Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears.

Polar bears are uniquely adapted to life in the High Arctic and have undergone drastic physiological changes in response to Arctic climates and a hyper-lipid diet of primarily marine mammal prey. We analyzed 89 complete genomes of polar bear and brown bear using population genomic modeling and show that the species diverged only 479-343 thousand years BP. We find that genes on the polar bear lineage have been under stronger positive selection than in brown bears; nine of the top 16 genes under strong positive selection are associated with cardiomyopathy and vascular disease, implying important reorganization of the cardiovascular system. One of the genes showing the strongest evidence of selection, APOB, encodes the primary lipoprotein component of low-density lipoprotein (LDL); functional mutations in APOB may explain how polar bears are able to cope with life-long elevated LDL levels that are associated with high risk of heart disease in humans.

Footprint evidence of early hominin locomotor diversity at Laetoli, Tanzania.

Bipedal trackways discovered in 1978 at Laetoli site G, Tanzania and dated to 3.66 million years ago are widely accepted as the oldest unequivocal evidence of obligate bipedalism in the human lineage1-3. Another trackway discovered two years earlier at nearby site A was partially excavated and attributed to a hominin, but curious affinities with bears (ursids) marginalized its importance to the paleoanthropological community, and the location of these footprints fell into obscurity3-5. In 2019, we located, excavated and cleaned the site A trackway, producing a digital archive using 3D photogrammetry and laser scanning. Here we compare the footprints at this site with those of American black bears, chimpanzees and humans, and we show that they resemble those of hominins more than ursids. In fact, the narrow step width corroborates the original interpretation of a small, cross-stepping bipedal hominin. However, the inferred foot proportions, gait parameters and 3D morphologies of footprints at site A are readily distinguished from those at site G, indicating that a minimum of two hominin taxa with different feet and gaits coexisted at Laetoli.

Taking a color photo: A homozygous 25-bp deletion in Bace2 may cause brown-and-white coat color in giant pandas.

Brown-and-white giant pandas (hereafter brown pandas) are distinct coat color mutants found exclusively in the Qinling Mountains, Shaanxi, China. However, its genetic mechanism has remained unclear since their discovery in 1985. Here, we identified the genetic basis for this coat color variation using a combination of field ecological data, population genomic data, and a CRISPR-Cas9 knockout mouse model. We de novo assembled a long-read-based giant panda genome and resequenced the genomes of 35 giant pandas, including two brown pandas and two family trios associated with a brown panda. We identified a homozygous 25-bp deletion in the first exon of Bace2, a gene encoding amyloid precursor protein cleaving enzyme, as the most likely genetic basis for brown-and-white coat color. This deletion was further validated using PCR and Sanger sequencing of another 192 black giant pandas and CRISPR-Cas9 edited knockout mice. Our investigation revealed that this mutation reduced the number and size of melanosomes of the hairs in knockout mice and possibly in the brown panda, further leading to the hypopigmentation. These findings provide unique insights into the genetic basis of coat color variation in wild animals.

Bear essentials.

Strangely, American black bears come in many colours. New work by Puckett et al. shows that a missense alteration in the gene encoding tyrosinase-related protein 1 (TYRP1) likely interferes with melanin synthesis and is responsible for the cinnamon colour variant in the southwest USA. However, the adaptive significance of colour polymorphisms in this large carnivore remains opaque.

A worldwide perspective on large carnivore attacks on humans.

