Extreme High-Elevation Mammal Surveys Reveal Unexpectedly High Upper Range Limits of Andean Mice.

AbstractIn the world's highest mountain ranges, uncertainty about the upper elevational range limits of alpine animals represents a critical knowledge gap regarding the environmental limits of life and presents a problem for detecting range shifts in response to climate change. Here we report results of mountaineering mammal surveys in the Central Andes, which led to the discovery of multiple species of mice living at extreme elevations that far surpass previously assumed range limits for mammals. We livetrapped small mammals from ecologically diverse sites spanning >6,700 m of vertical relief, from the desert coast of northern Chile to the summits of the highest volcanoes in the Andes. We used molecular sequence data and whole-genome sequence data to confirm the identities of species that represent new elevational records and to test hypotheses regarding species limits. These discoveries contribute to a new appreciation of the environmental limits of vertebrate life.

Genomic insights into the mystery of mouse mummies on the summits of Atacama volcanoes.

Our understanding of the limits of animal life is continually revised by scientific exploration of extreme environments. Here we report the discovery of mummified cadavers of leaf-eared mice, Phyllotis vaccarum, from the summits of three different Andean volcanoes at elevations 6,029-6,233 m above sea level in the Puna de Atacama in Chile and Argentina. Such extreme elevations were previously assumed to be completely uninhabitable by mammals. In combination with a live-captured specimen of the same species from the nearby summit of Volcán Llullaillaco (6,739 m)1, the summit mummies represent the highest altitude physical records of mammals in the world. We also report a chromosome-level genome assembly for P. vaccarum that, in combination with a whole-genome re-sequencing analysis and radiocarbon dating analysis, provides insights into the provenance and antiquity of the summit mice. Radiocarbon data indicate that the most ancient of the mummies are, at most, a few centuries old. Genomic polymorphism data revealed a high degree of continuity between the summit mice and conspecifics from lower elevations in the surrounding Altiplano. Genomic data also revealed equal numbers of males and females among the summit mice and evidence of close kinship between some individuals from the same summits. These findings bolster evidence for resident populations of Phyllotis at elevations >6,000 m and challenge assumptions about the environmental limits of vertebrate life and the physiological tolerances of small mammals.

Extreme high-elevation mammal surveys reveal unexpectedly high upper range limits of Andean mice.

In the world's highest mountain ranges, uncertainty about the upper elevational range limits of alpine animals represents a critical knowledge gap regarding the environmental limits of life and presents a problem for detecting range shifts in response to climate change. Here we report results of mountaineering mammal surveys in the Central Andes, which led to the discovery of multiple species of mice living at extreme elevations that far surpass previously assumed range limits for mammals. We live-trapped small mammals from ecologically diverse sites spanning >6700 m of vertical relief, from the desert coast of northern Chile to the summits of the highest volcanoes in the Andes. We used molecular sequence data and whole-genome sequence data to confirm the identities of species that represent new elevational records and to test hypotheses regarding species limits. These discoveries contribute to a new appreciation of the environmental limits of vertebrate life.

Developing an appropriate evolutionary baseline model for the study of SARS-CoV-2 patient samples.

Over the past 3 years, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has spread through human populations in several waves, resulting in a global health crisis. In response, genomic surveillance efforts have proliferated in the hopes of tracking and anticipating the evolution of this virus, resulting in millions of patient isolates now being available in public databases. Yet, while there is a tremendous focus on identifying newly emerging adaptive viral variants, this quantification is far from trivial. Specifically, multiple co-occurring and interacting evolutionary processes are constantly in operation and must be jointly considered and modeled in order to perform accurate inference. We here outline critical individual components of such an evolutionary baseline model-mutation rates, recombination rates, the distribution of fitness effects, infection dynamics, and compartmentalization-and describe the current state of knowledge pertaining to the related parameters of each in SARS-CoV-2. We close with a series of recommendations for future clinical sampling, model construction, and statistical analysis.

Breathing can be dangerous: Opportunistic fungal pathogens and the diverse community of the small mammal lung mycobiome.

Human lung mycobiome studies typically sample bronchoalveolar lavage or sputum, potentially overlooking fungi embedded in tissues. Employing ultra-frozen lung tissues from biorepositories, we obtained fungal ribosomal RNA ITS2 sequences from 199 small mammals across 39 species. We documented diverse fungi, including common environmental fungi such as Penicillium and Aspergillus, associates of the human mycobiome such as Malassezia and Candida, and others specifically adapted for lungs (Coccidioides, Blastomyces, and Pneumocystis). Pneumocystis sequences were detected in 83% of the samples and generally exhibited phylogenetic congruence with hosts. Among sequences from diverse opportunistic pathogens in the Onygenales, species of Coccidioides occurred in 12% of samples and species of Blastomyces in 85% of samples. Coccidioides sequences occurred in 14 mammalian species. The presence of neither Coccidioides nor Aspergillus fumigatus correlated with substantial shifts in the overall mycobiome, although there was some indication that fungal communities might be influenced by high levels of A. fumigatus. Although members of the Onygenales were common in lung samples (92%), they are not common in environmental surveys. Our results indicate that Pneumocystis and certain Onygenales are common commensal members of the lung mycobiome. These results provide new insights into the biology of lung-inhabiting fungi and flag small mammals as potential reservoirs for emerging fungal pathogens.

