193 results on '"Hoberg EP"'
Search Results
2. Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites
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Galbreath, KE, Hoberg, EP, Cook, JA, Armien, B, Bell, KC, Campbell, ML, Dunnum, JL, Dursahinhan, AT, Eckerlin, RP, Gardner, SL, Greiman, SE, Henttonen, H, Jimenez, FA, Koehler, AVA, Nyamsuren, B, Tkach, VV, Torres-Perez, F, Tsvetkova, A, Hope, AG, Galbreath, KE, Hoberg, EP, Cook, JA, Armien, B, Bell, KC, Campbell, ML, Dunnum, JL, Dursahinhan, AT, Eckerlin, RP, Gardner, SL, Greiman, SE, Henttonen, H, Jimenez, FA, Koehler, AVA, Nyamsuren, B, Tkach, VV, Torres-Perez, F, Tsvetkova, A, and Hope, AG
- Abstract
Museum specimens play an increasingly important role in predicting the outcomes and revealing the consequences of anthropogenically driven disruption of the biosphere. As ecological communities respond to ongoing environmental change, host-parasite interactions are also altered. This shifting landscape of host-parasite associations creates opportunities for colonization of different hosts and emergence of new pathogens, with implications for wildlife conservation and management, public health, and other societal concerns. Integrated archives that document and preserve mammal specimens along with their communities of associated parasites and ancillary data provide a powerful resource for investigating, anticipating, and mitigating the epidemiological, ecological, and evolutionary impacts of environmental perturbation. Mammalogists who collect and archive mammal specimens have a unique opportunity to expand the scope and impact of their field work by collecting the parasites that are associated with their study organisms. We encourage mammalogists to embrace an integrated and holistic sampling paradigm and advocate for this to become standard practice for museum-based collecting. To this end, we provide a detailed, field-tested protocol to give mammalogists the tools to collect and preserve host and parasite materials that are of high quality and suitable for a range of potential downstream analyses (e.g., genetic, morphological). Finally, we also encourage increased global cooperation across taxonomic disciplines to build an integrated series of baselines and snapshots of the changing biosphere. Los especímenes de museo desempeñan un papel cada vez más importante tanto en la descripción de los resultados de la alteración antropogénica de la biosfera como en la predicción de sus consecuencias. Dado que las comunidades ecológicas responden al cambio ambiental, también se alteran las interacciones hospedador-parásito. Este panorama cambiante de asociaciones hospedador-p
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- 2019
3. Phylogenomic and biogeographic reconstruction of the Trichinella complex
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Korhonen, PK, Pozio, E, La Rosa, G, Chang, BCH, Koehler, AV, Hoberg, EP, Boag, PR, Tan, P, Jex, AR, Hofmann, A, Sternberg, PW, Young, ND, Gasser, RB, Korhonen, PK, Pozio, E, La Rosa, G, Chang, BCH, Koehler, AV, Hoberg, EP, Boag, PR, Tan, P, Jex, AR, Hofmann, A, Sternberg, PW, Young, ND, and Gasser, RB
- Abstract
Trichinellosis is a globally important food-borne parasitic disease of humans caused by roundworms of the Trichinella complex. Extensive biological diversity is reflected in substantial ecological and genetic variability within and among Trichinella taxa, and major controversy surrounds the systematics of this complex. Here we report the sequencing and assembly of 16 draft genomes representing all 12 recognized Trichinella species and genotypes, define protein-coding gene sets and assess genetic differences among these taxa. Using thousands of shared single-copy orthologous gene sequences, we fully reconstruct, for the first time, a phylogeny and biogeography for the Trichinella complex, and show that encapsulated and non-encapsulated Trichinella taxa diverged from their most recent common ancestor ∼21 million years ago (mya), with taxon diversifications commencing ∼10-7 mya.
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- 2016
4. Integrated approaches and empirical models for investigation of parasitic diseases in northern wildlife.
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Hoberg EP, Polley L, Jenkins EJ, Kutz SJ, Veitch AM, Elkin BT, Hoberg, Eric P, Polley, Lydden, Jenkins, Emily J, Kutz, Susan J, Veitch, Alasdair M, and Elkin, Brett T
- Abstract
The North is a frontier for exploration of emerging infectious diseases and the large-scale drivers influencing distribution, host associations, and evolution of pathogens among persons, domestic animals, and wildlife. Leading into the International Polar Year 2007-2008, we outline approaches, protocols, and empirical models derived from a decade of integrated research on northern host-parasite systems. Investigations of emerging infectious diseases associated with parasites in northern wildlife involved a network of multidisciplinary collaborators and incorporated geographic surveys, archival collections, historical foundations for diversity, and laboratory and field studies exploring the interface for hosts, parasites, and the environment. In this system, emergence of parasitic disease was linked to geographic expansion, host switching, resurgence due to climate change, and newly recognized parasite species. Such integrative approaches serve as cornerstones for detection, prediction, and potential mitigation of emerging infectious diseases in wildlife and persons in the North and elsewhere under a changing global climate. [ABSTRACT FROM AUTHOR]
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- 2008
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5. Trichinella: Becoming a parasite.
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Zarlenga DS, Hoberg EP, Thompson P, and Rosenthal B
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Phylogenetic evidence indicates that free-living nematodes gave rise to parasitic nematodes where parasitism evolved independently at least 15 times. The high level of genetic and biological diversity among parasites dictates an equally high level of diversity in the transition to parasitism. We previously hypothesized that horizontal gene transfer (HGT) played an important role in the evolution of parasitism among early ancestors of Trichinella, mediated by an interplay of ecological and evolutionary pathways that contributed to persistence and diversification. We propose that host selection may have been associated with the metabolism of ammonia and engender a new paradigm whereby the reprogrammed nurse cell is capable of generating cyanate thereby enabling the importance of the Trichinella cyanase in the longevity of the cell. Parasites and parasitism have revealed considerable resilience against a backdrop of climate change and environmental perturbation. Here we provide a putative link between key periods in the evolution of Trichinella and major geological and climatological events dating back 500 million years. A useful lens for exploring such ideas, the Stockholm Paradigm, integrates Ecological Fitting (a foundation for host colonization and diversification), the Oscillation Hypothesis (recurring shifts between trends in generalization and specialization relative to host range), the Geographic Mosaic Theory of Coevolution (microevolutionary co-adaptive processes), and the Taxon Pulse Hypothesis (alternating events of biotic expansion i.e., exploitation in evolutionary and ecological time). Here we examine how one or more of these interactive theories, in a phylogenetic-historical context and in conjunction with HGT, may help explain the scope and depth of diversity among Trichinella genotypes., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Published by Elsevier B.V.)
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- 2024
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6. Late Cenozoic history and the role of Beringia in assembling a Holarctic cestode species complex.
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Galbreath KE, Makarikov AA, Bell KC, Greiman SE, Allen JM, Haas GMS, Li C, Cook JA, and Hoberg EP
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- Animals, Phylogeny, North America, Climate, Mammals, Arvicolinae, Cestoda genetics, Parasites
- Abstract
The dynamic climate history that drove sea level fluctuation during past glacial periods mediated the movement of organisms between Asia and North America via the Bering Land Bridge. Investigations of the biogeographic histories of small mammals and their parasites demonstrate facets of a complex history of episodic geographic colonization and refugial isolation that structured diversity across the Holarctic. We use a large multi-locus nuclear DNA sequence dataset to robustly resolve relationships within the cestode genus Arostrilepis (Cyclophyllidea: Hymenolepididae), a widespread parasite of predominantly arvicoline rodents (voles, lemmings). Using this phylogeny, we confirm that several Asian Arostrilepis lineages colonized North America during up to four distinct glacial periods in association with different rodent hosts, consistent with taxon-pulse dynamics. A previously inferred westward dispersal across the land bridge is rejected. We also refine interpretations of past host colonization, providing evidence for several distinct episodes of expanding host range, which probably contributed to diversification by Arostrilepis. Finally, Arostrilepis is shown to be paraphyletic with respect to Hymenandrya thomomyis, a parasite of pocket gophers, confirming that ancient Arostrilepis species colonized new host lineages upon arriving in North America., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 Elsevier Inc. All rights reserved.)
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- 2023
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7. Ecological super-spreaders drive host-range oscillations: Omicron and risk space for emerging infectious disease.
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Boeger WA, Brooks DR, Trivellone V, Agosta SJ, and Hoberg EP
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- Animals, Host Specificity, Humans, Mammals, SARS-CoV-2 genetics, COVID-19 epidemiology, COVID-19 veterinary, Communicable Diseases, Emerging epidemiology, Communicable Diseases, Emerging veterinary
- Abstract
The unusual genetic diversity of the Omicron strain has led to speculation about its origin. The mathematical modelling platform developed for the Stockholm Paradigm (SP) indicates strongly that it has retro-colonized humans from an unidentified nonhuman mammal, likely originally infected by humans. The relationship between Omicron and all other SARS-CoV-2 variants indicates oscillations among hosts, a core part of the SP. Such oscillations result from the emergence of novel variants following colonization of new hosts, replenishing and expanding the risk space for disease emergence. The SP predicts that pathogens colonize new hosts using pre-existing capacities. Those events are thus predictable to a certain extent. Novel variants emerge after a colonization and are not predictable. This makes it imperative to take proactive measures for anticipating emerging infectious diseases (EID) and mitigating their impact. The SP suggests a policy protocol, DAMA, to accomplish this goal. DAMA comprises: DOCUMENT to detect pathogens before they emerge in new places or colonize new hosts; ASSESS to determine risk; MONITOR to detect changes in pathogen populations that increase the risk of outbreaks and ACT to prevent outbreaks when possible and minimize their impact when they occur., (© 2022 Wiley-VCH GmbH.)
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- 2022
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8. MORPHOMETRY OF FIRST-STAGE LARVAE OF ORTHOSTRONGYLUS MACROTIS (NEMATODA: PROTOSTRONGYLIDAE), LUNGWORM OF WILD UNGULATES FROM WESTERN NORTH AMERICA.
