Genetic turnovers and northern survival during the last glacial maximum in European brown bears

The current phylogeographic pattern of European brown bears (Ursus arctos) has commonly been explained by postglacial recolonization out of geographically distinct refugia in southern Europe, a pattern well in accordance with the expansion/contraction model. Studies of ancient DNA from brown bear remains have questioned this pattern, but have failed to explain the glacial distribution of mitochondrial brown bear clades and their subsequent expansion across the European continent. We here present 136 new mitochondrial sequences generated from 346 remains from Europe, ranging in age between the Late Pleistocene and historical times. The genetic data show a high Late Pleistocene diversity across the continent and challenge the strict confinement of bears to traditional southern refugia during the last glacial maximum (LGM). The mitochondrial data further suggest a genetic turnover just before this time, as well as a steep demographic decline starting in the mid‐Holocene. Levels of stable nitrogen isotopes from the remains confirm a previously proposed shift toward increasing herbivory around the LGM in Europe. Overall, these results suggest that in addition to climate, anthropogenic impact and inter‐specific competition may have had more important effects on the brown bear's ecology, demography, and genetic structure than previously thought.     

Denning in brown bears

1. Hibernation represents an adaptation for coping with unfavorable environmental conditions. For brown bears Ursus arctos, hibernation is a critical period as pronounced temporal reductions in several physiological functions occur.
2. Here, we review the three main aspects of brown bear denning: (1) den chronology, (2) den characteristics, and (3) hibernation physiology in order to identify (a) proximate and ultimate factors of hibernation as well as (b) research gaps and conservation priorities.
3. Den chronology, which varies by sex and reproductive status, depends on environmental factors, such as snow, temperature, food availability, and den altitude. Significant variation in hibernation across latitudes occurs for both den entry and exit.
4. The choice of a den and its surroundings may affect individual fitness, for example, loss of offspring and excessive energy consumption. Den selection is the result of broad‐ and fine‐scale habitat selection, mainly linked to den insulation, remoteness, and availability of food in the surroundings of the den location.
5. Hibernation is a metabolic challenge for the brown bears, in which a series of physiological adaptations in tissues and organs enable survival under nutritional deprivation, maintain high levels of lipids, preserve muscle, and bone and prevent cardiovascular pathologies such as atherosclerosis.

It is important to understand: (a) proximate and ultimate factors in denning behavior and the difference between actual drivers of hibernation (i.e., factors to which bears directly respond) and their correlates; (b) how changes in climatic factors might affect the ability of bears to face global climate change and the human‐mediated changes in food availability; (c) hyperphagia (period in which brown bears accumulate fat reserves), predenning and denning periods, including for those populations in which bears do not hibernate every year; and (d) how to approach the study of bear denning merging insights from different perspectives, that is, physiology, ecology, and behavior.     

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.     

Evolutionary and ecological traps for brown bears Ursus arctos in human‐modified landscapes

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Room without a view—Den excavation in relation to body size in brown bears

Hibernation is an adaptive strategy to survive harsh winter conditions and food shortage. The use of well‐insulated winter dens helps animals minimize energy loss during hibernation. Brown bears (Ursus arctos) commonly use excavated dens for hibernation. Physical attributes of excavated dens are expected to impact the bear's heat retention and energy conservation. The objective of this study was to examine the determinants of cavity size of excavated dens and the impact of physical attributes of excavated dens on energy conservation in hibernating bears, hypothesizing that bears excavate dens in a way to minimize heat loss and optimize energy conservation during hibernation. We predicted that den cavity size would be determined by the bear's body size and that older bears would excavate better‐fitting cavities to minimize heat loss, due to their previous experience. We further predicted that physical attributes of excavated dens would affect the bears’ posthibernation body condition. Our results revealed that bears excavated a den cavity in relation to their body size, regardless of sex, and that older bears tended to excavate better‐fitting den cavities compared to young bears, as we expected. Older bears excavated better‐fitting den cavities, suggesting a potentially experience‐based shift with age in den‐excavation behavior and an optimum cavity size relative to a bear's body size. Our key finding is that insulation of excavated dens provided by wall/rood thickness and bedding materials had a significant positive effect on bears’ posthibernation body condition. We believe that our study provides new insight into how not only the quality of denning habitat, but also the quality of dens may affect hibernating animals, by presenting a potential adaptive aspect of den preparation (age effect on efficiency in den excavation) and effect of den attributes on the posthibernation body condition of brown bears.     

