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            Spiropoulou, Christina F (Ed.)ABSTRACT Bacterial pathogens remain poorly characterized in bats, especially in North America. We describe novel (and in some cases panmictic) hemoplasmas (10.1% positivity) and bartonellae (25.6% positivity) across three colonies of Mexican free-tailed bats (Tadarida brasiliensis), a partially migratory species that can seasonally travel hundreds of kilometers. Molecular analyses identified three novelCandidatushemoplasma species most similar to another novelCandidatusspecies in Neotropical molossid bats. We also detected novel hemoplasmas in sympatric cave myotis (Myotis velifer) and pallid bats (Antrozous pallidus), with sequences in the latter 96.5% related toCandidatusMycoplasma haematohominis. We identified nineBartonellagenogroups, including those in cave myotis with 96.1% similarity toCandidatusBartonella mayotimonensis. We also detectedBartonella rochalimaein migratory Mexican free-tailed bats, representing the first report of this human pathogen in the Chiroptera. Monthly sampling of migratory Mexican free-tailed bats during their North American occupancy period also revealed significant seasonality in infection for both bacterial pathogens, with prevalence increasing following spring migration, peaking in the maternity season, and declining into fall migration. The substantial diversity and seasonality of hemoplasmas and bartonellae observed here suggest that additional longitudinal, genomic, and immunological studies in bats are warranted to inform One Health approaches. IMPORTANCEBats have been intensively sampled for viruses but remain mostly understudied for bacterial pathogens. However, bacterial pathogens can have significant impacts on both human health and bat morbidity and even mortality. Hemoplasmas and bartonellae are facultative intracellular bacteria of special interest in bats, given their high prevalence and substantial genetic diversity. Surveys have also supported plausible zoonotic transmission of these bacteria from bats to humans, includingCandidatusMycoplasma haematohominis andCandidatusBartonella mayotimonensis. Greater characterization of these bacteria across global bat diversity (over 1,480 species) is therefore warranted to inform infection risks for both bats and humans, although little surveillance has thus far been conducted in North American bats. We here describe novel (and in some cases panmictic) hemoplasmas and bartonellae across three colonies of Mexican free-tailed bats and sympatric bat species. We find high genetic diversity and seasonality of these pathogens, including lineages closely related to human pathogens, such asBartonella rochalimae.more » « lessFree, publicly-accessible full text available December 11, 2025
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            Abstract Species that are geographically widespread may exist across environmentally heterogeneous landscapes that could influence patterns of occupation and phylogeographic structure. Previous studies have suggested that geographic range size should be positively correlated with niche breadth, allowing widespread species to sustain viable populations over diverse environmental gradients. We examined the congruence of phenotypic and phylogenetic divergence with the environmental factors that help maintain species level diversity in the geographically widespread hoary bats ( Lasiurus cinereus sensu lato) across their distribution. Genetic sequences were analyzed using multiple phylogenetic and species delimitation methods, and phenotypic data were analyzed using supervised and unsupervised machine learning approaches. Spatial data from environmental, geographic, and topographic features were analyzed in a multiple regression analysis to determine their relative effect on phenotypic diversity. Ecological niches of each hoary bat species were examined in environmental space to quantify niche overlap, equivalency, and the magnitude of niche differentiation. Phylogenetic and species delimitation analyses support existence of three geographically structured species of hoary bat, each of which is phenotypically distinct. However, the Hawaiian hoary bat is morphologically more similar to the South American species than to the North American species despite a closer phylogenetic relationship to the latter. Multiple regression and niche analyses revealed higher environmental similarities between the South American and Hawaiian species. Hoary bats thus exhibit a pattern of phenotypic variation that disagrees with well-supported genetic divergences, instead indicating phenotypic convergence driven by similar environmental features and relatively conserved niches occupied in tropical latitudes.more » « less
