Middle and Late Pleistocene Denisovan subsistence at Baishiya Karst Cave.

Genetic and fragmented palaeoanthropological data suggest that Denisovans were once widely distributed across eastern Eurasia1-3. Despite limited archaeological evidence, this indicates that Denisovans were capable of adapting to a highly diverse range of environments. Here we integrate zooarchaeological and proteomic analyses of the late Middle to Late Pleistocene faunal assemblage from Baishiya Karst Cave on the Tibetan Plateau, where a Denisovan mandible and Denisovan sedimentary mitochondrial DNA were found3,4. Using zooarchaeology by mass spectrometry, we identify a new hominin rib specimen that dates to approximately 48-32 thousand years ago (layer 3). Shotgun proteomic analysis taxonomically assigns this specimen to the Denisovan lineage, extending their presence at Baishiya Karst Cave well into the Late Pleistocene. Throughout the stratigraphic sequence, the faunal assemblage is dominated by Caprinae, together with megaherbivores, carnivores, small mammals and birds. The high proportion of anthropogenic modifications on the bone surfaces suggests that Denisovans were the primary agent of faunal accumulation. The chaîne opératoire of carcass processing indicates that animal taxa were exploited for their meat, marrow and hides, while bone was also used as raw material for the production of tools. Our results shed light on the behaviour of Denisovans and their adaptations to the diverse and fluctuating environments of the late Middle and Late Pleistocene of eastern Eurasia.

Using global remote camera data of a solitary species complex to evaluate the drivers of group formation.

The social system of animals involves a complex interplay between physiology, natural history, and the environment. Long relied upon discrete categorizations of "social" and "solitary" inhibit our capacity to understand species and their interactions with the world around them. Here, we use a globally distributed camera trapping dataset to test the drivers of aggregating into groups in a species complex (martens and relatives, family Mustelidae, Order Carnivora) assumed to be obligately solitary. We use a simple quantification, the probability of being detected in a group, that was applied across our globally derived camera trap dataset. Using a series of binomial generalized mixed-effects models applied to a dataset of 16,483 independent detections across 17 countries on four continents we test explicit hypotheses about potential drivers of group formation. We observe a wide range of probabilities of being detected in groups within the solitary model system, with the probability of aggregating in groups varying by more than an order of magnitude. We demonstrate that a species' context-dependent proclivity toward aggregating in groups is underpinned by a range of resource-related factors, primarily the distribution of resources, with increasing patchiness of resources facilitating group formation, as well as interactions between environmental conditions (resource constancy/winter severity) and physiology (energy storage capabilities). The wide variation in propensities to aggregate with conspecifics observed here highlights how continued failure to recognize complexities in the social behaviors of apparently solitary species limits our understanding not only of the individual species but also the causes and consequences of group formation.

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.

Clade-specific forebrain cytoarchitectures of the extinct Tasmanian tiger.

The thylacine, or Tasmanian tiger, is the largest of modern-day carnivorous marsupials and was hunted to extinction by European settlers in Australia. Its physical resemblance to eutherian wolves is a striking example of evolutionary convergence to similar ecological niches. However, whether the neuroanatomical organization of the thylacine brain resembles that of canids and how it compares with other mammals remain unknown due to the scarcity of available samples. Here, we gained access to a century-old hematoxylin-stained histological series of a thylacine brain, digitalized it at high resolution, and compared its forebrain cellular architecture with 34 extant species of monotremes, marsupials, and eutherians. Phylogenetically informed comparisons of cortical folding, regional volumes, and cell sizes and densities across cortical areas and layers provide evidence against brain convergences with canids, instead demonstrating features typical of marsupials, and more specifically Dasyuridae, along with traits that scale similarly with brain size across mammals. Enlarged olfactory, limbic, and neocortical areas suggest a small-prey predator and/or scavenging lifestyle, similar to extant quolls and Tasmanian devils. These findings are consistent with a nonuniformity of trait convergences, with brain traits clustering more with phylogeny and head/body traits with lifestyle. By making this resource publicly available as rapid web-accessible, hierarchically organized, multiresolution images for perpetuity, we anticipate that additional comparative insights might arise from detailed studies of the thylacine brain and encourage researchers and curators to share, annotate, and preserve understudied material of outstanding biological relevance.

The ecology of human-caused mortality for a protected large carnivore.

Mitigating human-caused mortality for large carnivores is a pressing global challenge for wildlife conservation. However, mortality is almost exclusively studied at local (within-population) scales creating a mismatch between our understanding of risk and the spatial extent most relevant to conservation and management of wide-ranging species. Here, we quantified mortality for 590 radio-collared mountain lions statewide across their distribution in California to identify drivers of human-caused mortality and investigate whether human-caused mortality is additive or compensatory. Human-caused mortality, primarily from conflict management and vehicles, exceeded natural mortality despite mountain lions being protected from hunting. Our data indicate that human-caused mortality is additive to natural mortality as population-level survival decreased as a function of increasing human-caused mortality and natural mortality did not decrease with increased human-caused mortality. Mortality risk increased for mountain lions closer to rural development and decreased in areas with higher proportions of citizens voting to support environmental initiatives. Thus, the presence of human infrastructure and variation in the mindset of humans sharing landscapes with mountain lions appear to be primary drivers of risk. We show that human-caused mortality can reduce population-level survival of large carnivores across large spatial scales, even when they are protected from hunting.

Conservation of chromatin conformation in carnivores.