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Verocai GG, Kafle P, Sulliotti V, Lejeune M, Hoberg EP, and Kutz SJ
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- Animals, DNA, Ribosomal Spacer genetics, Larva genetics, North America, Phylogeny, Deer parasitology, Metastrongyloidea, Strongylida Infections parasitology, Strongylida Infections veterinary
- Abstract
Orthostrongylus macrotis (Dikmans, 1931) is a protostrongylid lungworm in wild ungulates from western North America, including mule and Columbia black-tailed deer, pronghorn, and rarely moose and elk. The lack of morphological data for certain developmental stages of O. macrotis and the unresolved taxonomic status of the genus indicate a more detailed morphological characterization of the species is necessary. We provide a detailed description of first-stage larvae (L1) of O. macrotis including morphological, morphometric, and molecular data. Species identity was confirmed based on molecular sequence data from the internal transcribed spacer subunit 2 (ITS-2) and large subunit (28S) rDNA. A fragment of the cytochrome oxidase c subunit 1 (COI) was also sequenced, followed by the determination of genetic distance and phylogenetic analyses. Integrated data describing L1 of O. macrotis contributes to a broader understanding of the parasite fauna of wild ungulates from North America and may be of relevance for a future revision of the genus. Further, we outline information for differentiation among species of North American protostrongylids, with typical spike-tailed L1s, circulating among free-ranging and semi-domestic ungulates., (© American Society of Parasitologists 2022.)
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- 2022
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9. Emerging infectious disease: An underappreciated area of strategic concern for food security.
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Brooks DR, Hoberg EP, Boeger WA, and Trivellone V
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- Animals, Biodiversity, Climate Change, Food Security, Public Health, Communicable Diseases, Emerging epidemiology, Communicable Diseases, Emerging prevention & control, Communicable Diseases, Emerging veterinary
- Abstract
Emerging infectious diseases (EIDs) increasingly threaten global food security and public health. Despite technological breakthroughs, we are losing the battle with (re)emerging diseases as treatment costs and production losses rise. A horizon scan of diseases of crops, livestock, seafood and food-borne illness suggests these costs are unsustainable. The paradigm of coevolution between pathogens and particular hosts teaches that emerging diseases occur only when pathogens evolve specific capacities that allow them to move to new hosts. EIDs ought to be rare and unpredictable, so crisis response is the best we can do. Alternatively, the Stockholm Paradigm suggests that the world is full of susceptible but unexposed hosts that pathogens could infect, given the opportunity. Global climate change, globalized trade and travel, urbanization and land-use changes (often associated with biodiversity loss) increase those opportunities, making EID frequent. We can, however, anticipate their arrival in new locations and their behaviour once they have arrived. We can 'find them before they find us', mitigating their impacts. The DAMA (Document, Assess, Monitor, Act) protocol alters the current reactive stance and embodies proactive solutions to anticipate and mitigate the impacts of EID, extending human and material resources and buying time for development of new vaccinations, medications and control measures., (© 2021 The Authors. Transboundary and Emerging Diseases published by Wiley-VCH GmbH.)
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- 2022
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10. Food security and emerging infectious disease: risk assessment and risk management.
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Trivellone V, Hoberg EP, Boeger WA, and Brooks DR
- Abstract
Climate change, emerging infectious diseases (EIDs) and food security create a dangerous nexus. Habitat interfaces, assumed to be efficient buffers, are being disrupted by human activities which in turn accelerate the movement of pathogens. EIDs threaten directly and indirectly availability and access to nutritious food, affecting global security and human health. In the next 70 years, food-secure and food-insecure countries will face EIDs driving increasingly unsustainable costs of production, predicted to exceed national and global gross domestic products. Our modern challenge is to transform this business as usual and embrace an alternative vision of the biosphere formalized in the Stockholm paradigm (SP). First, a pathogen-centric focus shifts our vision of risk space , determining how pathogens circulate in realized and potential fitness space. Risk space and pathogen exchange are always heightened at habitat interfaces. Second, apply the document-assess-monitor-act (DAMA) protocol developing strategic data for EID risk, to be translated, synthesized and broadcast as actionable information. Risk management is realized through targeted interventions focused around information exchanged among a community of scientists, policy practitioners of food and public health security and local populations. Ultimately, SP and DAMA protect human rights, supporting food security, access to nutritious food, health interventions and environmental integrity., (© 2022 The Authors.)
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- 2022
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11. Leveraging natural history biorepositories as a global, decentralized, pathogen surveillance network.
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Colella JP, Bates J, Burneo SF, Camacho MA, Carrion Bonilla C, Constable I, D'Elía G, Dunnum JL, Greiman S, Hoberg EP, Lessa E, Liphardt SW, Londoño-Gaviria M, Losos E, Lutz HL, Ordóñez Garza N, Peterson AT, Martin ML, Ribas CC, Struminger B, Torres-Pérez F, Thompson CW, Weksler M, and Cook JA
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- Animals, Animals, Wild, Biodiversity, Biological Specimen Banks standards, Biological Specimen Banks supply & distribution, Biological Specimen Banks trends, COVID-19 epidemiology, Communicable Diseases, Emerging epidemiology, Communicable Diseases, Emerging microbiology, Communicable Diseases, Emerging virology, Community Networks standards, Community Networks supply & distribution, Community Networks trends, Disaster Planning methods, Disaster Planning organization & administration, Disaster Planning standards, Geography, Global Health standards, Global Health trends, Humans, Medical Countermeasures, Pandemics prevention & control, Public Health, Risk Assessment, SARS-CoV-2 physiology, Zoonoses epidemiology, Zoonoses prevention & control, Biological Specimen Banks organization & administration, Communicable Disease Control methods, Communicable Disease Control organization & administration, Communicable Disease Control standards, Communicable Diseases, Emerging prevention & control, Community Networks organization & administration, Public Health Surveillance methods
- Abstract
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., Competing Interests: The authors have declared that no competing interests exist.
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- 2021
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12. High prevalence, intensity, and genetic diversity of Trichinella spp. in wolverine (Gulo gulo) from Yukon, Canada.
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Sharma R, Harms NJ, Kukka PM, Jung TS, Parker SE, Ross S, Thompson P, Rosenthal B, Hoberg EP, and Jenkins EJ
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- Age Factors, Animals, Animals, Wild parasitology, Canada epidemiology, Cross-Sectional Studies, Female, Genotype, Male, Prevalence, Risk Factors, Tongue parasitology, Trichinella classification, Yukon Territory epidemiology, Genetic Variation, Mustelidae parasitology, Trichinella genetics, Trichinellosis epidemiology, Trichinellosis veterinary
- Abstract
Background: Species of Trichinella are globally important foodborne parasites infecting a number of domestic and wild vertebrates, including humans. Free-ranging carnivores can act as sentinel species for detection of Trichinella spp. Knowledge of the epidemiology of these parasites may help prevent Trichinella spp. infections in northern Canadian animals and people. Previous research on Trichinella spp. in wildlife from Yukon did not identify risk factors associated with infection, or the diversity and identity of species of Trichinella in regional circulation, based on geographically extensive sampling with large sample sizes., Methods: In a cross-sectional study, we determined the prevalence, infection intensity, risk factors, and species or genotypes of Trichinella in wolverine (Gulo gulo) in two regions of Yukon, Canada, from 2013-2017. A double separatory funnel digestion method followed by mutiplex PCR and PCR-RFLP were used to recover and identify species of Trichinella, respectively., Results: We found larvae of Trichinella in the tongues of 78% (95% CI 73-82) of 338 wolverine sampled. The odds of adult (≥ 2 years) and yearling (1 year) wolverine being Trichinella spp.-positive were four and two times higher, respectively, compared to juveniles (<1 year). The odds of Trichinella spp. presence were three times higher in wolverine from southeast than northwest Yukon. The mean intensity of infection was 22.6 ± 39 (SD, range 0.1-295) larvae per gram. Trichinella T6 was the predominant genotype (76%), followed by T. nativa (8%); mixed infections with Trichinella T6 and T. nativa (12%) were observed. In addition, T. spiralis was detected in one wolverine. Out of 22 isolates initially identified as T. nativa in multiplex PCR, 14 were analyzed by PCR-RFLP to distinguish them from T. chanchalensis, a recently discovered cryptic species, which cannot be distinguished from the T. nativa on multiplex PCR. Ten isolates were identified either as T. chanchalensis alone (n = 7), or mixed infection with T. chanchalensis and T. nativa (n = 2) or T. chanchalensis and Trichinella T6 (n = 1)]., Conclusions: Wolverine hosted high prevalence, high larval intensity, and multiple species of Trichinella, likely due to their scavenging habits, apex position in the food chain, and wide home range. Wolverine (especially adult males) should be considered as a sentinel species for surveys for Trichinella spp. across their distributional range.
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- 2021
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13. When parasites persist: tapeworms survive host extinction and reveal waves of dispersal across Beringia.
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Galbreath KE, Toman HM, Li C, and Hoberg EP
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- Animals, Asia, Host-Parasite Interactions, North America, Parasites, Biological Evolution, Cestoda physiology, Lagomorpha parasitology
- Abstract
Investigations of intercontinental dispersal between Asia and North America reveal complex patterns of geographic expansion, retraction and isolation, yet historical reconstructions are largely limited by the depth of the record that is retained in patterns of extant diversity. Parasites offer a tool for recovering deep historical insights about the biosphere, improving the resolution of past community-level interactions. We explored biogeographic hypotheses regarding the history of dispersal across Beringia, the region intermittently linking Asia and North America, through large-scale multi-locus phylogenetic analyses of the genus Schizorchis , an assemblage of host-specific cestodes in pikas (Lagomorpha: Ochotonidae). Our genetic data support palaeontological evidence for two separate geographic expansions into North America by Ochotona in the late Tertiary, a history that genomic evidence from extant pikas does not record. Pikas descending from the first colonization of Miocene age persisted into the Pliocene, subsequently coming into contact with a second wave of Nearctic colonists from Eurasia before going extinct. Spatial and temporal overlap of historically independent pika populations provided a window for host colonization, allowing persistence of an early parasite lineage in the contemporary fauna following the extinction of its ancestral hosts. Empirical evidence for ancient 'ghost assemblages' of hosts and parasites demonstrates how complex mosaic faunas are assembled in the biosphere through episodes of faunal mixing encompassing parasite lineages across deep and shallow time.
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- 2020
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14. Parasite intensity drives fetal development and sex allocation in a wild ungulate.
