Specimen collection is essential for modern science.

Natural history museums are vital repositories of specimens, samples and data that inform about the natural world; this Formal Comment revisits a Perspective that advocated for the adoption of compassionate collection practices, querying whether it will ever be possible to completely do away with whole animal specimen collection.

Two Decades of Wildlife Pathogen Surveillance: Case Study of Choclo orthohantavirus and Its Wild Reservoir Oligoryzomys costaricensis.

The Costa Rican pygmy rice rat (Oligoryzomys costaricensis) is the primary reservoir of Choclo orthohantavirus (CHOV), the causal agent of hantavirus disease, pulmonary syndrome, and fever in humans in Panama. Since the emergence of CHOV in early 2000, we have systematically sampled and archived rodents from >150 sites across Panama to establish a baseline understanding of the host and virus, producing a permanent archive of holistic specimens that we are now probing in greater detail. We summarize these collections and explore preliminary habitat/virus associations to guide future wildlife surveillance and public health efforts related to CHOV and other zoonotic pathogens. Host sequences of the mitochondrial cytochrome b gene form a single monophyletic clade in Panama, despite wide distribution across Panama. Seropositive samples were concentrated in the central region of western Panama, consistent with the ecology of this agricultural commensal and the higher incidence of CHOV in humans in that region. Hantavirus seroprevalence in the pygmy rice rat was >15% overall, with the highest prevalence in agricultural areas (21%) and the lowest prevalence in shrublands (11%). Host-pathogen distribution, transmission dynamics, genomic evolution, and habitat affinities can be derived from the preserved samples, which include frozen tissues, and now provide a foundation for expanded investigations of orthohantaviruses in Panama.

Disentangling environmental drivers of circadian metabolism in desert-adapted mice.

Metabolism is a complex phenotype shaped by natural environmental rhythms, as well as behavioral, morphological and physiological adaptations. Metabolism has been historically studied under constant environmental conditions, but new methods of continuous metabolic phenotyping now offer a window into organismal responses to dynamic environments, and enable identification of abiotic controls and the timing of physiological responses relative to environmental change. We used indirect calorimetry to characterize metabolic phenotypes of the desert-adapted cactus mouse (Peromyscus eremicus) in response to variable environmental conditions that mimic their native environment versus those recorded under constant warm and constant cool conditions, with a constant photoperiod and full access to resources. We found significant sexual dimorphism, with males being more prone to dehydration than females. Under circadian environmental variation, most metabolic shifts occurred prior to physical environmental change and the timing was disrupted under both constant treatments. The ratio of CO2 produced to O2 consumed (the respiratory quotient) reached greater than 1.0 only during the light phase under diurnally variable conditions, a pattern that strongly suggests that lipogenesis contributes to the production of energy and endogenous water. Our results are consistent with historical descriptions of circadian torpor in this species (torpid by day, active by night), but reject the hypothesis that torpor is initiated by food restriction or negative water balance.

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.

Limited Evidence for Parallel Evolution Among Desert-Adapted Peromyscus Deer Mice.

Warming climate and increasing desertification urge the identification of genes involved in heat and dehydration tolerance to better inform and target biodiversity conservation efforts. Comparisons among extant desert-adapted species can highlight parallel or convergent patterns of genome evolution through the identification of shared signatures of selection. We generate a chromosome-level genome assembly for the canyon mouse (Peromyscus crinitus) and test for a signature of parallel evolution by comparing signatures of selective sweeps across population-level genomic resequencing data from another congeneric desert specialist (Peromyscus eremicus) and a widely distributed habitat generalist (Peromyscus maniculatus), that may be locally adapted to arid conditions. We identify few shared candidate loci involved in desert adaptation and do not find support for a shared pattern of parallel evolution. Instead, we hypothesize divergent molecular mechanisms of desert adaptation among deer mice, potentially tied to species-specific historical demography, which may limit or enhance adaptation. We identify a number of candidate loci experiencing selective sweeps in the P. crinitus genome that are implicated in osmoregulation (Trypsin, Prostasin) and metabolic tuning (Kallikrein, eIF2-alpha kinase GCN2, APPL1/2), which may be important for accommodating hot and dry environmental conditions.

Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent.

