Genetics, morphology and ecology reveal a cryptic pika lineage in the Sikkim Himalaya.

Asian pika species are morphologically ∼similar and have overlapping ranges. This leads to uncertainty and species misidentification in the field. Phylogenetic analyses of such misidentified samples leads to taxonomic ambiguity. The ecology of many pika species remains understudied, particularly in the Himalaya, where sympatric species could be separated by elevation and/or substrate. We sampled, measured, and acquired genetic data from pikas in the Sikkim Himalaya. Our analyses revealed a cryptic lineage, Ochotona sikimaria, previously reported as a subspecies of O. thibetana. The results support the elevation of this lineage to the species level, as it is genetically divergent from O. thibetana, as well as sister species, O. cansus (endemic to central China) and O. curzoniae (endemic to the Tibetan plateau). The Sikkim lineage diverged from its sister species' about 1.7-0.8myrago, coincident with uplift events in the Himalaya. Our results add to the recent spate of cryptic diversity identified from the eastern Himalaya and highlight the need for further study within the Ochotonidae.

Genome report: chromosome-level draft assemblies of the snow leopard, African leopard, and tiger (Panthera uncia, Panthera pardus pardus, and Panthera tigris).

The big cats (genus Panthera) represent some of the most popular and charismatic species on the planet. Although some reference genomes are available for this clade, few are at the chromosome level, inhibiting high-resolution genomic studies. We assembled genomes from 3 members of the genus, the tiger (Panthera tigris), the snow leopard (Panthera uncia), and the African leopard (Panthera pardus pardus), at chromosome or near-chromosome level. We used a combination of short- and long-read technologies, as well as proximity ligation data from Hi-C technology, to achieve high continuity and contiguity for each individual. We hope that these genomes will aid in further evolutionary and conservation research of this iconic group of mammals.

Muskrats as a bellwether of a drying delta.

Wetlands worldwide are under threat from anthropogenic impacts. In large protected North American areas such as Yellowstone and Wood Buffalo National Parks, aquatic habitats are disappearing and wetland-dependent fauna are in decline1-3. Here we investigate population dynamics of an indicator species in Canada's Peace-Athabasca Delta ("the delta"), a World Heritage Site. Based on population surveys, habitat mapping and genetic data from 288 muskrats, we use agent-based modeling and genetic analyses to explain population expansion and decline of the semi-aquatic muskrat (Ondatra zibethicus). Simulations quantify a large population (~500,000 individuals) following flood-induced habitat gains, with decreased size (~10,000 individuals) during drying. Genetic analyses show extremely low long-term effective population size (Ne: 60-127), supporting a legacy of population bottlenecks. Our simulations indicate that the muskrat population in the delta is a metapopulation with individuals migrating preferentially along riparian pathways. Related individuals found over 40 km apart imply dispersal distances far greater than their typical home range (130 m). Rapid metapopulation recovery is achieved via riparian corridor migration and passive flood-transport of individuals. Source-sink dynamics show wetland loss impacts on the muskrat metapopulation's spatial extent. Dramatic landscape change is underway, devastating local fauna, including this generalist species even in a protected ecosystem.

Experimental study of hypoxia-induced changes in gene expression in an Asian pika, Ochotona dauurica.

Acclimation to environmental changes driven by alterations in gene expression will serve as an important response for some species facing rapid Anthropogenic climate change. Pikas, genus Ochotona, are particularly vulnerable to climate change and current trends suggest that only the highest, coldest elevations within their ranges may remain suitable habitat for these species. In this study we aimed to assess the role of changes in gene expression in potentially facilitating elevational movements in pikas by measuring gene expression in the only known captive pika population, Ochotona dauurica, in response to hypoxic conditions. Using a controlled experiment, we exposed four male pikas to oxygen concentrations characteristic of sea-level, 2,000 m, and 4,000 m for 5 days each. Using blood samples collected after each treatment, we used RNAseq to determine if candidate pathways were undergoing significant changes in gene expression at different levels of oxygen (~100%, ~77%, and ~61% of sea-level oxygen concentrations). Gene set enrichment analyses showed that gene sets associated with the oxidative phosphorylation pathway and electron transport chain were significantly enriched for up-regulated genes in the 4,000 m samples compared to samples from the same individuals at lower-elevation conditions. Up-regulation of these pathways is consistent with known mechanisms of oxygen compensation. Our results suggest that these pikas have the acclimation capacity to tolerate oxygen concentrations characteristic of any elevation within their species range and that gene expression can be changed in a matter of days to accommodate drastically different oxygen concentrations. Thus, rapid and radical elevational movements that may be required of some pika species to avoid warmer temperatures in the Anthropocene will likely not be limited by hypoxic stress.

Evolution for extreme living: variation in mitochondrial cytochrome c oxidase genes correlated with elevation in pikas (genus Ochotona).

The genus Ochotona (pikas) is a clade of cold-tolerant lagomorphs that includes many high-elevation species. Pikas offer a unique opportunity to study adaptations and potential limitations of an ecologically important mammal to high-elevation hypoxia. We analyzed the evolution of 3 mitochondrial genes encoding the catalytic core of cytochrome c oxidase (COX) in 10 pika species occupying elevations from sea level to 5000 m. COX is an enzyme highly reliant on oxygen and essential for cell function. One amino acid property, the equilibrium constant (ionization of COOH), was found to be under selection in the overall protein complex. We observed a strong relationship between the net value change in this property and the elevation each species occupies, with higher-elevation species having potentially more efficient proteins. We also found evidence of selection in low-elevation species for potentially less efficient COX, perhaps trading efficiency for heat production in the absence of hypoxia. Our results suggest that different pika species may have evolved elevation-specific COX proteins, specialization that may indicate limitations in their ability to shift their elevational ranges in response to future climate change.

Gene expression is implicated in the ability of pikas to occupy Himalayan elevational gradient.

Species are shifting their ranges due to climate change, many moving to cooler and higher locations. However, with elevation increase comes oxygen decline, potentially limiting a species' ability to track its environment depending on what mechanisms it has available to compensate for hypoxic stress. Pikas (Family Ochotonidae), cold-specialist small mammal species, are already undergoing elevational range shifts. We collected RNA samples from one population of Ochotona roylei in the western Himalaya at three sites- 3,600, 4,000, and 5,000 meters-and found no evidence of significant population genetic structure nor positive selection among sites. However, out of over 10,000 expressed transcripts, 26 were significantly upregulated at the 5,000 m site and were significantly enriched for pathways consistent with physiological compensation for limited oxygen. These results suggest that differences in gene expression may play a key role in enabling hypoxia tolerance on this local scale, indicating elevational flexibility that may facilitate successful range shifts in response to climate change.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems.

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.