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Aleuy OA, Serrano E, Ruckstuhl KE, Hoberg EP, and Kutz S
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- Animals, Animals, Wild, Female, Male, Sex Factors, Sheep, Sheep Diseases pathology, Trichostrongyloidiasis parasitology, Trichostrongyloidiasis pathology, Fetal Development, Sheep Diseases parasitology, Trichostrongyloidea physiology, Trichostrongyloidiasis veterinary
- Abstract
An understanding of the mechanisms influencing prenatal characteristics is fundamental to comprehend the role of ecological and evolutionary processes behind survival and reproductive success in animals. Although the negative influence of parasites on host fitness is undisputable, we know very little about how parasitic infection in reproductive females might influence prenatal factors such as fetal development and sex allocation. Using an archival collection of Dall's sheep (Ovis dalli dalli), a capital breeder that depends on its body reserves to overcome the arctic winter, we investigated the direct and indirect impacts of the parasite community on fetal development and sex allocation. Using partial least squares modelling, we observed a negative effect of parasite community on fetal development, driven primarily by the nematode Marshallagia marshalli. Principal component analysis demonstrated that mothers with low parasite burden and in good body condition were more likely to have female versus male fetuses. This association was primarily driven by the indirect effect of M. marshalli on ewe body condition. Refining our knowledge of the direct and indirect impact that parasite communities can have on reproduction in mammals is critical for understanding the effects of infectious diseases on wildlife populations. This can be particularly relevant for species living in ecosystems sensitive to the effects of global climate change.
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- 2020
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15. Hiding in plain sight: discovery and phylogeography of a cryptic species of Trichinella (Nematoda: Trichinellidae) in wolverine (Gulo gulo).
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Sharma R, Thompson PC, Hoberg EP, Brad Scandrett W, Konecsni K, Harms NJ, Kukka PM, Jung TS, Elkin B, Mulders R, Larter NC, Branigan M, Pongracz J, Wagner B, Kafle P, Lobanov VA, Rosenthal BM, and Jenkins EJ
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- Alaska, Animals, Canada, DNA, Helminth genetics, DNA, Ribosomal genetics, Genome, Mitochondrial genetics, Life Cycle Stages, Phylogeny, Phylogeography, Polymerase Chain Reaction methods, Polymerase Chain Reaction veterinary, Siberia, Trichinella spiralis anatomy & histology, Trichinella spiralis classification, Trichinella spiralis genetics, Trichinella spiralis isolation & purification, Trichinellosis parasitology, Trichinellosis veterinary, Mustelidae parasitology, Trichinella anatomy & histology, Trichinella classification, Trichinella genetics, Trichinella isolation & purification
- Abstract
Understanding parasite diversity and distribution is essential in managing the potential impact of parasitic diseases in animals and people. Imperfect diagnostic methods, however, may conceal cryptic species. Here, we report the discovery and phylogeography of a previously unrecognized species of Trichinella in wolverine (Gulo gulo) from northwestern Canada that was indistinguishable from T. nativa using the standard multiplex PCR assay based on the expansion segment 5 (ESV) of ribosomal DNA. The novel genotype, designated as T13, was discovered when sequencing the mitochondrial genome. Phylogenetic analyses of the mitochondrial genome and of 15 concatenated single copy orthologs of nuclear DNA indicated a common ancestor for the encapsulated clade is shared by a subclade containing Trichinella spiralis and Trichinella nelsoni, and a subclade containing T13 and remaining taxa: T12 + (T2 + T6) + [(T5 + T9) + (T3 + T8)]. Of 95 individual hosts from 12 species of mammalian carnivores from northwestern Canada from which larvae were identified as T. nativa on multiplex PCR, only wolverines were infected with T13 (14 of 42 individuals). These infections were single or mixed with T. nativa and/or T6. Visual examination and motility testing confirmed that T13 is encapsulated and likely freeze-tolerant. We developed a new Polymerase Chain Reaction-Restriction Fragment Length Polymorphism which unequivocally distinguishes between T13 and T. nativa. We propose Trichinella chanchalensis n. sp. for T13, based on significant genetic divergence from other species of Trichinella and broad-based sampling of the Trichinella genome. Exploration of Alaskan and Siberian isolates may contribute to further resolution of a phylogeographically complex history for species of Trichinella across Beringia, including Trichinella chanchalensis n. sp. (T13)., (Published by Elsevier Ltd.)
- Published
- 2020
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16. Wild ruminants as reservoirs of domestic livestock gastrointestinal nematodes.
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Barone CD, Wit J, Hoberg EP, Gilleard JS, and Zarlenga DS
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- Animals, Cattle, Cattle Diseases epidemiology, Cattle Diseases parasitology, High-Throughput Nucleotide Sequencing methods, Polymerase Chain Reaction methods, Prevalence, Trichostrongyloidea classification, Trichostrongyloidiasis epidemiology, Trichostrongyloidiasis parasitology, United States epidemiology, Animals, Wild, DNA, Ribosomal Spacer analysis, High-Throughput Nucleotide Sequencing veterinary, Polymerase Chain Reaction veterinary, Ruminants, Trichostrongyloidea isolation & purification, Trichostrongyloidiasis veterinary
- Abstract
Gastrointestinal nematode (GIN) infections in cattle cause appetite suppression which leads to poor feed conversion, reduced weight gain and reduced milk production. Overuse and exclusive reliance on anthelmintic drugs has resulted in widespread resistance in many parasitic nematode species infecting livestock making control increasingly difficult. Wild ruminants are competent hosts of a number of nematode species that typically infect and are best adapted for cattle, sheep, and goats. Thus, the potential exists for wild ruminants to act as reservoirs in the translocation of domestic GIN, including those carrying anthelmintic resistance mutations as well as susceptible genotypes. The potential for parasite exchange is heightened by interfaces or ecotones between managed and wild rangelands, and by perturbations linked to climate warming that can increasingly alter the distributions of wild ungulates and their interactions with domestic and free-ranging ruminants. To investigate the extent to which wild ruminants harbour parasites capable of infecting domestic ruminants we first performed an epidemiological study of feces from wildlife hosts that spanned 16 states and included white-tailed deer (85 % of the samples), pronghorn, elk, mule deer, bighorn sheep, moose, cattle, and caribou across the United States. All samples were cultured to third stage larvae and nematode DNA was isolated and PCR amplified. Among the 548 wild ruminant samples received, 33 % (181 samples) were positive for nematode DNA, among which half (84 samples) contained DNA from GIN species commonly found in cattle. DNA from cattle GIN species was detected in 46 % of samples from the Northeast, 42 % from the Southeast, 10 % from the Midwest, 0 % from the Southwest and 11 % from the West. Deep amplicon sequencing of the ITS-2 rDNA indicated that Ostertagia and Trichostrongylus were present in 90 % and 69 % of the nematode DNA positive samples, respectively, whereas Haemonchus, Cooperia and Oesophagostomum were present in 26 %, 2 % and 10 % of the samples, respectively. These data clearly show that wild ruminants commonly harbour multiple parasite species whose primary hosts are domestic cattle, and suggest that further work is warranted to investigate their specific roles in the management of anthelmintic resistance., Competing Interests: Declaration of Competing Interest None., (Copyright © 2020 Elsevier B.V. All rights reserved.)
- Published
- 2020
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17. Phenotypic plasticity and local adaptation in freeze tolerance: Implications for parasite dynamics in a changing world.
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Aleuy OA, Peacock S, Hoberg EP, Ruckstuhl KE, Brooks T, Aranas M, and Kutz S
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- Acclimatization, Adaptation, Physiological, Animals, Climate Change, Eggs, Feces parasitology, Freezing, Gastrointestinal Tract parasitology, Nematoda parasitology, Nematoda physiology, North America, Population Dynamics, Ruminants, Sheep Diseases parasitology, Temperature, Trichostrongyloidea parasitology, Sheep parasitology, Sheep, Bighorn parasitology, Strongylida Infections veterinary, Trichostrongyloidea physiology
- Abstract
Marshallagia marshalli is a multi-host gastrointestinal nematode that infects a variety of artiodactyl species from temperate to Arctic latitudes. Eggs of Marshallagia are passed in host faeces and develop through three larval stages (L1, L2, and L3) in the environment. Although eggs normally hatch as L1s, they can also hatch as L3s. We hypothesised that this phenotypic plasticity in hatching behaviour may improve fitness in subzero and highly variable environments, and this may constitute an evolutionary advantage under current climate change scenarios. To test this, we first determined if the freeze tolerance of different free-living stages varied at different temperatures (-9 °C, -20 °C and -35 °C). We then investigated if there were differences in freeze tolerance of M. marshalli eggs sourced from three discrete, semi-isolated, populations of wild bighorn and thinhorn sheep living in western North America (latitudes: 40°N, 50°N, 64°N). The survival rates of eggs and L3s were significantly higher than L1s at -9 °C and -20 °C, and survival of all three stages decreased significantly with increasing freeze duration and decreasing temperature. The survival of unhatched L1s was significantly higher than the survival of hatched L1s. There was no evidence of local thermal adaptation in freeze tolerance among eggs from different locations. We conclude that developing to the L3 in the egg may result in a fitness advantage for M. marshalli, with the egg protecting the more vulnerable L1 under freezing conditions. This phenotypic plasticity in life-history traits of M. marshalli might be an important capacity, a potential exaptation capable of enhancing parasite fitness under temperature extremes., (Copyright © 2020 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved.)
- Published
- 2020
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18. Conservation Genomics in a Changing Arctic.
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Colella JP, Talbot SL, Brochmann C, Taylor EB, Hoberg EP, and Cook JA
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- Arctic Regions, Climate Change, Conservation of Natural Resources, Genomics, Biodiversity, Ecosystem
- Abstract
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., (Copyright © 2019 Elsevier Ltd. All rights reserved.)
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- 2020
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19. Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America.