Large carnivores have long fascinated human societies and have profound influences on ecosystems. However, their conservation represents one of the greatest challenges of our time, particularly where attacks on humans occur. Where human recreational and/or livelihood activities overlap with large carnivore ranges, conflicts can become particularly serious. Two different scenarios are responsible for such overlap: In some regions of the world, increasing human populations lead to extended encroachment into large carnivore ranges, which are subject to increasing contraction, fragmentation, and degradation. In other regions, human and large carnivore populations are expanding, thus exacerbating conflicts, especially in those areas where these species were extirpated and are now returning. We thus face the problem of learning how to live with species that can pose serious threats to humans. We collected a total of 5,440 large carnivore (Felidae, Canidae, and Ursidae; 12 species) attacks worldwide between 1950 and 2019. The number of reported attacks increased over time, especially in lower-income countries. Most attacks (68%) resulted in human injuries, whereas 32% were fatal. Although attack scenarios varied greatly within and among species, as well as in different areas of the world, factors triggering large carnivore attacks on humans largely depend on the socioeconomic context, with people being at risk mainly during recreational activities in high-income countries and during livelihood activities in low-income countries. The specific combination of local socioeconomic and ecological factors is thus a risky mix triggering large carnivore attacks on humans, whose circumstances and frequencies cannot only be ascribed to the animal species. This also implies that effective measures to reduce large carnivore attacks must also consider the diverse local ecological and social contexts.

Top predator sea stars are the benthic equivalent to polar bears of the pelagic realm.

The marine pelagic compartment spans numerous trophic levels and consists of numerous reticulate connections between species from primary producers to iconic apex predators, while the benthic compartment is perceived to be simpler in structure and comprised of only low trophic level species. Here, we challenge this paradigm by illustrating that the benthic compartment is home to a subweb of similar structure and complexity to that of the pelagic realm, including the benthic equivalent to iconic polar bears: megafaunal-predatory sea stars.

Uncovering the enigmatic evolution of bears in greater depth: The hybrid origin of the Asiatic black bear.

Bears are fascinating mammals because of their complex pattern of speciation and rapid evolution of distinct phenotypes. Interspecific hybridization has been common and has shaped the complex evolutionary history of bears. In this study, based on the largest population-level genomic dataset to date involving all Ursinae species and recently developed methods for detecting hybrid speciation, we provide explicit evidence for the hybrid origin of Asiatic black bears, which arose through historical hybridization between the ancestor of polar bear/brown bear/American black bears and the ancestor of sun bear/sloth bears. This was inferred to have occurred soon after the divergence of the two parental lineages in Eurasia due to climate-driven population expansion and dispersal. In addition, we found that the intermediate body size of this hybrid species arose from its combination of relevant genes derived from two parental lineages of contrasting sizes. This and alternate fixation of numerous other loci that had diverged between parental lineages may have initiated the reproductive isolation of the Asiatic black bear from its two parents. Our study sheds further light on the evolutionary history of bears and documents the importance of hybridization in new species formation and phenotypic evolution in mammals.

Insights into bear evolution from a Pleistocene polar bear genome.

The polar bear (Ursus maritimus) has become a symbol of the threat to biodiversity from climate change. Understanding polar bear evolutionary history may provide insights into apex carnivore responses and prospects during periods of extreme environmental perturbations. In recent years, genomic studies have examined bear speciation and population history, including evidence for ancient admixture between polar bears and brown bears (Ursus arctos). Here, we extend our earlier studies of a 130,000- to 115,000-y-old polar bear from the Svalbard Archipelago using a 10× coverage genome sequence and 10 new genomes of polar and brown bears from contemporary zones of overlap in northern Alaska. We demonstrate a dramatic decline in effective population size for this ancient polar bear's lineage, followed by a modest increase just before its demise. A slightly higher genetic diversity in the ancient polar bear suggests a severe genetic erosion over a prolonged bottleneck in modern polar bears. Statistical fitting of data to alternative admixture graph scenarios favors at least one ancient introgression event from brown bears into the ancestor of polar bears, possibly dating back over 150,000 y. Gene flow was likely bidirectional, but allelic transfer from brown into polar bear is the strongest detected signal, which contrasts with other published work. These findings may have implications for our understanding of climate change impacts: Polar bears, a specialist Arctic lineage, may not only have undergone severe genetic bottlenecks but also been the recipient of generalist, boreal genetic variants from brown bears during critical phases of Northern Hemisphere glacial oscillations.

Assessing the risk of climate maladaptation for Canadian polar bears.