A sensitive and specific multiplex PCR approach for sex identification of ursine and tremarctine bears suitable for non‐invasive samples

We report a new approach for molecular sex identification of extant Ursinae and Tremarctinae bears. Two Y‐specific fragments (SMCY and 318.2) and one X‐specific fragment (ZFX) are amplified in a multiplex PCR, yielding a double test for male‐specific amplification and an internal positive control. The primers were designed and tested to be bear‐specific, thereby minimizing the risk of cross‐amplification in other species including humans. The high sensitivity and small amplicon sizes (100, 124, 160 base pairs) facilitate analysis of non‐invasively obtained DNA material. DNA from tissue and blood as well as from 30 non‐invasively collected hair and faeces yielded clear and easily interpretable results. The fragments were detected both by standard gel electrophoresis and automated capillary electrophoresis.     

Consequences of a demographic bottleneck on genetic structure and variation in the Scandinavian brown bear

The Scandinavian brown bear went through a major decline in population size approximately 100 years ago, due to intense hunting. After being protected, the population subsequently recovered and today numbers in the thousands. The genetic diversity in the contemporary population has been investigated in considerable detail, and it has been shown that the population consists of several subpopulations that display relatively high levels of genetic variation. However, previous studies have been unable to resolve the degree to which the demographic bottleneck impacted the contemporary genetic structure and diversity. In this study, we used mitochondrial and microsatellite DNA markers from pre‐ and postbottleneck Scandinavian brown bear samples to investigate the effect of the bottleneck. Simulation and multivariate analysis suggested the same genetic structure for the historical and modern samples, which are clustered into three subpopulations in southern, central and northern Scandinavia. However, the southern subpopulation appears to have gone through a marked change in allele frequencies. When comparing the mitochondrial DNA diversity in the whole population, we found a major decline in haplotype numbers across the bottleneck. However, the loss of autosomal genetic diversity was less pronounced, although a significant decline in allelic richness was observed in the southern subpopulation. Approximate Bayesian computations provided clear support for a decline in effective population size during the bottleneck, in both the southern and northern subpopulations. These results have implications for the future management of the Scandinavian brown bear because they indicate a recent loss in genetic diversity and also that the current genetic structure may have been caused by historical ecological processes rather than recent anthropogenic persecution.     

Responses of an endangered brown bear population to climate change based on predictable food resource and shelter alterations

The survival of an increasing number of species is threatened by climate change: 20%–30% of plants and animals seem to be at risk of range shift or extinction if global warming reaches levels projected to occur by the end of this century. Plant range shifts may determine whether animal species that rely on plant availability for food and shelter will be affected by new patterns of plant occupancy and availability. Brown bears in temperate forested habitats mostly forage on plants and it may be expected that climate change will affect the viability of the endangered populations of southern Europe. Here, we assess the potential impact of climate change on seven plants that represent the main food resources and shelter for the endangered population of brown bears in the Cantabrian Mountains (Spain). Our simulations suggest that the geographic range of these plants might be altered under future climate warming, with most bear resources reducing their range. As a consequence, this brown bear population is expected to decline drastically in the next 50 years. Range shifts of brown bear are also expected to displace individuals from mountainous areas towards more humanized ones, where we can expect an increase in conflicts and bear mortality rates. Additional negative effects might include: (a) a tendency to a more carnivorous diet, which would increase conflicts with cattle farmers; (b) limited fat storage before hibernation due to the reduction of oak forests; (c) increased intraspecific competition with other acorn consumers, that is, wild ungulates and free‐ranging livestock; and (d) larger displacements between seasons to find main trophic resources. The magnitude of the changes projected by our models emphasizes that conservation practices focused only on bears may not be appropriate and thus we need more dynamic conservation planning aimed at reducing the impact of climate change in forested landscapes.     

