C, Darby DA (2005a) Variability of sea ice cover in the Chukchi Sea (western Arctic Ocean) during the Holocene. Paleoceanography, 20, PA4018. doi: 10.1029/2005PA001157
- 49.de Vernal A, Eynaud F, Henry M, Hillaire-Marcel C, Londeix L, Mangin S, Matthiessen J, Marret F, Radi T, Rochon A, Solignac S, Turon J-L (2005) Reconstruction of sea-surface conditions at middle to high latitudes of the Northern Hemisphere during the Last Glacial Maximum (LGM) based on dinoflagellate cyst assemblages. Quat Sci Rev 24:897–924CrossRefGoogle Scholar
- 53.Dowsett HJ, Robinson MM, Haywood AM, Hill DJ, Dolan AM, Stoll DK, Chan W-L, Abe-Ouchi A, Chandler MA, Rosenbloom NA, Otto-Bliesner BL, Bragg FJ, Lunt DJ, Foley KM, Riesselman CR (2012) Assessing confidence in Pliocene sea surface temperatures to evaluate predictive models. Nat Clim Change 2:365–371CrossRefGoogle Scholar
- 58.Einarsson T, Hopkins DM, Doell RD (1967) The stratigraphy of Tjörnes, Northern Iceland, and the history of the Bering Land Bridge. In: Hopkins DM (ed) The bering land bridge. Stanford University Press, Stanford, pp 312–325Google Scholar
- 59.Expedition 302 Scientists (2006) Sites M0001–M0004. In: Backman J, Moran K, McInroy DB, Mayer LA (eds), and the Expedition 302 Scientists, Proceedings of IODP, 302: Edinburgh (Integrated Ocean Drilling Program Management International, Inc.). doi: 10.2204/iodp.proc.302.104.2006
- 61.Fagel N, Not C, Gueibe J, Mattielli N, Bazhenova E (2014) Late quaternary evolution of sediment provenances in the Central Arctic Ocean: mineral assemblage, trace element composition and Nd and Pb isotope fingerprints of detrital fraction from the Northern Mendeleev Ridge. Quat Sci Rev 92:140–154CrossRefGoogle Scholar
- 63.Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. US Department of the Interior, Fish and Wildlife Service. North American Fauna 74:1–279Google Scholar
- 70.Gardner AS, Moholdt G, Cogley JG, Wouters B, Arendt AA, Wahr J, Berthier E, Hock R, Pfeffer WT, Kaser G, Ligtenberg SRM, Bolch T, Sharp MJ, Hagen JO, van den Broeke MR, Paul F (2013) A reconciled estimate of glacier contributions to sea level rise: 2003–2009. Science 340:852–857CrossRefGoogle Scholar
- 76.Grebmeier JM, Bluhm BA, Cooper LW, Danielson S, Arrigo KR, Blanchard AL, Clarke JT, Day RH, Frey KE, Gradinger RR, Kedra M, Konar B, Kuletz KJ, Lee SH, Lovvorn JR, Norcross BL, Okkonen SR (2015) Ecosystem characteristics and processes facilitating persistent macrobenthic biomass hotspots and associated benthivory in the Pacific Arctic. Prog Oceanogr. doi: 10.1016/j.pocean.2015.05.006 Google Scholar
- 82.Harington CR, Beard G (1992) The Qualicum walrus: a Late Pleistocene walrus (Odobenus rosmarus) skeleton from Vancouver Island, British Columbia, Canada. Ann Zool Fennici 28:311–319Google Scholar
- 83.Harington CR, Cournoyer M, Chartier M, Fulton TL, Shapiro B (2014) Brown bear (Ursus arctos) (9880 ± 35 BP) from late-glacial Champlain Sea deposits at Saint-Nicolas, Quebec, Canada, and the dispersal history of brown bears. Can J Earth Sci 51:527–535. doi: 10.1139/cjes-2013-0220 CrossRefGoogle Scholar