The Arctic is warming four times faster than the rest of the world, threatening the persistence of many Arctic species. It is uncertain if Arctic wildlife will have sufficient time to adapt to such rapidly warming environments. We used genetic forecasting to measure the risk of maladaptation to warming temperatures and sea ice loss in polar bears (Ursus maritimus) sampled across the Canadian Arctic. We found evidence for local adaptation to sea ice conditions and temperature. Forecasting of genome-environment mismatches for predicted climate scenarios suggested that polar bears in the Canadian high Arctic had the greatest risk of becoming maladapted to climate warming. While Canadian high Arctic bears may be the most likely to become maladapted, all polar bears face potentially negative outcomes to climate change. Given the importance of the sea ice habitat to polar bears, we expect that maladaptation to future warming is already widespread across Canada.

Highly Pathogenic Avian Influenza Virus A(H5N1) Clade 2.3.4.4b Infection in Free-Ranging Polar Bear, Alaska, USA.

We report a natural infection with a Eurasian highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus in a free-ranging juvenile polar bear (Ursus maritimus) found dead in North Slope Borough, Alaska, USA. Continued community and hunter-based participation in wildlife health surveillance is key to detecting emerging pathogens in the Arctic.

Selective autophagy bears bone.

The endoplasmic reticulum (ER) is a dynamic intracellular network responsible for folding and maturation of organellar and secreted proteins. Selective autophagy of ER (ER-phagy) is emerging as an essential process that maintains proteostasis in the ER and is regulated by growth conditions. In this issue, Cinque et al (2020) show that fibroblast growth factor 18 (FGF18) specifically activates ER-phagy through a TFEB/TFE-dependent transcriptional regulation of the ER-phagy receptor Fam134b, a process essential for bone ossification and skeletal development.

Coupled social and ecological change drove the historical extinction of the California grizzly bear (Ursus arctos californicus).

Large carnivores (order Carnivora) are among the world's most threatened mammals due to a confluence of ecological and social forces that have unfolded over centuries. Combining specimens from natural history collections with documents from archival records, we reconstructed the factors surrounding the extinction of the California grizzly bear (Ursus arctos californicus), a once-abundant brown bear subspecies last seen in 1924. Historical documents portrayed California grizzlies as massive hypercarnivores that endangered public safety. Yet, morphological measurements on skulls and teeth generate smaller body size estimates in alignment with extant North American grizzly populations (approx. 200 kg). Stable isotope analysis (δ13C, δ15N) of pelts and bones (n = 57) revealed that grizzlies derived less than 10% of their nutrition from terrestrial animal sources and were therefore largely herbivorous for millennia prior to the first European arrival in this region in 1542. Later colonial land uses, beginning in 1769 with the Mission era, led grizzlies to moderately increase animal protein consumption (up to 26% of diet), but grizzlies still consumed far less livestock than otherwise claimed by contemporary accounts. We show how human activities can provoke short-term behavioural shifts, such as heightened levels of carnivory, that in turn can lead to exaggerated predation narratives and incentivize persecution, triggering rapid loss of an otherwise widespread and ecologically flexible animal.

The origins and diversification of Holarctic brown bear populations inferred from genomes of past and present populations.

The brown bear (Ursus arctos) is one of the survivors of the Late Quaternary megafauna extinctions. However, despite being widely distributed across the Holarctic, brown bears have experienced extensive range reductions, and even extirpations in some geographical regions. Previous research efforts using genetic data have provided valuable insights into their evolutionary history. However, most studies have been limited to contemporary individuals or mitochondrial DNA, limiting insights into population processes that preceded the present. Here, we present genomic data from two Late Pleistocene brown bears from Honshu, Japan and eastern Siberia, and combine them with published contemporary and ancient genomes from across the Holarctic range of brown bears to investigate the evolutionary relationships among brown bear populations through time and space. By including genomic data from Late Pleistocene and Holocene individuals sampled outside the current distribution range, we uncover diversity not present in contemporary populations. Notably, although contemporary individuals display geographically structured populations most likely driven by isolation-by-distance, this pattern varies among the ancient samples across different regions. The inclusion of ancient brown bears in our analysis provides novel insights into the evolutionary history of brown bears and contributes to understanding the populations and diversity lost during the Late Quaternary.

Running, jumping, hunting, and scavenging: Functional analysis of vertebral mobility and backbone properties in carnivorans.