Leveraging natural history biorepositories as a global, decentralized, pathogen surveillance network.

The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) pandemic reveals a major gap in global biosecurity infrastructure: a lack of publicly available biological samples representative across space, time, and taxonomic diversity. The shortfall, in this case for vertebrates, prevents accurate and rapid identification and monitoring of emerging pathogens and their reservoir host(s) and precludes extended investigation of ecological, evolutionary, and environmental associations that lead to human infection or spillover. Natural history museum biorepositories form the backbone of a critically needed, decentralized, global network for zoonotic pathogen surveillance, yet this infrastructure remains marginally developed, underutilized, underfunded, and disconnected from public health initiatives. Proactive detection and mitigation for emerging infectious diseases (EIDs) requires expanded biodiversity infrastructure and training (particularly in biodiverse and lower income countries) and new communication pipelines that connect biorepositories and biomedical communities. To this end, we highlight a novel adaptation of Project ECHO's virtual community of practice model: Museums and Emerging Pathogens in the Americas (MEPA). MEPA is a virtual network aimed at fostering communication, coordination, and collaborative problem-solving among pathogen researchers, public health officials, and biorepositories in the Americas. MEPA now acts as a model of effective international, interdisciplinary collaboration that can and should be replicated in other biodiversity hotspots. We encourage deposition of wildlife specimens and associated data with public biorepositories, regardless of original collection purpose, and urge biorepositories to embrace new specimen sources, types, and uses to maximize strategic growth and utility for EID research. Taxonomically, geographically, and temporally deep biorepository archives serve as the foundation of a proactive and increasingly predictive approach to zoonotic spillover, risk assessment, and threat mitigation.

Reassortment Between Divergent Strains of Camp Ripley Virus (Hantaviridae) in the Northern Short-Tailed Shrew (Blarina brevicauda).

Genomic reassortment of segmented RNA virus strains is an important evolutionary mechanism that can generate novel viruses with profound effects on human and animal health, such as the H1N1 influenza pandemic in 2009 arising from reassortment of two swine influenza viruses. Reassortment is not restricted to influenza virus and has been shown to occur in members of the order Bunyavirales. The majority of reassortment events occurs between closely related lineages purportedly due to molecular constraints during viral packaging. In the original report of Camp Ripley virus (RPLV), a newfound hantavirus in the northern short-tailed shrew (Blarina brevicauda), phylogenetic incongruence between different genomic segments suggested reassortment. We have expanded sampling to include RPLV sequences amplified from archival tissues of 36 northern short-tailed shrews collected in 12 states (Arkansas, Iowa, Kansas, Maryland, Massachusetts, Michigan, Minnesota, New Hampshire, Ohio, Pennsylvania, Virginia, Wisconsin), and one southern short-tailed shrew (Blarina carolinensis) from Florida, within the United States. Using Bayesian phylogenetic analysis and Graph-incompatibility-based Reassortment Finder, we identified multiple instances of reassortment that spanned the Hantaviridae phylogenetic tree, including three highly divergent, co-circulating lineages of the M segment that have reassorted with a conserved L segment in multiple populations of B. brevicauda. In addition to identifying the first known mobatvirus-like M-segment sequences from a soricid host and only the second from a eulipotyphlan mammal, our results suggest that reassortment may be common between divergent virus strains and provide strong justification for expanded spatial, temporal, and taxonomic analyses of segmented viruses.

Complex History of Codiversification and Host Switching of a Newfound Soricid-Borne Orthohantavirus in North America.

Orthohantaviruses are tightly linked to the ecology and evolutionary history of their mammalian hosts. We hypothesized that in regions with dramatic climate shifts throughout the Quaternary, orthohantavirus diversity and evolution are shaped by dynamic host responses to environmental change through processes such as host isolation, host switching, and reassortment. Jemez Springs virus (JMSV), an orthohantavirus harbored by the dusky shrew (Sorex monticola) and five close relatives distributed widely in western North America, was used to test this hypothesis. Total RNAs, extracted from liver or lung tissue from 164 shrews collected from western North America during 1983-2007, were analyzed for orthohantavirus RNA by reverse transcription polymerase chain reaction (RT-PCR). Phylogenies inferred from the L-, M-, and S-segment sequences of 30 JMSV strains were compared with host mitochondrial cytochrome b. Viral clades largely corresponded to host clades, which were primarily structured by geography and were consistent with hypothesized post-glacial expansion. Despite an overall congruence between host and viral gene phylogenies at deeper scales, phylogenetic signals were recovered that also suggested a complex pattern of host switching and at least one reassortment event in the evolutionary history of JMSV. A fundamental understanding of how orthohantaviruses respond to periods of host population expansion, contraction, and secondary host contact is the key to establishing a framework for both more comprehensive understanding of orthohantavirus evolutionary dynamics and broader insights into host-pathogen systems.