Large‐scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011

We combine satellite and ground observations during 1950–2011 to study the long‐term links between multiple climate (air temperature and cryospheric dynamics) and vegetation (greenness and atmospheric CO₂ concentrations) indicators of the growing season of northern ecosystems (>45°N) and their connection with the carbon cycle. During the last three decades, the thermal potential growing season has lengthened by about 10.5 days (P < 0.01, 1982–2011), which is unprecedented in the context of the past 60 years. The overall lengthening has been stronger and more significant in Eurasia (12.6 days, P < 0.01) than North America (6.2 days, P > 0.05). The photosynthetic growing season has closely tracked the pace of warming and extension of the potential growing season in spring, but not in autumn when factors such as light and moisture limitation may constrain photosynthesis. The autumnal extension of the photosynthetic growing season since 1982 appears to be about half that of the thermal potential growing season, yielding a smaller lengthening of the photosynthetic growing season (6.7 days at the circumpolar scale, P < 0.01). Nevertheless, when integrated over the growing season, photosynthetic activity has closely followed the interannual variations and warming trend in cumulative growing season temperatures. This lengthening and intensification of the photosynthetic growing season, manifested principally over Eurasia rather than North America, is associated with a long‐term increase (22.2% since 1972, P < 0.01) in the amplitude of the CO₂ annual cycle at northern latitudes. The springtime extension of the photosynthetic and potential growing seasons has apparently stimulated earlier and stronger net CO₂ uptake by northern ecosystems, while the autumnal extension is associated with an earlier net release of CO₂ to the atmosphere. These contrasting responses may be critical in determining the impact of continued warming on northern terrestrial ecosystems and the carbon cycle.     

Range expansion during the Pleistocene drove morphological radiation of the fir genus (Abies,Pinaceae) in the Qinghai‐Tibet Plateau and Himalayas

Range expansion caused by climate oscillations in the past probably promoted morphological radiation in a few plant groups. In this study, we aim to test this hypothesis through phylogeographical analysis of the cold‐tolerant fir genus (Abies) in the Qinghai‐Tibet Plateau (QTP) and Himalayas, where it comprises 12 described species. We examined sequence variation in two maternally inherited mitochondrial (mt) DNA fragments (nad5‐4 and nad7‐1) and two paternally inherited plastid DNA fragments (trnS‐G and trnL‐F) for 733 individuals from 75 populations of the species in a monophyletic group. Only six mtDNA haplotypes were recovered, but five were shared between multiple species and one occurred at a high frequency, providing strong evidence of range expansion. Forty‐three plastid DNA haplotypes were detected, 19 of which were shared between species and three occurred at high frequency. Network, mismatch and Bayesian skyline plot analyses of all plastid DNA haplotypes from this clade clearly suggested range expansion. This expansion was dated as having occurred during the longest and most extensive glaciation in the Pleistocene. Our results therefore supported the range expansion hypothesis for this clade of Abies during the Pleistocene; expansion probably drove the morphological radiation of the clade in the QTP and Himalayas, although it remains unclear whether the different morphotypes should be acknowledged as independent, reproductively isolated species. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 444–453.     

Black Bear Reactions to Venomous and Non‐venomous Snakes in Eastern North America

Bears are often considered ecological equivalents of large primates, but the latter often respond with fear, avoidance, and alarm calls to snakes, both venomous and non‐venomous, there is sparse information on how bears respond to snakes. We videotaped or directly observed natural encounters between black bears (Ursus americanus) and snakes. Inside the range of venomous snakes in Arkansas and West Virginia, adolescent and adult black bears reacted fearfully in seven of seven encounters upon becoming aware of venomous and non‐venomous snakes; but in northern Michigan and Minnesota where venomous snakes have been absent for millennia, black bears showed little or no fear in four encounters with non‐venomous snakes of three species. The possible roles of experience and evolution in bear reactions to snakes and vice versa are discussed. In all areas studied, black bears had difficulty to recognize non‐moving snakes by smell or sight. Bears did not react until snakes moved in 11 of 12 encounters with non‐moving timber rattlesnakes (Crotalus horridus) and four species of harmless snakes. However, in additional tests in this study, bears were repulsed by garter snakes that had excreted pungent anal exudates, which may help explain the absence of snakes, both venomous and harmless, in bear diets reported to date.     