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            Pfeifer, Susanne (Ed.)Abstract Bats are exceptional among mammals for their powered flight, extended lifespans, and robust immune systems and therefore have been of particular interest in comparative genomics. Using the Oxford Nanopore Technologies long-read platform, we sequenced the genomes of two bat species with key phylogenetic positions, the Jamaican fruit bat (Artibeus jamaicensis) and the Mesoamerican mustached bat (Pteronotus mesoamericanus), and carried out a comprehensive comparative genomic analysis with a diverse collection of bats and other mammals. The high-quality, long-read genome assemblies revealed a contraction of interferon (IFN)-α at the immunity-related type I IFN locus in bats, resulting in a shift in relative IFN-ω and IFN-α copy numbers. Contradicting previous hypotheses of constitutive expression of IFN-α being a feature of the bat immune system, three bat species lost all IFN-α genes. This shift to IFN-ω could contribute to the increased viral tolerance that has made bats a common reservoir for viruses that can be transmitted to humans. Antiviral genes stimulated by type I IFNs also showed evidence of rapid evolution, including a lineage-specific duplication of IFN-induced transmembrane genes and positive selection in IFIT2. In addition, 33 tumor suppressors and 6 DNA-repair genes showed signs of positive selection, perhaps contributing to increased longevity and reduced cancer rates in bats. The robust immune systems of bats rely on both bat-wide and lineage-specific evolution in the immune gene repertoire, suggesting diverse immune strategies. Our study provides new genomic resources for bats and sheds new light on the extraordinary molecular evolution in this critically important group of mammals.more » « less
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            Bats carry many zoonotic pathogens without showing pronounced pathology, with a few exceptions. The underlying immune tolerance mechanisms in bats remain poorly understood, although information-rich omics tools hold promise for identifying a wide range of immune markers and their relationship with infection. To evaluate the generality of immune responses to infection, we assessed the differences and similarities in serum proteomes of wild vampire bats (Desmodus rotundus) across infection status with five taxonomically distinct pathogens: bacteria (Bartonellaspp., hemoplasmas), protozoa (Trypanosoma cruzi), and DNA (herpesviruses) and RNA (alphacoronaviruses) viruses. From 19 bats sampled in 2019 in Belize, we evaluated the up- and downregulated immune responses of infected versus uninfected individuals for each pathogen. Using a high-quality genome annotation for vampire bats, we identified 586 serum proteins but found no evidence for differential abundance nor differences in composition between infected and uninfected bats. However, using receiver operating characteristic curves, we identified four to 48 candidate biomarkers of infection depending on the pathogen, including seven overlapping biomarkers (DSG2, PCBP1, MGAM, APOA4, DPEP1, GOT1, and IGFALS). Enrichment analysis of these proteins revealed that our viral pathogens, but not the bacteria or protozoa studied, were associated with upregulation of extracellular and cytoplasmatic secretory vesicles (indicative of viral replication) and downregulation of complement activation and coagulation cascades. Additionally, herpesvirus infection elicited a downregulation of leukocyte-mediated immunity and defense response but an upregulation of an inflammatory and humoral immune response. In contrast to our two viral infections, we found downregulation of lipid and cholesterol homeostasis and metabolism withBartonellaspp. infection, of platelet-dense and secretory granules with hemoplasma infection, and of blood coagulation pathways withT. cruziinfection. Despite the small sample size, our results suggest that vampire bats have a similar suite of immune mechanisms for viruses distinct from responses to the other pathogen taxa, and we identify potential biomarkers that can expand our understanding of pathogenesis of these infections in bats. By applying a proteomic approach to a multi-pathogen system in wild animals, our study provides a distinct framework that could be expanded across bat species to increase our understanding of how bats tolerate pathogens.more » « less
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            Abstract Substantial global attention is focused on how to reduce the risk of future pandemics. Reducing this risk requires investment in prevention, preparedness, and response. Although preparedness and response have received significant focus, prevention, especially the prevention of zoonotic spillover, remains largely absent from global conversations. This oversight is due in part to the lack of a clear definition of prevention and lack of guidance on how to achieve it. To address this gap, we elucidate the mechanisms linking environmental change and zoonotic spillover using spillover of viruses from bats as a case study. We identify ecological interventions that can disrupt these spillover mechanisms and propose policy frameworks for their implementation. Recognizing that pandemics originate in ecological systems, we advocate for integrating ecological approaches alongside biomedical approaches in a comprehensive and balanced pandemic prevention strategy.more » « less
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            ABSTRACT Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells – lymphocytes and granulocytes (neutrophils/heterophils) – across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there may be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections.more » « less
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