Carnivorans are well-known for their exceptional backbone mobility, which enables them to excel in fast running and long jumping, leading to them being among the most successful predators amongst terrestrial mammals. This study presents the first large-scale analysis of mobility throughout the presacral region of the vertebral column in carnivorans. The study covers representatives of 6 families, 24 genera and 34 species. We utilized a previously developed osteometry-based method to calculate available range of motion, quantifying all three directions of intervertebral mobility: sagittal bending (SB), lateral bending (LB), and axial rotation (AR). We observed a strong phylogenetic signal in the structural basis of the vertebral column (vertebral and joint formulae, length proportions of the backbone modules) and an insignificant phylogenetic signal in most characteristics of intervertebral mobility. This indicates that within the existing structure (stabilization of which occurred rather early in different phylogenetic lineages), intervertebral mobility in carnivorans is quite flexible. Our findings reveal that hyenas and canids, which use their jaws to seize prey, are characterized by a noticeably elongated cervical region and significantly higher SB and LB mobility of the cervical joints compared to other carnivorans. In representatives of other carnivoran families, the cervical region is very short, but the flexibility of the neck (both SB and LB) is significantly higher than that of short-necked odd-toed and even-toed ungulates. The lumbar region of the backbone in carnivorans is dorsomobile in the sagittal plane, being on average ~23° more mobile than in artiodactyls and ~38° more mobile than in perissodactyls. However, despite the general dorsomobility, only some representatives of Canidae, Felidae, and Viverridae are superior in lumbar flexibility to the most dorsomobile ungulates. The most dorsomobile artiodactyls are equal or even superior to carnivorans in their ability to engage in dorsal extension during galloping. In contrast, carnivorans are far superior to ungulates in their ability to engage ventral flexion. The cumulative SB in the lumbar region in carnivorans largely depends on the mode of running and hunting. Thus, adaptation to prolonged and enduring pursuit of prey in hyenas is accompanied by markedly reduced SB flexibility in the lumbar region. A more dorsostable run is also a characteristic of the Ursidae, and the peculiar maned wolf. Representatives of Felidae and Canidae have significantly more available SB mobility in the lumbar region. However, they fully engage it only occasionally at key moments of the hunt associated with the direct capture of the prey or when running in a straight line at maximum speed.

Gestational giant panda plasma metabolomics: amino acid metabolism characteristics may predict panda pregnancy outcomes.

In brief: The metabolic processes of the gestation period in pandas remain poorly understood. Our study comprehensively characterizes the metabolism of giant pandas during gestation and proposes arginine and histidine as potential novel biomarkers for detecting the pregnancy state of giant pandas. Abstract: There has been remarkable progress in the conservation and reproduction of giant pandas. However, the physiology of the gestation period in pandas remains poorly understood. The metabolic processes from estrus to pregnancy are dynamic and precisely regulated, playing a crucial role in pregnancy and related dysfunctions. In this study, we conducted a metabolomic analysis of 37 blood samples collected from pandas in estrus, acyclic, and potential pregnant states, employing rigorous screening to minimize the influence of diet. Our findings suggest that a reduced appetite can serve as an indicator for evaluating implantation time, representing a characteristic response to pregnancy and aiding in the prediction of delivery time in pregnant pandas. Metabolomic results indicate great metabolism variation from estrus to pregnancy, highlighting the association between amino acid metabolism and pregnancy outcomes. Compared to other pandas, individuals who successfully bred exhibit significantly elevated levels of arginine and histidine, even 2 months before experiencing a reduced appetite. Furthermore, the lipid profile undergoes distinct dynamic changes only in estrus samples. In summary, our study comprehensively characterizes the metabolism of giant pandas during gestation and proposes arginine and histidine as potential novel biomarkers for detecting the pregnancy state of giant pandas.

Outbreak of Human Trichinellosis - Arizona, Minnesota, and South Dakota, 2022.