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Makarikov AA, Galbreath KE, Eckerlin RP, and Hoberg EP
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- Animals, Cestoda classification, Female, Male, North America, Phylogeny, Arvicolinae parasitology, Cestoda isolation & purification
- Abstract
Species of the genus Arostrilepis were discovered and definitively identified for the first time in rodents from geographically disparate localities along the Appalachian Mountain range of eastern North America (West Virginia, Virginia, and Maine). These are the first confirmed records for species of Arostrilepis occurring east of the Rocky Mountains and the Mississippi River in North America. Arostrilepis gardneri n. sp. is described on the basis of specimens obtained from two phylogenetically divergent rodent hosts: Southern Red-Backed Vole Myodes gapperi (Cricetidae: Arvicolinae) (from West Virginia) and the Woodland Jumping Mouse Napaeozapus insignis (Dipodidae: Zapodinae) (West Virginia, Virginia, and Maine). Additionally, in a mixed infection, specimens of Arostrilepis insperata n. sp. were also found in a Southern Red-Backed Vole from West Virginia. These previously unknown species are primarily distinguished from congeners based on shape, dimensions, and spination (pattern, shape, and size of spines) of the cirrus. Specimens of A. gardneri n. sp. are further characterized by the relative position and length of the cirrus-sac, arrangement of the testes, and relative size of the external seminal vesicle and seminal receptacle. Specimens of A. insperata n. sp. are structurally most similar to A. macrocirrosa from the western Nearctic and Palearctic but with consistently greater dimensions for the cirrus-sac, testes, and seminal receptacle. Phylogenetic analysis of Arostrilepis spp. using partial sequences of the mitochondrial cytochrome b gene and the nuclear second ribosomal internal transcribed spacer strongly supported the status of A. gardneri n. sp. and A. insperata n. sp. within an unresolved clade of congeners in Red-Backed Voles (Myodini and species of Myodes). Our observations extend the known geographic distribution for species of Arostrilepis to the Appalachian Mountains in either a disjunct or possibly continuous but patchy range across North America. Prior observations, summarizing field and museum collections, had suggested that geographic ranges for a diverse assemblage of Arostrilepis in North America were largely restricted to the north-western region of the continent, with historical connections to Beringia and Eurasia. Recognition of a more extensive distribution is consistent with a history of episodic biotic expansion and isolation under a dynamic of taxon pulses for arvicoline rodents and an associated parasite fauna in the Nearctic during the Quaternary. Occurrence in a dipodid rodent represents an event of host colonization from an arvicoline source.
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- 2020
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20. The biogeography of the caribou lungworm, Varestrongylus eleguneniensis (Nematoda: Protostrongylidae) across northern North America.
- Author
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Verocai GG, Hoberg EP, Simard M, Beckmen KB, Musiani M, Wasser S, Cuyler C, Manseau M, Chaudhry UN, Kashivakura CK, Gilleard JS, and Kutz SJ
- Abstract
Varestrongylus eleguneniensis (Nematoda; Protostrongylidae) is a recently described species of lungworm that infects caribou ( Rangifer tarandus ), muskoxen ( Ovibos moschatus ) and moose ( Alces americanus ) across northern North America. Herein we explore the geographic distribution of V. eleguneniensis through geographically extensive sampling and discuss the biogeography of this multi-host parasite. We analyzed fecal samples of three caribou subspecies (n = 1485), two muskox subspecies (n = 159), and two moose subspecies (n = 264) from across northern North America. Protostrongylid dorsal-spined larvae (DSL) were found in 23.8%, 73.6%, and 4.2% of these ungulates, respectively. A portion of recovered DSL were identified by genetic analyses of the ITS-2 region of the nuclear rDNA or the cytochrome oxidase c subunit I (COI) region of the mtDNA. We found V. eleguneniensis widely distributed among caribou and muskox populations across most of their geographic prange in North America but it was rare in moose. Parelaphostrongylus andersoni was present in caribou and moose and we provide new geographic records for this species. This study provides a substantial expansion of the knowledge defining the current distribution and biogeography of protostrongylid nematodes in northern ungulates. Insights about the host and geographic range of V. eleguneniensis can serve as a geographically extensive baseline for monitoring current distribution and in anticipating future biogeographic scenarios under a regime of accelerating climate and anthropogenic perturbation., Competing Interests: The authors declare no conflict of interest., (© 2020 The Author(s).)
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- 2020
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21. Adaptations and phenotypic plasticity in developmental traits of Marshallagia marshalli.
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Aleuy OA, Hoberg EP, Paquette C, Ruckstuhl KE, and Kutz S
- Subjects
- Alberta, Animals, Environment, Feces parasitology, Hot Temperature, Larva physiology, Phenotype, Sheep, Bighorn parasitology, Trichostrongyloidea classification, Trichostrongyloidea genetics, Trichostrongyloidea growth & development, Trichostrongyloidiasis parasitology, Trichostrongyloidiasis transmission, Adaptation, Physiological physiology, Life History Traits, Trichostrongyloidea physiology, Trichostrongyloidiasis veterinary
- Abstract
Despite the economic, social and ecological importance of the ostertagiine abomasal nematode Marshallagia marshalli, little is known about its life history traits and its adaptations to cope with environmental extremes. Conserved species-specific traits can act as exaptations that may enhance parasite fitness in changing environments. Using a series of experiments, we revealed several unique adaptations of the free-living stages of M. marshalli that differ from other ostertagiines. Eggs were isolated from the feces of bighorn sheep (Ovis canadensis) from the Canadian Rocky Mountains and were cultured at different temperatures and with different media. Hatching occurred primarily as L1s in an advanced stage of development, morphologically very similar to a L2. When cultured at 20 °C, however, 2.86% of eggs hatched as L3, with this phenomenon being significantly more common at higher temperatures, peaking at 30 °C with 28.95% of eggs hatching as L3s. After hatching, free-living larvae of M. marshalli did not feed nor grow as they matured from L1 to infective L3. These life history traits seem to be adaptations to cope with the extreme environmental conditions that Marshallagia faces across its extensive latitudinal distribution in North America and Eurasia. In order to refine the predictions of parasite dynamics under scenarios of a changing climate, basic life history traits and temperature-dependent phenotypic behaviour should be incorporated into models for parasite biology., (Copyright © 2019 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved.)
- Published
- 2019
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22. The next chapter of human-plague science.
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McLean BS, Cook JA, Durden LA, Hoberg EP, and Guralnick RP
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- Humans, USSR, Plague, Yersinia pestis
- Abstract
Competing Interests: The authors declare no conflict of interest.
- Published
- 2019
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23. Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites.
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Galbreath KE, Hoberg EP, Cook JA, Armién B, Bell KC, Campbell ML, Dunnum JL, Dursahinhan AT, Eckerlin RP, Gardner SL, Greiman SE, Henttonen H, Jiménez FA, Koehler AVA, Nyamsuren B, Tkach VV, Torres-Pérez F, Tsvetkova A, and Hope AG
- Abstract
Museum specimens play an increasingly important role in predicting the outcomes and revealing the consequences of anthropogenically driven disruption of the biosphere. As ecological communities respond to ongoing environmental change, host-parasite interactions are also altered. This shifting landscape of host-parasite associations creates opportunities for colonization of different hosts and emergence of new pathogens, with implications for wildlife conservation and management, public health, and other societal concerns. Integrated archives that document and preserve mammal specimens along with their communities of associated parasites and ancillary data provide a powerful resource for investigating, anticipating, and mitigating the epidemiological, ecological, and evolutionary impacts of environmental perturbation. Mammalogists who collect and archive mammal specimens have a unique opportunity to expand the scope and impact of their field work by collecting the parasites that are associated with their study organisms. We encourage mammalogists to embrace an integrated and holistic sampling paradigm and advocate for this to become standard practice for museum-based collecting. To this end, we provide a detailed, field-tested protocol to give mammalogists the tools to collect and preserve host and parasite materials that are of high quality and suitable for a range of potential downstream analyses (e.g., genetic, morphological). Finally, we also encourage increased global cooperation across taxonomic disciplines to build an integrated series of baselines and snapshots of the changing biosphere. Los especímenes de museo desempeñan un papel cada vez más importante tanto en la descripción de los resultados de la alteración antropogénica de la biosfera como en la predicción de sus consecuencias. Dado que las comunidades ecológicas responden al cambio ambiental, también se alteran las interacciones hospedador-parásito. Este panorama cambiante de asociaciones hospedador-parásito crea oportunidades para la colonización de diferentes hospedadores y para la aparición de nuevos patógenos, con implicancias en la conservación y manejo de la vida silvestre, la salud pública y otras preocupaciones de importancia para la sociedad. Archivos integrados que documentan y preservan especímenes de mamíferos junto con sus comunidades de parásitos y datos asociados, proporcionan un fuerte recurso para investigar, anticipar y mitigar los impactos epidemiológicos, ecológicos y evolutivos de las perturbaciones ambientales. Los mastozoólogos que recolectan y archivan muestras de mamíferos, tienen una oportunidad única de ampliar el alcance e impacto de su trabajo de campo mediante la recolección de los parásitos que están asociados con los organismos que estudian. Alentamos a los mastozoólogos a adoptar un paradigma de muestreo integrado y holístico y abogamos para que esto se convierta en una práctica estándarizada de la obtención de muestras para museos. Con este objetivo, proporcionamos un protocolo detallado y probado en el campo para brindar a los mastozoólogos las herramientas para recolectar y preservar materiales de parásitos y hospedadores de alta calidad y adecuados para una gran variedad de análisis subsecuentes (e.g., genéticos, morfológicos, etc.). Finalmente, también abogamos por una mayor cooperación global entre las diversas disciplinas taxonómicas para construir una serie integrada de líneas de base y registros actuales de nuestra cambiante biosfera.
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- 2019
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24. A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria.
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Zarlenga DS, Mitreva M, Thompson P, Tyagi R, Tuo W, and Hoberg EP
- Subjects
- Animals, Bacteria genetics, Plants genetics, Biological Evolution, Carbon-Nitrogen Lyases analysis, Gene Transfer, Horizontal, Helminth Proteins analysis, Nematoda genetics
- Abstract
Horizontal gene transfer (HGT) has played an important role in the evolution of nematodes. Among candidate genes, cyanase, which is typically found only in plants, bacteria and fungi, is present in more than 35 members of the Phylum Nematoda, but absent from free-living and clade V organisms. Phylogenetic analyses showed that the cyanases of clade I organisms Trichinella spp., Trichuris spp. and Soboliphyme baturini (Subclass: Dorylaimia) represent a well-supported monophyletic clade with plant cyanases. In contrast, all cyanases found within the Subclass Chromadoria which encompasses filarioids, ascaridoids and strongyloids are homologous to those of bacteria. Western blots exhibited typical multimeric forms of the native molecule in protein extracts of Trichinella spiralis muscle larvae, where immunohistochemical staining localized the protein to the worm hypodermis and underlying muscle. Recombinant Trichinella cyanase was bioactive where gene transcription profiles support functional activity in vivo. Results suggest that: (1) independent HGT in parasitic nematodes originated from different Kingdoms; (2) cyanase acquired an active role in the biology of extant Trichinella; (3) acquisition occurred more than 400 million years ago (MYA), prior to the divergence of the Trichinellida and Dioctophymatida, and (4) early, free-living ancestors of the genus Trichinella had an association with terrestrial plants.