- 85.Heaton TH, Grady F (2009) The fossil bears of Southeast Alaska. In: Proceedings of the 15th international congress of speleology 1(1):I-NGoogle Scholar
- 87.Hipsley CA, Müller J (2014) Beyond fossil calibrations: realities of molecular clock practices in evolutionary biology. Front Genet 5(138):1–11Google Scholar
- 89.Ingólfsson Ó, Norodahl H, Schomacker A (2010) Deglaciation and Holocene glacial history of Iceland. Dev Quat Sci 13:51–68Google Scholar
- 90.Jakobsson M (2000) Mapping the Arctic Ocean: bathymetry and pleistocene paleoceanography. Stockholm University, StockholmGoogle Scholar
- 95.Jakobsson M, Nilsson J, O’Regan M, Backman J, Löwemark L, Dowdeswell JA, Mayer L, Polyak L, Colleoni F, Anderson LG, Björk G, Darby D, Eriksson B, Hanslik D, Hell B, Marcussen C, Sellén E, Wallin Å (2010) An Arctic Ocean ice shelf during MIS 6 constrained by new geophysical and geological data. Quat Sci Rev 29:3505–3517. doi: 10.1016/j.quascirev.2010.03.015 CrossRefGoogle Scholar
- 96.Jakobsson M, Mayer L, Coakley B, Dowdeswell JA, Forbes S, Fridman B, Hodnesdal H, Noormets R, Pedersen R, Rebesco M, Schenke HW, Zarayskaya Y, Accettella D, Armstrong A, Anderson RM, Bienhoff P, Camerlenghi A, Church I, Edwards M, Gardner JV, Hall JK, Hell B, Hestvik O, Kristoffersen Y, Marcussen C, Mohammad R, Mosher D, Nghiem SV, Pedrosa MT, Travaglini PG, Weatherall P (2012) The international bathymetric chart of the Arctic Ocean (IBCAO) version 3.0. Geophys Res Lett 39:L12609. doi: 10.1029/2012gl052219 Google Scholar
- 98.Jakobsson M, Nilsson J, Anderson L, Backman J, Björk G, Cronin TM, Kirchner N, Koshurnikov A, Mayer L, Noormets R, O’Regan M, Stranne C, SWERUS-C3 Scientific Team (in press) An ice shelf covering the entire central Arctic Ocean during the penultimate glaciation. Nat CommunGoogle Scholar
- 99.Jouzel J, Masson-Delmotte V, Cattani O, Dreyfus G, Falourd S, Hoffmann G, Minster B, Nouet J, Barnola JM, Chappellaz J, Fischer H, Gallet JC, Johnsen S, Leuenberger M, Loulergue L, Luethi D, Oerter H, Parrenin F, Raisbeck G, Raynaud D, Schilt A, Schwander J, Selmo E, Souchez R, Spahni R, Stauffer B, Steffensen JP, Stenni B, Stocker TF, Tison JL, Werner M, Wolff EW (2007) Orbital and millennial Antarctic climate variability over the past 800,000 years. Science 317:793–796CrossRefGoogle Scholar
- 101.Kaufman DS, Ager TA, Anderson NJ, Anderson PM, Andrews JT, Bartlein PJ, Brubaker LB, Coats LL, Cwynar LC, Duvall ML, Dyke AS, Edwards ME, Eisner WR, Gajewski K, Geirsdóttir A, Hu FS, Jennings AE, Kaplan MR, Kerwin MW, Lozhkin AV, MacDonald GM, Miller GH, Mock CJ, Oswald WW, Otto-Bliesner BL, Porinchu DF, Rühland K, Smol JP, Steig EJ, Wolfe BB (2004) Holocene thermal maximum in the western Arctic (0–180 W). Quat Sci Rev 23:529–560CrossRefGoogle Scholar
- 102.Kaufman DS, Schneider DP, McKay NP, Ammann CM, Bradley RS, Briffa KR, Miller GH, Otto-Bliesner BL, Overpeck JT, Vinther BM, Arctic Lakes 2 k Project Members (2009) Recent warming reverses long-term Arctic cooling. Science 325: 1236–1239Google Scholar