Migration and isolation during the turbulent Ponto‐Caspian Pleistocene create high diversity in the crustacean Paramysis lacustris

The Ponto‐Caspian brackish‐water fauna inhabits estuaries and rivers of the Black, Azov and Caspian seas and is fragmented by higher salinity waters and a major interbasin watershed. The fauna is known for the high levels of endemism, complex zoogeographic histories, and as a recent source of successful invasive species. It remains debated whether the Black and Azov Sea brackish‐water populations survived unfavourable Pleistocene conditions in multiple separate refugia or whether the two seas were (repeatedly) recolonized from the Caspian. Using microsatellite and mtDNA markers, we demonstrate deep among‐ and within‐basin subdivisions in a widespread Ponto‐Caspian mysid crustacean Paramysis lacustris. Five genetic clusters were identified, but their relationships did not reflect the geography of the region. The Azov cluster was the most distinct (4–5% COI divergence), despite its geographic position in the corridor between Black and Caspian seas, and may represent a new species. In the northern Black Sea area, the Dnieper cluster was closer to the Caspian cluster than to the neighbouring Danube–Dniester–Bug populations, suggesting separate colonizations of the Black Sea. Overall, the data implied a predominant gene flow from the east to the Black Sea and highlight the importance of Caspian Sea transgressions in facilitating dispersal. Yet, the presence of distinct lineages in the Black Sea points to the persistence of isolated refugial populations that have gained diagnostic differences under presumably high mutation rates and large population sizes. The unfavourable Pleistocene periods in the Black Sea therefore appear to have promoted diversification of the brackish‐water lineages, rather than extirpated them.     

Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages

We estimated the phylogenetic relationships of brown bear maternal haplotypes from countries of northeastern Europe (Estonia, Finland and European Russia), using sequences of mitochondrial DNA (mtDNA) control region of 231 bears. Twenty-five mtDNA haplotypes were identified. The brown bear population in northeastern Europe can be divided into three haplogroups: one with bears from all three countries, one with bears from Finland and Russia, and the third composed almost exclusively of bears from European Russia. Four haplotypes from Finland and European Russia matched exactly with haplotypes from Slovakia, suggesting the significance of the current territory of Slovakia in ancient demographic processes of brown bears. Based on the results of this study and those from the recent literature, we hypothesize that the West Carpathian Mountains have served either as one of the northernmost refuge areas or as an important movement corridor for brown bears of the Eastern lineage towards northern Europe during or after the last ice age. Bayesian analyses were performed to investigate the temporal framework of brown bear lineages in Europe. The molecular clock was calibrated using Beringian brown bear sequences derived from radiocarbon-dated ancient samples, and the estimated mutation rate was 29.8% (13.3%-47.6%) per million years. The whole European population and Western and Eastern lineages formed about 175,000, 70,000 and 25,000 years before present, respectively. Our approach to estimating the time frame of brown bear evolution demonstrates the importance of using an appropriate mutation rate, and this has implications for other studies of Pleistocene populations.     

Historical faunal exchange between the Pontocaspian Basin and North America

Ecrobia is a genus of small brackish‐water mud snails with an amphi‐Atlantic distribution. Interestingly, the species occurring in the northwestern Atlantic, Ecrobia truncata, is more closely related to the Pontocaspian taxa, Ecrobia grimmi and Ecrobia maritima, than to the species occurring in the northeastern Atlantic and Mediterranean Sea. At least three colonization scenarios may account for this peculiar biogeographical pattern: (1) a recent human‐mediated dispersal, (2) a historical transatlantic interchange, and (3) a historical transpolar interchange. To test these three scenarios, we used five operational criteria—time of species divergence, first appearance in the fossil record, dispersal limitation as well as environmental filtering and biotic interactions along the potential migration routes. Specifically, we inferred a time‐calibrated molecular phylogeny for Ecrobia and reconstructed a paleogeographical map of the Arctic Ocean at 2.5 million years ago (Mya). Based on the five operational criteria, scenarios 1 and 2 can likely be rejected. In contrast, all criteria support scenario 3 (historical transpolar interchange). It is therefore suggested that a bird‐mediated and/or ocean current‐mediated faunal interchange via the Arctic Ocean occurred during the Late Pliocene or Early Pleistocene. This dispersal was likely facilitated by reduced distances between the Eurasian and North American/Greenland landmasses, marine introgressions, and/or a stepping‐stone system of brackish‐water habitats in northern Siberia, as well as a lack of competition along the migration route. As for the direction of dispersal, the scientific data presented are not conclusive. However, there is clearly more support for the scenario of dispersal from the Pontocaspian Basin to North America than vice versa. This is the first study providing evidence for a natural faunal exchange between the Pontocaspian Basin and North America via the Arctic Ocean.     