- Published
- 2019
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25. Museum metabarcoding: A novel method revealing gut helminth communities of small mammals across space and time.
- Author
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Greiman SE, Cook JA, Tkach VV, Hoberg EP, Menning DM, Hope AG, Sonsthagen SA, and Talbot SL
- Subjects
- Animals, Biodiversity, Computational Biology, DNA, Helminth isolation & purification, DNA, Mitochondrial chemistry, DNA, Ribosomal chemistry, Feasibility Studies, Gene Library, Helminths genetics, Helminths isolation & purification, Museums, RNA, Ribosomal genetics, RNA, Ribosomal, 16S genetics, RNA, Ribosomal, 28S genetics, Time Factors, DNA Barcoding, Taxonomic methods, Gastrointestinal Tract parasitology, Helminthiasis, Animal parasitology, Helminths classification, Shrews parasitology
- Abstract
Natural history collections spanning multiple decades provide fundamental historical baselines to measure and understand changing biodiversity. New technologies such as next generation DNA sequencing have considerably increased the potential of museum specimens to address significant questions regarding the impact of environmental changes on host and parasite/pathogen dynamics. We developed a new technique to identify intestinal helminth parasites and applied it to shrews (Eulipotyphla: Soricidae) because they are ubiquitous, occupy diverse habitats, and host a diverse and abundant parasite fauna. Notably, we included museum specimens preserved in various ways to explore the efficacy of using metabarcoding analyses that may enable identification of helminth symbiont communities from historical archives. We successfully sequenced the parasite communities (using 12S mtDNA, 16S mtDNA, 28S rDNA) of 23 whole gastrointestinal tracts. All gastrointestinal tracts were obtained from the Museum of Southwestern Biology, USA, and from recent field collections, varying both in time since fixation (ranging from 4 months to 16 years) and preservation method (70% or 95% ethanol stored at room temperature, or flash frozen in liquid nitrogen and stored at -80 °C). Our proof of concept demonstrates the feasibility of applying next generation DNA sequencing techniques to authoritatively identify the parasite/pathogen communities within whole gastrointestinal tracts from museum specimens of varying age and fixation, and the value of future preservation of host-associated whole gastrointestinal tracts in public research archives. This powerful approach facilitates future comparative examinations of the distributions and interactions among multiple associated groups of organisms through time and space., (Copyright © 2018 Australian Society for Parasitology. All rights reserved.)
- Published
- 2018
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26. A cryptic species of Onchocerca (Nematoda: Onchocercidae) in blackflies (Simulium spp.) from southern California, USA.
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Verocai GG, Nelson KJ, Callahan RT, Wekesa JW, Hassan HK, and Hoberg EP
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- Animals, Biodiversity, California epidemiology, DNA, Mitochondrial genetics, Deer parasitology, Disease Vectors, Electron Transport Complex IV genetics, Female, Insect Vectors parasitology, NADH Dehydrogenase genetics, Onchocerca isolation & purification, Onchocerciasis transmission, Phylogeny, Polymerase Chain Reaction, Onchocerca classification, Onchocerca genetics, Onchocerciasis epidemiology, Simuliidae parasitology
- Abstract
Background: Entomological surveillance for pathogens based on molecular screening of putative arthropod vectors such as blackflies (Diptera: Simuliidae) is becoming increasingly important. Surveillance provides a means to understand host and geographical patterns of underestimated biodiversity among North American species of Onchocerca and a pathway to identify and track expanding emergence of the zoonotic Onchocerca lupi. Herein, we have screened two blackfly species, Simulium tescorum and Simulium vittatum (s.l.), from Los Angeles County, southern California, USA for DNA of filarioid nematodes to better understand species richness and limits within the genus Onchocerca., Methods: A total of 1056 and 378 female blackflies was collected using CO
2 -baited mosquito traps from March to November of 2015 and 2016, respectively. All blackflies during 2015 were individually processed for DNA extraction and PCR targeting of the cytochrome c oxidase subunit 1 (cox1) of the mitochondrial DNA (mtDNA). Specimens of S. tescorum collected in 2016 were processed individually with heads and bodies extracted separately, whereas those of S. vittatum (s.l.) were processed in pooled samples with heads and bodies extracted separately. A subset of filarioid-positive samples from 2015 and all samples from 2016 were screened using a PCR targeting the NADH dehydrogenase subunit 5 (nad5) gene (mtDNA)., Results: In 2015, 356 S. tescorum (33.7%) and 683 S. vittatum (s.l.) (64.7%) were collected, and an additional 17 specimens were not assessed morphologically. In 2016, a total of 378 blackflies was collected. Of these, 43 (11.6%) were S. tescorum and 327 (88.4%) were S. vittatum (s.l.), and an additional 8 specimens were not assessed morphologically. In 2015, Onchocerca sequences were detected in 4.8% (n = 17) of S. tescorum samples, and only one S. vittatum (0.15%). In 2016, only a single S. vittatum pool was positive for the same cryptic Onchocerca species. In phylogenetic comparisons based on nad5, the Onchocerca sequences from California formed a clade with those isolates in white-tailed deer from upstate New York, suggesting these belong to a single widespread cryptic species., Conclusions: An uncharacterized species of Onchocerca associated with cervid hosts was found in blackflies from southern California. Sequence data demonstrated it is likely conspecific with an unnamed species of Onchocerca previously found in white-tailed deer from upstate New York. Current data support recognition of a broad geographical distribution across North America for an apparently cryptic species of Onchocerca that is discrete from O. cervipedis, considered to be a typical filarioid among cervids. Our data suggest that this cryptic species of Onchocerca may infect subspecies of white-tailed deer (Odocoileus virginianus), and mule and black-tailed deer (Odocoileus hemionus) at temporal latitudes. The blackflies Simulium tescorum and S. vittatum (s.l.) (presumably, S. tribulatum) are putative vectors. Discovery of a cryptic complex indicates that species diversity and putative associations for definitive hosts and vectors of Onchocerca species in North America must be reassessed.- Published
- 2018
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27. Genetic characterisation and phylogenetic status of whipworms (Trichuris spp.) from captive non-human primates in China, determined by nuclear and mitochondrial sequencing.
- Author
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Xie Y, Zhao B, Hoberg EP, Li M, Zhou X, Gu X, Lai W, Peng X, and Yang G
- Subjects
- Animals, Biological Evolution, Cercopithecidae, China epidemiology, DNA, Helminth chemistry, DNA, Helminth genetics, DNA, Ribosomal Spacer chemistry, DNA, Ribosomal Spacer genetics, Electron Transport Complex IV genetics, Female, Host Specificity, Hylobates, Male, Phylogeny, Primates, Sequence Analysis, DNA veterinary, Trichuriasis epidemiology, Trichuriasis parasitology, Trichuris classification, Trichuris isolation & purification, Genetic Variation, Trichuriasis veterinary, Trichuris genetics
- Abstract
Background: Whipworms (Nematoda: Trichuridae), among the most common soil-transmitted helminths (STHs), can cause the socioeconomically important disease trichuriasis in various mammalian hosts including humans and non-human primates. For many years, Trichuris from non-human primates has been assigned to the same species as the one infecting humans Trichuris trichiura. More recently, several molecular reports challenged this assumption following recognition of a Trichuris species complex observed in humans and non-human primates. A refined concept for species limits within Trichuris contributes to an understanding of diversity and the potential (zoonotic) transmission among humans and non-human primates. In this study, we expanded previous investigations by exploring the diversity of Trichuris among eight primates including three Asian autochthonous species (i.e. Rhinopithecus roxellana, Rhinopithecus bieti and Nomascus leucogenys). Species-level identification, whether novel or assignable to known lineages of Trichuris, was based on analyses of nuclear internal transcribed spacers (ITS) and mitochondrial cytochrome c oxidase subunit 1 (cox1) genes., Results: In total, seven genetically distinct subgroups of whipworms were determined to be present among the primates sampled. Most Trichuris lineages, including Subgroups 1, 1', 3, 5 and 6, showed a broad host range and were not restricted to particular primate species; in addition to T. trichiura, a complex of Trichuris species was shown infecting primates. Furthermore, it was assumed that Trichuris spp. from either N. leucogenys and P. hamadryas or R. roxellana and R. bieti, respectively, were conspecific. Each pair was indicated to be a discrete lineage of Trichuris, designated, respectively, as Subgroups 1 or 1' and 2, based on integrated genetic and phylogenetic evidence., Conclusion: These results emphasise that the taxonomy and genetic variations of Trichuris are more complicated than previously acknowledged. These cumulative molecular and phylogenetic data provide a better understanding of the taxonomy, genetics and evolutionary biology of the whipworms.
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- 2018
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28. Transuterine infection by Baylisascaris transfuga : Neurological migration and fatal debilitation in sibling moose calves ( Alces alces gigas ) from Alaska.
- Author
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Hoberg EP, Burek-Huntington K, Beckmen K, Camp LE, and Nadler SA
- Abstract
Larval Baylisascaris nematodes (L3), resulting from transuterine infection and neural migration, were discovered in the cerebrum of sibling moose calves ( Alces alces gigas ) near 1-3 days in age from Alaska. We provide the first definitive identification, linking morphology, biogeography, and molecular phylogenetics, of Baylisascaris transfuga in naturally infected ungulates. Life history and involvement of paratenic hosts across a broader assemblage of mammals, from rodents to ungulates, in the transmission of B. transfuga remains undefined. Neural infections, debilitating young moose, may seasonally predispose calves to predation by brown bears, facilitating transmission to definitive hosts. Discovery of fatal neurological infections by L3 of B. transfuga in mammalian hosts serves to demonstrate the potential for zoonotic infection, as widely established for B. procyonis, in other regions and where raccoon definitive hosts are abundant. In zones of sympatry for multi-species assemblages of Baylisascaris across the Holarctic region presumptive identification of B. procyonis in cases of neurological larval migrans must be considered with caution. Diagnostics in neural and somatic larval migrans involving species of Baylisascaris in mammalian and other vertebrate hosts should include molecular-based and authoritative identification established in a phylogenetic context.
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- 2018
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29. Varestrongylus (Nematoda: Protostrongylidae), lungworms of ungulates: a phylogenetic framework based on comparative morphology.