- 107.Knies J, Mattingsdal R, Fabian K, Grøsfjeld K, Baranwal S, Husum K, De Schepper S, Vogt C, Andersen N, Matthiessen J, Andreassen K, Jokat W, Nam S-I, Gaina C (2014) Earth and Planetary Science Letters 387: 132–144Google Scholar
- 109.Krause J, Unger T, Noçon A, Malaspinas A-S, Kolokotronis S-O, Stiller M, Soibelzon L, Spriggs H, Dear PH, Briggs AW et al (2008) Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary. Biomed Central Evol Biol 8:220. doi: 10.1186/1471-2148-8-220 Google Scholar
- 110.Kristoffersen Y, Coakley B, Jokat W, Edwards M, Brekke H, Gjengedal J (2004) Seabed erosion on the Lomonosov Ridge, central Arctic Ocean: a tale of deep draft icebergs in the Eurasia Basin and the influence of Atlantic water inflow on iceberg motion. Paleoceanography. doi: 10.1029/2003PA000985 Google Scholar
- 111.Kurtén B (1964) The evolution of the polar bear, Ursus maritimus (Phipps). Acta Zool Fenn 108:1–30Google Scholar
- 119.Marzen R, DeNinno L, Cronin TM. Arctic Ocean calcareous microfossil and productivity cycles over orbital timescales (submitted)Google Scholar
- 123.Melles M, Brigham-Grette J, Minyuk PS, Nowaczyk NR, Wennrich V, DeConto RM, Anderson PM, Andreev AA, Coletti A, Cook TL, Haltia-Hovi EA, Kukkonen M, Lozhkin AV, Rosén P, Tarasov P, Vogel H, Wagner B (2012) 2.8 million years of Arctic climate change from Lake El’gygytgyn NE Russia. Science 337:315–320CrossRefGoogle Scholar
- 129.Moran K, Backman J, Brinkhuis H, Clemens SC, Cronin T, Dickens GR, Eynaud F, Gattacceca J, Jakobsson M, Jordan RW, Kaminski M, King J, Koc N, Krylov A, Martinez N, Matthiessen J, McInroy D, Moore TC, Onodera J, O’Regan M, Pälike H, Rea B, Rio D, Sakamoto T, Smith DC, Stein R, St John K, Suto I, Suzuki N, Takahashi K, Watanabe M, Yamamoto M, Farrel J, Frank M, Kubik P, Jokat W, Kristoffersen Y (2006) The Cenozoic palaeoenvironment of the Arctic Ocean. Nature 441:601–605CrossRefGoogle Scholar
- 133.Nørgaard-Pedersen N, Mikkelsen N, Lassen SJ, Kristoffersen Y, Sheldon E (2007) Reduced sea ice concentrations in the Arctic Ocean during the last interglacial period revealed by sediment cores off northern Greenland. Paleoceanography 22: PA1218. doi: 10.1029/2006PA001283
- 135.O’Regan M (2011) Late Cenozoic Paleoceanography of the Central Arctic Ocean. IOP Conference Series: Earth and Environmental Science 14. doi: 10.1088/1755-1315/14/1/012002
- 137.Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A, CAPE Last Interglacial Project members (2006) Simulating Arctic climate warmth and icefield retreat in the last interglaciations. Science 311: 1751–1753Google Scholar
- 142.Pamillo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583Google Scholar
- 156.Poore RZ, Ishman SE, Phillips RL, McNeil DH (1994) Quaternary stratigraphy and paleoceanography of the Canada basin, Western Arctic Ocean. US Geological Survey Bulletin 2080Google Scholar
- 166.Ruppel C (2011) Methane hydrates and contemporary climate change. Nat Knowl 2(12):12 (online only) Google Scholar