Trichinellosis is a parasitic zoonotic disease transmitted through the consumption of meat from animals infected with Trichinella spp. nematodes. In North America, human trichinellosis is rare and is most commonly acquired through consumption of wild game meat. In July 2022, a hospitalized patient with suspected trichinellosis was reported to the Minnesota Department of Health. One week before symptom onset, the patient and eight other persons shared a meal that included bear meat that had been frozen for 45 days before being grilled and served rare with vegetables that had been cooked with the meat. Investigation identified six trichinellosis cases, including two in persons who consumed only the vegetables. Motile Trichinella larvae were found in remaining bear meat that had been frozen for >15 weeks. Molecular testing identified larvae from the bear meat as Trichinella nativa, a freeze-resistant species. Persons who consume meat from wild game animals should be aware that that adequate cooking is the only reliable way to kill Trichinella parasites and that infected meat can cross-contaminate other foods.

New threats in the recovery of large carnivores inhabiting human-modified landscapes: the case of the Cantabrian brown bear (Ursus arctos).

Understanding mortality causes is important for the conservation of endangered species, especially in small and isolated populations inhabiting anthropized landscapes where both natural and human-caused mortality may hinder the conservation of these species. We investigated the mortality causes of 53 free-ranging brown bears (Ursus arctos) found dead between 1998 and 2023 in the Cantabrian Mountains (northwestern Spain), a highly human-modified region where bears are currently recovering after being critically threatened in the last century. We detected natural traumatic injuries in 52.63% and infectious diseases in 39.47% of the 38 bears for which the mortality causes were registered, with 21.05% of these cases presenting signs of both infectious diseases and traumas. More specifically, almost 30% of the bears died during or after intraspecific fights, including sexually selected infanticide (10.53%). In addition, primary infectious diseases such as infectious canine hepatitis, distemper, clostridiosis and colibacillosis caused the death of 15.79% of the bears. The number of direct human-caused deaths (i.e., shooting, poisoning, snare) decreased over the study period. This study also reveals three new mortality causes triggered by pathogens, two of which-Clostridium novyi and verotoxigenic Escherichia coli-not previously described in ursids, and the other one, canine distemper virus, never reported in brown bears as cause of death. New management strategies for the conservation of Cantabrian bears, which are urgently needed due to the rapid expansion of the population, should consider the mortality causes described in this study and must promote further research to elucidate how the high prevalence of infectious diseases may threaten the current recovery of the population.

Predation risk drives long-term shifts in migratory behaviour and demography in a large herbivore population.

Migration is an adaptive life-history strategy across taxa that helps individuals maximise fitness by obtaining forage and avoiding predation risk. The mechanisms driving migratory changes are poorly understood, and links between migratory behaviour, space use, and demographic consequences are rare. Here, we use a nearly 20-year record of individual-based monitoring of a large herbivore, elk (Cervus canadensis) to test hypotheses for changing patterns of migration in and adjacent to a large protected area in Banff National Park (BNP), Canada. We test whether bottom-up (forage quality) or top-down (predation risk) factors explained trends in (i) the proportion of individuals using 5 different migratory tactics, (ii) differences in survival rates of migratory tactics during migration and whilst on summer ranges, (iii) cause-specific mortality by wolves and grizzly bears, and (iv) population abundance. We found dramatic shifts in migration consistent with behavioural plasticity in individual choice of annual migratory routes. Shifts were inconsistent with exposure to the bottom-up benefits of migration. Instead, exposure to landscape gradients in predation risk caused by exploitation outside the protected area drove migratory shifts. Carnivore exploitation outside the protected area led to higher survival rates for female elk remaining resident or migrating outside the protected area. Cause-specific mortality aligned with exposure to predation risk along migratory routes and summer ranges. Wolf predation risk was higher on migratory routes than summer ranges of montane-migrant tactics, but wolf predation risk traded-off with heightened risk from grizzly bears on summer ranges. A novel eastern migrant tactic emerged following a large forest fire that enhanced forage in an area with lower predation risk outside of the protected area. The changes in migratory behaviour translated to population abundance, where abundance of the montane-migratory tactics declined over time. The presence of diverse migratory life histories maintained a higher total population abundance than would have been the case with only one migratory tactic in the population. Our study demonstrates the complex ways in which migratory populations change over time through behavioural plasticity and associated demographic consequences because of individuals balancing predation risk and forage trade-offs.