- Author
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Verocai GG, Kutz SJ, and Hoberg EP
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- Animals, Male, Metastrongyloidea isolation & purification, North America epidemiology, Phylogeny, Strongylida Infections parasitology, Animals, Domestic parasitology, Deer parasitology, Metastrongyloidea classification, Strongylida Infections epidemiology, Strongylida Infections veterinary
- Abstract
Varestrongylus Bhalerao, 1932 comprises ten valid lungworm species infecting wild and domestic ungulates from Eurasia and North America. Here, we present a phylogenetic hypothesis for the genus based on morphological characters in a broader context for the family Protostrongylidae and discuss species relationships and aspects of character evolution. Phylogenetic analysis of 25 structural attributes, including binary and multistate characters, among the 10 species of Varestrongylus resulted in one fully resolved most parsimonious tree (61 steps; consistency index = 0.672, retention index = 0.722, and consistency index excluding uninformative characters = 0.667). Varestrongylus forms a monophyletic clade and is the sister of Pneumostrongylus, supporting recognition of the subfamily Varestrongylinae. Monophyly for Varestrongylus is diagnosed by six unequivocal synapomorphies, all associated with structural characters of the copulatory system of males. Varestrongylus pneumonicus is basal, and sister to all other species within the genus, which form two subclades. The subclade I contains V. sagittatus + V. tuvae and V. qinghaiensis + V. longispiculatus. Subclade II contains V. alpenae, V. capricola, V. capreoli, and V. eleguneniensis + V. alces. Both subclades are diagnosed by two unambiguous synapomorphies. Highlighted is the continuing importance of phylogenetic assessments based on comparative morphology as a foundation to explore the structure of the biosphere across space and time.
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- 2018
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30. Historical biogeography among species of Varestrongylus lungworms (Nematoda: Protostrongylidae) in ungulates: episodic expansion and host colonization linking Eurasia and North America.
- Author
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Verocai GG, Kutz SJ, and Hoberg EP
- Subjects
- Animals, Climate, Ecosystem, Geography, North America epidemiology, Phylogeny, Strongylida Infections parasitology, Deer parasitology, Goats parasitology, Metastrongyloidea classification, Metastrongyloidea isolation & purification, Strongylida Infections epidemiology, Strongylida Infections veterinary
- Abstract
Varestrongylus lungworms (Nematoda: Protostrongylidae) include 10 nominal species that parasitize wild and domesticated artiodactyles. Eight species are endemic to the western Palearctic and Eurasia, whereas two are limited in distribution to the Nearctic. Complex host associations, primarily among Cervidae and Bovidae (Caprinae), and biogeography were explored based on direct comparisons of parasite and host phylogenies to reveal the historical development of this fauna. Diversification among Varestrongylus species has an intricate history extending over the Pliocene and Quaternary involving episodic processes for geographic and host colonization: (1) Varestrongylus has origins in Eurasia with independent expansion events into bordering ecozones; (2) cervids are ancestral hosts; (3) the caprine-associated V. pneumonicus is basal and a result of an independent host colonization event; (4) secondary diversification, linked to sequential and independent host colonization events, occurred within cervids (V. sagittatus + V. tuvae; V. alpenae; and V. capreoli, V. alces + V. eleguneniensis); (5) at least two additional host colonization events into caprines occurred, followed or not by diversification (V. qinghaiensis + V. longispiculatus; V. capricola, respectively); (6) two independent events of geographic expansion into North America from Eurasia with cervids in the late Pliocene and early Pleistocene are postulated (V. alpenae, V. eleguneniensis). Comparisons based on phylogenetic hypotheses derived from comparative morphology and molecular inference for these nematodes are consistent with the postulated history for coevolutionary and biogeographic history. Episodes of geographic and host colonization, often in relation to rapid shifts in climate and habitat perturbation, have dominated the history of diversification of Varestrongylus.
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- 2018
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31. Diversity of gastrointestinal helminths in Dall's sheep and the negative association of the abomasal nematode, Marshallagia marshalli, with fitness indicators.
- Author
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Aleuy OA, Ruckstuhl K, Hoberg EP, Veitch A, Simmons N, and Kutz SJ
- Subjects
- Animals, Canada epidemiology, Prevalence, Sheep parasitology, Sheep Diseases epidemiology, Sheep Diseases parasitology, Trichostrongyloidea, Trichostrongyloidiasis epidemiology, Trichostrongyloidiasis parasitology
- Abstract
Gastrointestinal helminths can have a detrimental effect on the fitness of wild ungulates. Arctic and Subarctic ecosystems are ideal for the study of host-parasite interactions due to the comparatively simple ecological interactions and limited confounding factors. We used a unique dataset assembled in the early seventies to study the diversity of gastrointestinal helminths and their effect on fitness indicators of Dall's sheep, Ovis dalli dalli, in the Mackenzie Mountains, Northwest Territories, Canada. Parasite diversity included nine species, among which the abomasal nematode Marshallagia marshalli occurred with the highest prevalence and infection intensity. The intensity of M. marshalli increased with age and was negatively associated with body condition and pregnancy status in Dall's sheep across all the analyses performed. The intensity of the intestinal whipworm, Trichuris schumakovitschi, decreased with age. No other parasites were significantly associated with age, body condition, or pregnancy. Our study suggests that M. marshalli might negatively influence fitness of adult female Dall's sheep.
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- 2018
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32. A new worm infiltrating the human cornea: A report of three cases.
- Author
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McBurney-Lin S, Khorram D, Gee S, Hoberg EP, Klassen-Fischer MK, and Neafie RC
- Abstract
Purpose: To characterize a new species of parasitic nematode that triggers uveitis., Observations: Three previously healthy, relatively young people each contracted a corneal stromal nematode that, upon surgical removal and examination, did not match any known nematodes. Clinical ocular findings included corneal opacification, visible corneal worms, conjunctival injection, and uveitis., Conclusions and Importance: The three cases presented here represent a previously undescribed parasitic infection of the cornea by an unidentified nematode. These findings may represent a previously unrecognized zoonotic infection from wildlife sources and potentially a newly documented nematode requiring description. Future clinical findings regarding this newly described nematode are needed to further develop our understanding of the disease.
- Published
- 2018
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33. Embracing Colonizations: A New Paradigm for Species Association Dynamics.
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Nylin S, Agosta S, Bensch S, Boeger WA, Braga MP, Brooks DR, Forister ML, Hambäck PA, Hoberg EP, Nyman T, Schäpers A, Stigall AL, Wheat CW, Österling M, and Janz N
- Subjects
- Animals, Insecta parasitology, Insecta physiology, Parasitology, Plants parasitology, Species Specificity, Host-Parasite Interactions, Invertebrates parasitology, Invertebrates physiology, Vertebrates parasitology, Vertebrates physiology
- Abstract
Parasite-host and insect-plant research have divergent traditions despite the fact that most phytophagous insects live parasitically on their host plants. In parasitology it is a traditional assumption that parasites are typically highly specialized; cospeciation between parasites and hosts is a frequently expressed default expectation. Insect-plant theory has been more concerned with host shifts than with cospeciation, and more with hierarchies among hosts than with extreme specialization. We suggest that the divergent assumptions in the respective fields have hidden a fundamental similarity with an important role for potential as well as actual hosts, and hence for host colonizations via ecological fitting. A common research program is proposed which better prepares us for the challenges from introduced species and global change., (Copyright © 2017 Elsevier Ltd. All rights reserved.)
- Published
- 2018
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34. Specific status of Echinococcus canadensis (Cestoda: Taeniidae) inferred from nuclear and mitochondrial gene sequences.
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Yanagida T, Lavikainen A, Hoberg EP, Konyaev S, Ito A, Sato MO, Zaikov VA, Beckmen K, and Nakao M
- Subjects
- Alleles, Animals, Base Sequence, Cell Nucleus enzymology, Cell Nucleus genetics, DNA Polymerase III genetics, DNA, Helminth chemistry, DNA, Mitochondrial chemistry, Echinococcus classification, Echinococcus enzymology, Electron Transport Complex IV genetics, Genetic Markers genetics, Haplotypes, Humans, Phylogeny, Polymorphism, Genetic, Retrospective Studies, Sequence Alignment, DNA, Helminth genetics, DNA, Mitochondrial genetics, Echinococcus genetics
- Abstract
The specific status of Echinococcus canadensis has long been controversial, mainly because it consists of the mitochondrial lineages G6, G7, G8 and G10 with different host affinity: G6 (camel strain) and G7 (pig strain) with domestic cycles and G8 (cervid strain) and G10 (Fennoscandian cervid strain) with sylvatic or semi-domestic cycles. There is an argument whether the mitochondrial lineages should be recognised as separate species which correspond to the biological or epidemiological aggregation. In the present study, the specific status of E. canadensis was investigated using mitochondrial DNA and single copy nuclear DNA markers. Nucleotide sequences of complete mitochondrial cytochrome c oxidase subunit 1 (cox1) and partial nuclear phosphoenolpyruvate carboxykinase (pepck) and DNA polymerase delta (pold) were determined for 48 isolates of E. canadensis collected from different hosts in a wide range of regions. The mitochondrial phylogeny of cox1 showed that all the isolates were clearly divided into three clades corresponding to G6/G7, G8 and G10. Five and three alleles were confirmed at pepck and pold loci, respectively. These alleles were generally divided into two groups corresponding to G6/G7 or G8 and G10. However, allele sharing was confirmed among individuals belonging to different lineages. The allele sharing occurred primarily in regions where different mitochondrial DNA lineages were found in sympatry. The resultant nuclear mitochondrial discordance suggests the genetic exchangeability among E. canadensis isolates belonging to different lineages. An apparently mosaic parasite fauna that reflects faunal mixing due to natural and anthropogenic disturbance, including introductions and invasion, precludes us from designating each of G6/G7, G8 and G10 into a different species., (Copyright © 2017 Australian Society for Parasitology. All rights reserved.)
- Published
- 2017
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35. Arctic systems in the Quaternary: ecological collision, faunal mosaics and the consequences of a wobbling climate.