- 167.Sangiorgi F, van Soelen EE, Spofforth DJA, Pälike H, Stickley CE, St. John K, Koç N, Schouten S, Damsté S, Brinkhuis H (2008) Cyclicity in the middle Eocene central Arctic Ocean sediment record: orbital forcing and environmental response. Paleoceanography 23. doi: 10.1029/2007PA001487
- 168.Sarkissian C et al (2015) Ancient genomics. Philos Trans R Soc B 370:2013087Google Scholar
- 169.Scott DB, Schell T, St-Onge G, Rochon A, Blasco S (2009) Foraminiferal assemblage changes over the last 15,000 years on the Mackenzie/Beaufort sea slope and Amundsen Gulf, Canada: implications for past sea-ice conditions: Paleoceanography 24, PA2219. doi: 10.1029/2007PA001575
- 170.Seidenkrantz M-S et al (2014) Northern Hemisphere sea-ice cover during the Holocene—proxy data reconstruction and Modeling. AGU Abstract Dec. 2014 Annual MtgGoogle Scholar
- 174.Sluijs A, Schouten S, Pagani M, Woltering M, Brinkhuis H, Sinninghe Damsté JP, Dickens GR, Huber M, Reichart G-J, Stein R, Matthiessen J, Lourens LJ, Pedentchouk N, Backman J, Moran K, the Expedition 302 Scientists (2006) Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum. Nature 441: 610–613Google Scholar
- 180.Stein R, MacDonald RW (eds) (2004) The organic carbon cycle in the Arctic Ocean. Springer, BerlinGoogle Scholar
- 183.Stein R, Fahl K, Müller J (2012) Proxy reconstruction of Cenozoic Arctic Ocean Sea-Ice History—from IRD to IP25. Polarforschung, 82(1):37–71. hdl:10013/epic.40432.d001Google Scholar
- 184.Stickley CE, St. John K, Koç N, Jordan RW, Passchier S, Pearce RB, Kearns LE (2009) Evidence for middle Eocene Arctic sea ice from diatoms and ice-rafted debris. Nature 460:376–379Google Scholar
- 185.Stirling I (2011) Polar bears: the natural history of a threatened species. Fitzhenry & Whiteside, BrightonGoogle Scholar
- 187.Sundqvist HS, Kaufman DS, McKay NP, Balascio NL, Briner JP, Cwynar LC, Sejrup HP, Seppä H, Subetto DA, Andrews JT, Axford Y, Bakke J, Birks HJB, Brooks SJ, de Vernal A, Jennings AE, Ljungqvist FC, Rühland KM, Saenger C, Smol JP, Viau AE (2014) Arctic Holocene proxy climate database—new approaches to assessing geochronological accuracy and encoding climate variables. Clim Past 10:1–63CrossRefGoogle Scholar
- 188.Svendsen JI, Alexanderson H, Astakhov VI, Demidov I, Dowdeswell JA, Funder S, Gataullin V, Henriksen M, Hjort C, Houmark-Nielsen M, Hubberten HW, Ingólfsson Ó, Jakobsson M, Kjaer KH, Larsen El, Lokrantz H, Lunkka JP, Lyså A, Mangerud J, Matiouchkov A, Murray A, Möller P, Niessen F, Nikolskaya O, Polyak L, Saarnisto M, Siegert C, Siegert MJ, Spielhagen RF, Stein R (2004) Late quaternary ice sheet history of northern Eurasia. Quat Sci Rev 23:1229–1271Google Scholar
- 195.Vermeij GJ (1991) Anatomy of invasion: the trans-Arctic interchange. Paleobiology 17:281–307Google Scholar
- 199.Wayne RK, Van Valkenburgh B, O’Brien SJ (1991) Molecular distance and divergence time in carnivores and primates. Mol Biol Evol 8:297–319Google Scholar
- 209.Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, pp 97–166Google Scholar