Evaluating hybrid speciation and swamping in wild carnivores with a decision-tree approach.

Hybridization is an important evolutionary force with a principal role in the origin of new species, known as hybrid speciation. However, ongoing hybridization can create hybrid swamping, in which parental genomes are completely lost. This can become a biodiversity threat if it involves species that have adapted to certain environmental conditions and occur nowhere else. Because conservation scientists commonly have a negative attitude toward hybrids, it is important to improve understanding of the influence of interspecific gene flow on the persistence of species. We reviewed the literature on species hybridization to build a list of all known cases in the order Carnivora. To examine the relative impact, we also noted level of introgression, whether fertile offspring were produced, and whether there was mention of negative or positive evolutionary effects (hybrid speciation and swamping). To evaluate the conservation implications of hybrids, we developed a decision-making tree with which to determine which actions should be taken to manage hybrid species. We found 53 hybrids involving 68 unique taxa, which is roughly 23% of all carnivore species. They mainly involved monophyletic (83%) and sympatric species (75%). For 2 species, the outcome of the assessment was to eliminate or restrict the hybrids: Ethiopian wolf (Canis simensis) and Scottish wildcat (Felis silvestris silvestris). Both species hybridize with their domestic conspecifics. For all other cases, we suggest hybrids be protected in the same manner as native species. We found no evidence of genomic extinction in Carnivora. To the contrary, some species appear to be of hybrid origin, such as the Asiatic black bear (Ursus thibetanus) and African golden wolf (Canis lupaster). Other positive outcomes of hybridization are novel genetic diversity, adaptation to extreme environments, and increased reproductive fitness. These outcomes are particularly valuable for counterbalancing genetic drift and enabling adaptive introgression in a human-dominated world.

La especiación por hibridación es una fuerza evolutiva importante con un papel principal en el origen de una nueva especie. Sin embargo, la hibridación continua puede generar un estancamiento híbrido en el que se pierden por completo los genomas parentales. Esto puede convertirse en una amenaza para la biodiversidad si involucra a una especie que se ha adaptado a ciertas condiciones ambientales y sólo se encuentra en un lugar. Ya que los científicos de la conservación suelen tener una actitud negativa hacia los híbridos, es importante incrementar el entendimiento de la influencia que tiene el flujo interespecífico sobre la persistencia de las especies. Revisamos la literatura sobre la hibridación de especies para generar una lista de todos los casos conocidos en el orden Carnívora. También observamos el nivel de introgresión, si se produjo descendencia fértil y si hubo mención de los efectos evolutivos positivos o negativos (especiación híbrida y estancamiento) para analizar el impacto relativo. Desarrollamos un árbol de decisión con el cual determinar cuáles acciones deberían tomarse en el manejo de las especies híbridas para evaluar las implicaciones que tienen los híbridos para la conservación. Encontramos 53 híbridos de 68 taxones únicos, lo que representa aproximadamente el 23% de todos los carnívoros. Estos híbridos incluyen principalmente a especies monofiléticas (83%) y simpátricas (75%). Para dos especies, los resultados del análisis fueron la eliminación o restricción de los híbridos: el lobo etíope (Canis simensis) y el lince escocés (Felis silvestris silvestris). Ambas especies hibridan con sus coespecíficos domésticos. Para todos los demás casos sugerimos que se proteja a los híbridos de la misma manera que a las especies nativas. No encontramos evidencias de una extinción genómica en el orden Carnívora. Al contrario, algunas especies parecen tener un origen híbrido, como el oso negro asiático (Ursus thibetanus) y el lobo dorado africano (Canis lupaster). Otros resultados positivos de la hibridación son la diversidad genética novedosa, la adaptación a ambientes extremos y el incremento en la adaptabilidad reproductiva. Estos resultados son de valor particular para contrarrestar la deriva génica y permitir la introgresión adaptativa en un mundo dominado por humanos. Evaluación de la especiación y estancamiento en carnívoros silvestres con una estrategia de árbol de decisión.