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Hoberg EP, Cook JA, Agosta SJ, Boeger W, Galbreath KE, Laaksonen S, Kutz SJ, and Brooks DR
- Subjects
- Arctic Regions, Spatio-Temporal Analysis, Biodiversity, Climate, Ecosystem
- Abstract
Climate oscillations and episodic processes interact with evolution, ecology and biogeography to determine the structure and complex mosaic that is the biosphere. Parasites and parasite-host assemblages are key components in a general explanatory paradigm for global biodiversity. We explore faunal assembly in the context of Quaternary time frames of the past 2.6 million years, a period dominated by episodic shifts in climate. Climate drivers cross a continuum from geological to contemporary timescales and serve to determine the structure and distribution of complex biotas. Cycles within cycles are apparent, with drivers that are layered, multifactorial and complex. These cycles influence the dynamics and duration of shifts in environmental structure on varying temporal and spatial scales. An understanding of the dynamics of high-latitude systems, the history of the Beringian nexus (the intermittent land connection linking Eurasia and North America) and downstream patterns of diversity depend on teasing apart the complexity of biotic assembly and persistence. Although climate oscillations have dominated the Quaternary, contemporary dynamics are driven by tipping points and shifting balances emerging from anthropogenic forces that are disrupting ecological structure. Climate change driven by anthropogenic forcing has supplanted a history of episodic variation and is eliminating ecological barriers and constraints on development and distribution for pathogen transmission. A framework to explore interactions of episodic processes on faunal structure and assembly is the Stockholm Paradigm, which appropriately shifts the focus from cospeciation to complexity and contingency in explanations of diversity.
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- 2017
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36. Ancylostoma ailuropodae n. sp. (Nematoda: Ancylostomatidae), a new hookworm parasite isolated from wild giant pandas in Southwest China.
- Author
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Xie Y, Hoberg EP, Yang Z, Urban JF Jr, and Yang G
- Subjects
- Ancylostoma anatomy & histology, Ancylostoma genetics, Ancylostomiasis parasitology, Ancylostomiasis veterinary, Animals, Base Sequence, China, DNA, Helminth genetics, DNA, Mitochondrial genetics, Female, Male, Phylogeny, Sequence Alignment, Sequence Analysis, DNA, Ancylostoma classification, Ancylostoma isolation & purification, Ursidae parasitology
- Abstract
Background: Hookworms belonging to the genus Ancylostoma (Dubini, 1843) cause ancylostomiasis, a disease of considerable concern in humans and domestic and wild animals. Molecular and epidemiological data support evidence for the zoonotic potential among species of Ancylostoma where transmission to humans is facilitated by rapid urbanization and increased human-wildlife interactions. It is important to assess and describe these potential zoonotic parasite species in wildlife, especially in hosts that have physiological similarities to humans and share their habitat. Moreover, defining species diversity within parasite groups that can circulate among free-ranging host species and humans also provides a pathway to understanding the distribution of infection and disease. In this study, we describe a previously unrecognized species of hookworm in the genus Ancylostoma in the giant panda, including criteria for morphological and molecular characterization., Methods: The hookworm specimens were obtained from a wild giant panda that died in the Fengtongzai Natural Reserve in Sichuan Province of China in November 2013. They were microscopically examined and then genetically analyzed by sequencing the nuclear internal transcribed spacer (ITS, ITS1-5.8S-ITS2) and mitochondrial cytochrome c oxidase subunit 1 (cox1) genes in two representative specimens (one female and one male, FTZ1 and FTZ2, respectively)., Results: Ancylostoma ailuropodae n. sp. is proposed for these hookworms. Morphologically the hookworm specimens differ from other congeneric species primarily based on the structure of the buccal capsule in males and females, characterized by 2 pairs of ventrolateral and 2 pairs of dorsolateral teeth; males differ in the structure and shape of the copulatory bursa, where the dorsal ray possesses 2 digitations. Pairwise nuclear and mitochondrial DNA comparisons, genetic distance analysis, and phylogenetic data strongly indicate that A. ailuropodae from giant pandas is a separate species which shared a most recent common ancestor with A. ceylanicum Looss, 1911 in the genus Ancylostoma (family Ancylostomatidae)., Conclusion: Ancylostoma ailuropodae n. sp. is the fourth species of hookworm described from the Ursidae and the fifteenth species assigned to the genus Ancylostoma. A sister-species association with A. ceylanicum and phylogenetic distinctiveness from the monophyletic Uncinaria Frölich, 1789 among ursids and other carnivorans indicate a history of host colonization in the evolutionary radiation among ancylostomatid hookworms. Further, phylogenetic relationships among bears and a history of ecological and geographical isolation for giant pandas may be consistent with two independent events of host colonization in the diversification of Ancylostoma among ursid hosts. A history for host colonization within this assemblage and the relationship for A. ailuropodae n. sp. demonstrate the potential of this species as a zoonotic parasite and as a possible threat to human health. The cumulative morphological, molecular and phylogenetic data presented for A. ailuropodae n. sp. provides a better understanding of the taxonomy, diagnostics and evolutionary biology of the hookworms.
- Published
- 2017
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37. A comparison of two methods for quantifying parasitic nematode fecundity.
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Austin LV, Budischak SA, Ramadhin J, Hoberg EP, Abrams A, Jolles AE, and Ezenwa VO
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- Animals, Female, Fertility, Nematode Infections epidemiology, Nematode Infections parasitology, Ovum cytology, South Africa epidemiology, Buffaloes parasitology, Feces parasitology, Nematoda isolation & purification, Nematode Infections veterinary, Parasite Egg Count methods
- Abstract
Accurate measures of nematode fecundity can provide important information for investigating parasite life history evolution, transmission potential, and effects on host health. Understanding differences among fecundity assessment protocols and standardizing methods, where possible, will enable comparisons across different studies and host and parasite species and systems. Using the trichostrongyle nematode Cooperia fuelleborni isolated from wild African buffalo (Syncerus caffer), we compared egg recovery and enumeration between two methods for measuring the fecundity of female worms. The first method, in utero egg count, involves visual enumeration of the eggs via microscopic inspection of the uterine system. The second method, ex utero egg count, involves dissolving the same specimens from above in a sodium chloride solution to release the eggs from the female's uterus, then enumeration under an inverted microscope. On average, the ex utero method resulted in 34% more eggs than the in utero method. However, results indicate that the two methods used to quantify parasitic nematode fecundity are highly correlated. Thus, while both methods are viable options for estimating relative nematode fecundity, we recommend caution in undertaking comparative studies that utilize egg count data collected using different methods.
- Published
- 2017
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38. Insights on the host associations and geographic distribution of Hymenolepis folkertsi (Cestoda: Hymenolepididae) among rodents across temperate latitudes of North America.
- Author
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Hoberg EP, Makarikov AA, Tkach VV, Meagher S, Nims TN, Eckerlin RP, and Galbreath KE
- Subjects
- Animal Distribution, Animals, Base Sequence, Biodiversity, Biological Evolution, Climate, Geography, Host Specificity, Hymenolepiasis parasitology, Hymenolepis genetics, Hymenolepis physiology, Mice, North America, Hymenolepiasis veterinary, Hymenolepis isolation & purification, Peromyscus parasitology, Rodent Diseases parasitology, Sciuridae parasitology
- Abstract
Synoptic data and an understanding of helminth parasite diversity among diverse rodent assemblages across temperate latitudes of North America remain remarkably incomplete. Renewed attention to comprehensive survey and inventory to establish the structure of biodiverse faunas is essential in providing indicators and proxies for identifying the outcomes of accelerating change linked to climate warming and anthropogenic forcing. Subsequent to the description of Hymenolepis folkertsi in the oldfield mouse, Peromyscus polionotus, additional specimens of hymenolepidids were collected or discovered in archived museum repositories from multiple species of deer mice (Peromyscus maniculatus, Peromyscus leucopus), the golden mouse (Ochrotomys nuttalli), chipmunks (Tamias striatus, Tamias amoenus), the 13-lined ground squirrel (Ictidomys tridecemlineatus), and tree squirrels (Sciurus carolinensis, Sciurus niger) from disjunct localities in the USA spanning southern Georgia, Virginia, Pennsylvania, Connecticut, the Upper Peninsula of Michigan, Wisconsin, and central Idaho. Specimens were largely consistent morphologically with the original description of H. folkertsi. Initial DNA sequence data, from a portion of the mitochondrial NADH dehydrogenase subunit 1, demonstrated intraspecific variation among three apparently geographically isolated populations attributed to H. folkertsi (uncorrected genetic distances of 2.7 % (Idaho and Michigan), 2.4 % (Virginia + Pennsylvania and Michigan), and 1.89 % (VA + PA and ID). Geography rather than host association explains the distribution and occurrence of H. folkertsi, and host colonization among deer mice, chipmunks, and other sciurids within regional sites is indicated. Genetic divergence revealed across localities for H. folkertsi suggests historically isolated populations, consistent with extended evolutionary and biogeographic trajectories among hymenolepidids and species of Peromyscus and Tamias in North America. Field inventory, that revealed these parasite populations, substantially alters our understanding of the distribution of diversity and provides insights about the nature of the complex relationships that serve to determine cestode faunas in rodents.
- Published
- 2016
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39. Temporal and spatial mosaics: deep host association and shallow geographic drivers shape genetic structure in a widespread pinworm, Rauschtineria eutamii .
- Author
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Bell KC, Calhoun KL, Hoberg EP, Demboski JR, and Cook JA
- Abstract
Climate and host demographic cycling often shape both parasite genetic diversity and host distributions, processes that transcend a history of strict host-parasite association. We explored host associations and histories based on an evaluation of mitochondrial and nuclear sequences to reveal the underlying history and genetic structure of a pinworm, Rauschtineria eutamii , infecting 10 species of western North American chipmunks (Rodentia: Tamias , subgenus Neotamias ). Rauschtineria eutamii contains divergent lineages influenced by the diversity of hosts and variation across the complex topography of western North America. We recovered six reciprocally monophyletic R. eutamii mitochondrial clades, largely supported by nuclear gene trees, exhibiting divergence levels comparable to intraspecific variation reported for other nematodes. Phylogenetic relationships among pinworm clades suggest that R. eutamii colonized an ancestral lineage of western chipmunks and lineages persisted during historical isolation in diverging Neotamias species or species groups. Pinworm diversification, however, is incongruent and asynchronous relative to host diversification. Secondarily, patterns of shallow divergence were shaped by geography through events of episodic colonization reflecting an interaction of taxon pulses and ecological fitting among assemblages in recurrent sympatry. Pinworms occasionally infect geographically proximal host species; however, host switching may be unstable or ephemeral, as there is no signal of host switching in the deeper history of R. eutamii .
- Published
- 2016
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40. Target gene enrichment in the cyclophyllidean cestodes, the most diverse group of tapeworms.