Phylogeographic characteristics of hypervariable regions in the mitochondrial genome of a cosmopolitan,bloom‐forming raphidophyte,Heterosigma akashiwo

The global distribution of phytoplankton is defined by many events, including long‐term evolutionary processes and shorter time span processes (e.g., global climate change). Furthermore, human‐assisted, unintentional dispersion, including the transport of live fish and spat for aquaculture, and transfer of aquatic microorganisms contained in ship ballast water, may aid the spread of phytoplankton. To understand the phylogeographic history of a species, the development of useful molecular markers is crucial. We previously reported a hypervariable mitochondrial gene in the cosmopolitan bloom‐forming alga, Heterosigma akashiwo. In this study, we identified two additional hypervariable segments in the H. akashiwo mitochondrial genome, one a protein coding sequence, and the other an intergenic region, by comparing the whole mitogenomes of strains obtained from various geographic origins. Interestingly, the newly identified hypervariable protein coding sequence was a paralogue of the previously identified gene, and both sequences showed tendencies to correlate with latitude of geographic origin. However, the hypervariable intergenic sequence did not show a clear correlation with origin. Our results demonstrated that the protein coding sequences may serve as useful tools for understanding the phylogeographic history of H. akashiwo, and they may crucially function in adaptation of the species to the environment.     

Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene

The phylogeography of Atlantic brown trout ( Salmo trutta ) was analysed using mitochondrial DNA control region complete sequences of 774 individuals from 57 locations. Additionally, the available haplotype information from 100 published populations was incorporated in the analysis. Combined information from nested clade analysis, haplotype trees, mismatch distributions, and coalescent simulations was used to characterize population groups in the Atlantic basin. A major clade involved haplotypes assigned to the Atlantic (AT) lineage, but another major clade should be considered as a distinct endemic lineage restricted to the Iberian Peninsula. The phylogeography of the Atlantic populations showed the mixed distribution of several Atlantic clades in glaciated areas of Northern Europe, whereas diverged haplotypes dominated the coastal Iberian rivers. Populations inhabiting the Atlantic rivers of southern France apparently contributed to postglacial colonization of northern basins, but also comprised the source of southern expansions during the Pleistocene.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 904–917.     

Large‐scale impact of climate change vs. land‐use change on future biome shifts in Latin America

Climate change and land‐use change are two major drivers of biome shifts causing habitat and biodiversity loss. What is missing is a continental‐scale future projection of the estimated relative impacts of both drivers on biome shifts over the course of this century. Here, we provide such a projection for the biodiverse region of Latin America under four socio‐economic development scenarios. We find that across all scenarios 5–6% of the total area will undergo biome shifts that can be attributed to climate change until 2099. The relative impact of climate change on biome shifts may overtake land‐use change even under an optimistic climate scenario, if land‐use expansion is halted by the mid‐century. We suggest that constraining land‐use change and preserving the remaining natural vegetation early during this century creates opportunities to mitigate climate‐change impacts during the second half of this century. Our results may guide the evaluation of socio‐economic scenarios in terms of their potential for biome conservation under global change.     

Recent and rapid diversification of the small carpenter bees in eastern North America

Bees fulfil a critical ecological role as pollinators, significantly contributing to the reproductive success of myriad angiosperm species. Although increasingly appreciated for their agricultural contributions, relatively little is yet known about the natural history of the vast majority of the more than 20 000 wild bee species worldwide. The small carpenter bee genus Ceratina occurs globally, and is represented in North America by its most recently diverged subgenera, Ceratinula and Zadontomerus. Recent genetic analysis of eastern Ceratina (Zadontomerus) supports the existence of five closely related, yet genetically distinct species living in sympatry. This phylogeographical study employs molecular barcoding of the most comprehensive specimen collection yet assembled to confirm the identities of these recently diverged eastern North American Ceratina (Zadontomerus) species. Delineation of extant population structure, evolutionary history and known range of this emerging model native pollinator are greatly improved by this study. We consider ecological and behavioural factors potentially contributing to the maintenance of genetic identity among these sympatric species.