Organisms that live in deserts offer the opportunity to investigate how species adapt to environmental conditions that are lethal to most plants and animals. In the hot deserts of North America, high temperatures and lack of water are conspicuous challenges for organisms living there. The cactus mouse (Peromyscus eremicus) displays several adaptations to these conditions, including low metabolic rate, heat tolerance, and the ability to maintain homeostasis under extreme dehydration. To investigate the genomic basis of desert adaptation in cactus mice, we built a chromosome-level genome assembly and resequenced 26 additional cactus mouse genomes from two locations in southern California (USA). Using these data, we integrated comparative, population, and functional genomic approaches. We identified 16 gene families exhibiting significant contractions or expansions in the cactus mouse compared to 17 other Myodontine rodent genomes, and found 232 sites across the genome associated with selective sweeps. Functional annotations of candidate gene families and selective sweeps revealed a pervasive signature of selection at genes involved in the synthesis and degradation of proteins, consistent with the evolution of cellular mechanisms to cope with protein denaturation caused by thermal and hyperosmotic stress. Other strong candidate genes included receptors for bitter taste, suggesting a dietary shift towards chemically defended desert plants and insects, and a growth factor involved in lipid metabolism, potentially involved in prevention of dehydration. Understanding how species adapted to deserts will provide an important foundation for predicting future evolutionary responses to increasing temperatures, droughts and desertification in the cactus mouse and other species.

A linked-read approach to museomics: Higher quality de novo genome assemblies from degraded tissues.

High-throughput sequencing technologies are a proposed solution for accessing the molecular data in historical specimens. However, degraded DNA combined with the computational demands of short-read assemblies has posed significant laboratory and bioinformatics challenges for de novo genome assembly. Linked-read or "synthetic long-read" sequencing technologies, such as 10× Genomics, may provide a cost-effective alternative solution to assemble higher quality de novo genomes from degraded tissue samples. Here, we compare assembly quality (e.g., genome contiguity and completeness, presence of orthogroups) between four new deer mouse (Peromyscus spp.) genomes assembled using linked-read technology and four published genomes assembled from a single shotgun library. At a similar price-point, these approaches produce vastly different assemblies, with linked-read assemblies having overall higher contiguity and completeness, measured by larger N50 values and greater number of genes assembled, respectively. As a proof-of-concept, we used annotated genes from the four Peromyscus linked-read assemblies and eight additional rodent taxa to generate a phylogeny, which reconstructed the expected relationships among species with 100% support. Although not without caveats, our results suggest that linked-read sequencing approaches are a viable option to build de novo genomes from degraded tissues, which may prove particularly valuable for taxa that are extinct, rare or difficult to collect.

Conservation Genomics in a Changing Arctic.

Although logistically challenging to study, the Arctic is a bellwether for global change and is becoming a model for questions pertinent to the persistence of biodiversity. Disruption of Arctic ecosystems is accelerating, with impacts ranging from mixing of biotic communities to individual behavioral responses. Understanding these changes is crucial for conservation and sustainable economic development. Genomic approaches are providing transformative insights into biotic responses to environmental change, but have seen limited application in the Arctic due to a series of limitations. To meet the promise of genome analyses, we urge rigorous development of biorepositories from high latitudes to provide essential libraries to improve the conservation, monitoring, and management of Arctic ecosystems through genomic approaches.

Whole-genome analysis of Mustela erminea finds that pulsed hybridization impacts evolution at high latitudes.

At high latitudes, climatic shifts hypothetically initiate recurrent episodes of divergence by isolating populations in glacial refugia-ice-free regions that enable terrestrial species persistence. Upon glacial recession, populations subsequently expand and often come into contact with other independently diverging populations, resulting in gene flow. To understand how recurrent periods of isolation and contact may have impacted evolution at high latitudes, we investigated introgression dynamics in the stoat (Mustela erminea), a Holarctic mammalian carnivore, using whole-genome sequences. We identify two spatio-temporally distinct episodes of introgression coincident with large-scale climatic shifts: contemporary introgression in a mainland contact zone and ancient contact ~200 km south of the contemporary zone, in the archipelagos along North America's North Pacific Coast. Repeated episodes of gene flow highlight the central role of cyclic climates in structuring high-latitude diversity, through refugial divergence and introgressive hybridization. When introgression is followed by allopatric isolation (e.g., insularization) it may ultimately expedite divergence.

Natural history collections-based research: progress, promise, and best practices.

Specimens and associated data in natural history collections (NHCs) foster substantial scientific progress. In this paper, we explore recent contributions of NHCs to the study of systematics and biogeography, genomics, morphology, stable isotope ecology, and parasites and pathogens of mammals. To begin to assess the magnitude and scope of these contributions, we analyzed publications in the Journal of Mammalogy over the last decade, as well as recent research supported by a single university mammal collection (Museum of Southwestern Biology, Division of Mammals). Using these datasets, we also identify weak links that may be hindering the development of crucial NHC infrastructure. Maintaining the vitality and growth of this foundation of mammalogy depends on broader engagement and support from across the scientific community and is both an ethical and scientific imperative given the rapidly changing environmental conditions on our planet.