High throughput chromatin conformation capture (Hi-C) of leukocyte DNA was used to investigate the evolutionary stability of chromatin conformation at the chromosomal level in 11 species from three carnivore families: Felidae, Canidae, and Ursidae. Chromosome-scale scaffolds (C-scaffolds) of each species were initially used for whole-genome alignment to a reference genome within each family. This approach established putative orthologous relationships between C-scaffolds among the different species. Hi-C contact maps for all C-scaffolds were then visually compared and found to be distinct for a given reference chromosome or C-scaffold within a species and indistinguishable for orthologous C-scaffolds having a 1:1 relationship within a family. The visual patterns within families were strongly supported by eigenvectors from the Hi-C contact maps. Analysis of Hi-C contact maps and eigenvectors across the three carnivore families revealed that most cross-family orthologous subchromosomal fragments have a conserved three-dimensional (3D) chromatin structure and thus have been under strong evolutionary constraint for ∼54 My of carnivore evolution. The most pronounced differences in chromatin conformation were observed for the X chromosome and the red fox genome, whose chromosomes have undergone extensive rearrangements relative to other canids. We also demonstrate that Hi-C contact map pattern analysis can be used to accurately identify orthologous relationships between C-scaffolds and chromosomes, a method we termed "3D comparative scaffotyping." This method provides a powerful means for estimating karyotypes in de novo sequenced species that have unknown karyotype and no physical mapping information.

A Neandertal dietary conundrum: Insights provided by tooth enamel Zn isotopes from Gabasa, Spain.

The characterization of Neandertals' diets has mostly relied on nitrogen isotope analyses of bone and tooth collagen. However, few nitrogen isotope data have been recovered from bones or teeth from Iberia due to poor collagen preservation at Paleolithic sites in the region. Zinc isotopes have been shown to be a reliable method for reconstructing trophic levels in the absence of organic matter preservation. Here, we present the results of zinc (Zn), strontium (Sr), carbon (C), and oxygen (O) isotope and trace element ratio analysis measured in dental enamel on a Pleistocene food web in Gabasa, Spain, to characterize the diet and ecology of a Middle Paleolithic Neandertal individual. Based on the extremely low δ66Zn value observed in the Neandertal's tooth enamel, our results support the interpretation of Neandertals as carnivores as already suggested by δ15N isotope values of specimens from other regions. Further work could help identify if such isotopic peculiarities (lowest δ66Zn and highest δ15N of the food web) are due to a metabolic and/or dietary specificity of the Neandertals.

The reorganization of predator-prey networks over 20 million years explains extinction patterns of mammalian carnivores.

Linking the species interactions occurring at the scale of local communities to their potential impact at evolutionary timescales is challenging. Here, we used the high-resolution fossil record of mammals from the Iberian Peninsula to reconstruct a timeseries of trophic networks spanning more than 20 million years and asked whether predator-prey interactions affected regional extinction patterns. We found that, despite small changes in species richness, trophic networks showed long-term trends, gradually losing interactions and becoming sparser towards the present. This restructuring of the ecological networks was driven by the loss of medium-sized herbivores, which reduced prey availability for predators. The decrease in prey availability was associated with predator longevity, such that predators with less available prey had greater extinction risk. These results not only reveal long-term trends in network structure but suggest that prey species richness in ecological communities may shape large scale patterns of extinction and persistence among predators.

Reliable biogeography requires fossils: insights from a new species-level phylogeny of extinct and living carnivores.

A central objective of historical biogeography is to understand where clades originated and how they moved across space and over time. However, given the dynamic history of ecosystem changes in response to climate change and geological events, the manifold long-distance dispersals over evolutionary timescales, and regional and global extinctions, it remains uncertain how reliable inferences based solely on extant taxa can be achieved. Using a novel species-level phylogeny of all known extant and extinct species of the mammalian order Carnivora and related extinct groups, we show that far more precise and accurate ancestral areas can be estimated by fully integrating extinct species into the analyses, rather than solely relying on extant species or identifying ancestral areas only based on the geography of the oldest fossils. Through a series of simulations, we further show that this conclusion is robust under realistic scenarios in which the unknown extinct taxa represent a biased subset of all extinct species. Our results highlight the importance of integrating fossil taxa into a phylogenetic framework to further improve our understanding of historical biogeography and reveal the dynamic dispersal and diversification history of carnivores.

The influence of the land-to-sea macroevolutionary transition on vertebral column disparification in Pinnipedia.

The repeated returns of vertebrates to the marine ecosystems since the Triassic serve as an evolutionary model to understand macroevolutionary change. Here we investigate the effects of the land-to-sea transition on disparity and constraint of the vertebral column in aquatic carnivorans (Carnivora; Pinnipedia) to assess how their functional diversity and evolutionary innovations influenced major radiations of crown pinnipeds. We use three-dimensional geometric morphometrics and multivariate analysis for high-dimensional data under a phylogenetic framework to quantify vertebral size and shape in living and extinct pinnipeds. Our analysis demonstrates an important shift in vertebral column evolution by 10-12 million years ago, from an unconstrained to a constrained evolutionary scenario, a point of time that coincides with the major radiation of crown pinnipeds. Moreover, we also demonstrate that the axial skeleton of phocids and otariids followed a different path of morphological evolution that was probably driven by their specialized locomotor strategies. Despite this, we found a significant effect of habitat preference (coastal versus pelagic) on vertebral morphology of crown taxa regardless of the family they belong. In summary, our analysis provides insights into how the land-to-sea transition influenced the complex evolutionary history of pinniped vertebral morphology.