- Author
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Yuan H, Jiang J, Jiménez FA, Hoberg EP, Cook JA, Galbreath KE, and Li C
- Subjects
- Animals, DNA chemistry, DNA genetics, Evolution, Molecular, High-Throughput Nucleotide Sequencing, Oligonucleotide Probes genetics, Phylogeny, Polymerase Chain Reaction, Transcriptome, Cestoda classification, Cestoda genetics, DNA isolation & purification, Exons, Genotyping Techniques methods, Nucleic Acid Hybridization methods, Specimen Handling methods
- Abstract
The Cyclophyllidea is the most diverse order of tapeworms, encompassing species that infect all classes of terrestrial tetrapods including humans and domesticated animals. Available phylogenetic reconstructions based either on morphology or molecular data lack the resolution to allow scientists to either propose a solid taxonomy or infer evolutionary associations. Molecular markers available for the Cyclophyllidea mostly include ribosomal DNA and mitochondrial loci. In this study, we identified 3641 single-copy nuclear coding loci by comparing the genomes of Hymenolepis microstoma, Echinococcus granulosus and Taenia solium. We designed RNA baits based on the sequence of H. microstoma, and applied target enrichment and Illumina sequencing to test the utility of those baits to recover loci useful for phylogenetic analyses. We captured DNA from five species of tapeworms representing two families of cyclophyllideans. We obtained an average of 3284 (90%) of the targets from the test samples and then used captured sequences (2 181 361 bp in total; fragment size ranging from 301 to 6969 bp) to reconstruct a phylogeny for the five test species plus the three species for which genomic data are available. The results were consistent with the current consensus regarding cyclophyllidean relationships. To assess the potential for our method to yield informative genetic variation at intraspecific scales, we extracted 14 074 single nucleotide polymorphisms (SNPs) from alignments of four Arostrilepis macrocirrosa and two A. cooki and successfully inferred their relationships. The results showed that our target gene tools yield data sets that provide robust inferences at a range of taxonomic scales in the Cyclophyllidea., (© 2016 John Wiley & Sons Ltd.)
- Published
- 2016
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41. Experimental insight into the process of parasite community assembly.
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Budischak SA, Hoberg EP, Abrams A, Jolles AE, and Ezenwa VO
- Subjects
- Animals, Antinematodal Agents administration & dosage, Fenbendazole administration & dosage, Gastrointestinal Diseases drug therapy, Gastrointestinal Diseases parasitology, Gastrointestinal Diseases veterinary, Nematode Infections drug therapy, Nematode Infections parasitology, Nematode Infections veterinary, Population Dynamics, Random Allocation, South Africa, Stochastic Processes, Biota, Buffaloes parasitology, Host-Parasite Interactions, Nematoda physiology
- Abstract
Community assembly is a fundamental process that has long been a central focus in ecology. Extending community assembly theory to communities of co-infecting parasites, we used a gastrointestinal nematode removal experiment in free-ranging African buffalo to examine the community assembly patterns and processes. We first asked whether reassembled communities differ from undisturbed communities by comparing anthelmintic-treated and control hosts. Next, we examined the temporal dynamics of assembly using a cross-section of communities that reassembled for different periods of time since last experimental removal. Next, we tested for evidence of assembly processes that might drive such reassembly patterns: environmental filtering based on host traits (i.e. habitat patches), interspecific interactions, priority effects and chance dispersal from the environmental pool of infective stages (i.e. the regional species pool). On average, reassembled parasite communities had lower abundance, but were more diverse and even, and these patterns varied tightly with reassembly time. Over time, the communities within treated hosts progressively resembled controls as diversity and evenness decreased, while total abundance increased. Notably, experimental removal allowed us to attribute observed differences in abundance, diversity and evenness to the process of community assembly. During early reassembly, parasite accumulation was biased towards a subordinate species and, by excluding stochastic assembly processes (i.e. chance dispersal and priority effects), we were able to determine that early assembly is deterministic. Later in the reassembly process, we established that host traits, as well as stochastic dispersal from the environmental pool of infective stages, can affect the community composition. Overall, our results suggest that there is a high degree of resiliency and environmental dependence to the worm communities of buffalo. More generally, our data show that both deterministic and stochastic processes may play a role in the assembly of parasite communities of wild hosts, but their relative importance may vary temporally. Consequently, the best strategy for managing reassembling parasite communities may also need to shift over time., (© 2016 The Authors. Journal of Animal Ecology © 2016 British Ecological Society.)
- Published
- 2016
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42. Broadening diversity in the Arostrilepis horrida complex: Arostrilepis kontrimavichusi n. sp. (Cyclophyllidea: Hymenolepididae) in the western red-backed vole Myodes californicus (Merriam) (Cricetidae: Arvicolinae) from temperate latitudes of the Pacific Northwest, North America.
- Author
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Makarikov AA and Hoberg EP
- Subjects
- Animals, Arvicolinae anatomy & histology, Biodiversity, Host Specificity, Northwestern United States, Species Specificity, Arvicolinae parasitology, Cestoda classification
- Abstract
Specimens originally identified provisionally as Hymenolepis horrida (Linstow, 1901) [later Arostrilepis horrida (Linstow, 1901)] in Myodes californicus (Merriam) from near the Pacific coastal zone of southern Oregon are revised. Specimens in western red-backed voles represent an undescribed species of Arostrilepis Mas Coma & Tenora, 1997, contributing to recognition and resolution of a broadening complex encompassing cryptic diversity for these hymenolepidid tapeworms distributed across the Holarctic region. Consistent with recent studies defining diversity in the genus, the form, dimensions, and spination (pattern, shape and size) of the cirrus are diagnostic. Among 12 nominal congeners, specimens of A. kontrimavichusi n. sp. are further distinguished by the relative position and length of the cirrus-sac, arrangement of the testes and relative size of the external seminal vesicle and seminal receptacle. Specimens from Oregon voles represent the fifth endemic hymenolepidid in this genus from the Nearctic. Host range for the North American assemblage of species includes Cricetidae (Arvicolinae and Neotominae), Heteromyidae, Geomyidae, and rarely Sciuridae.
- Published
- 2016
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43. Definitive Hosts of Versteria Tapeworms (Cestoda: Taeniidae) Causing Fatal Infection in North America.
- Author
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Lee LM, Wallace RS, Clyde VL, Gendron-Fitzpatrick A, Sibley SD, Stuchin M, Lauck M, O'Connor DH, Nakao M, Lavikainen A, Hoberg EP, and Goldberg TL
- Subjects
- Animals, Animals, Zoo, Asia epidemiology, Cestoda classification, Cestoda isolation & purification, Cestode Infections epidemiology, Cestode Infections parasitology, Cestode Infections transmission, Electron Transport Complex IV genetics, Europe epidemiology, Female, Helminth Proteins genetics, Host-Parasite Interactions, Male, North America epidemiology, Phylogeography, Cestoda genetics, Cestode Infections veterinary, Disease Reservoirs parasitology, Mustelidae parasitology, Phylogeny, Pongo pygmaeus parasitology
- Abstract
We previously reported fatal infection of a captive Bornean orangutan with metacestodes of a novel taeniid tapeworm, Versteria sp. New data implicate mustelids as definitive hosts of these tapeworms in North America. At least 2 parasite genetic lineages circulate in North America, representing separate introductions from Eurasia.
- Published
- 2016
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44. Phylogenomic and biogeographic reconstruction of the Trichinella complex.
- Author
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Korhonen PK, Pozio E, La Rosa G, Chang BC, Koehler AV, Hoberg EP, Boag PR, Tan P, Jex AR, Hofmann A, Sternberg PW, Young ND, and Gasser RB
- Subjects
- Animals, Gene Expression Regulation physiology, Genome, Helminth, Genotype, Genomics, Phylogeny, Trichinella genetics
- Abstract
Trichinellosis is a globally important food-borne parasitic disease of humans caused by roundworms of the Trichinella complex. Extensive biological diversity is reflected in substantial ecological and genetic variability within and among Trichinella taxa, and major controversy surrounds the systematics of this complex. Here we report the sequencing and assembly of 16 draft genomes representing all 12 recognized Trichinella species and genotypes, define protein-coding gene sets and assess genetic differences among these taxa. Using thousands of shared single-copy orthologous gene sequences, we fully reconstruct, for the first time, a phylogeny and biogeography for the Trichinella complex, and show that encapsulated and non-encapsulated Trichinella taxa diverged from their most recent common ancestor ∼21 million years ago (mya), with taxon diversifications commencing ∼10-7 mya.
- Published
- 2016
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45. The Identification of Haemonchus Species and Diagnosis of Haemonchosis.
- Author
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Zarlenga DS, Hoberg EP, and Tuo W
- Subjects
- Animals, Goat Diseases diagnosis, Goats, Haemonchiasis diagnosis, Haemonchiasis parasitology, Haemonchus classification, Haemonchus genetics, Haemonchus immunology, Ruminants, Sheep, Sheep Diseases diagnosis, Sheep Diseases epidemiology, Goat Diseases parasitology, Haemonchiasis veterinary, Haemonchus isolation & purification, Sheep Diseases parasitology
- Abstract
Diagnosis is often equated with identification or detection when discussing parasitic diseases. Unfortunately, these are not necessarily mutually exclusive activities; diseases and infections are generally diagnosed and organisms are identified. Diagnosis is commonly predicated upon some clinical signs; in an effort to determine the causative agent, identification of genera and species is subsequently performed. Both identification and diagnosis play critical roles in managing an infection, and involve the interplay of direct and indirect methods of detection, particularly in light of the complex and expanding problem of drug-resistance in parasites. Accurate and authoritative identification that is cost- and time-effective, based on structural and molecular attributes of specimens, provides a foundation for defining parasite diversity and changing patterns of geographical distribution, host association and emergence of disease. Most techniques developed thus far have been grounded in assumptions based on strict host associations between Haemonchus contortus and small ruminants, that is, sheep and goats, and between Haemonchus placei and bovids. Current research and increasing empirical evidence of natural infections in the field demonstrates that this assumption misrepresents the host associations for these species of Haemonchus. Furthermore, the capacity of H. contortus to utilize a considerably broad spectrum of ungulate hosts is reflected in our understanding of the role of anthropogenic forcing, the 'breakdown' of ecological isolation, global introduction and host switching as determinants of distribution. Nuanced insights about distribution, host association and epidemiology have emerged over the past 30years, coincidently with the development of increasingly robust means for parasite identification. In this review and for the sake of argument, we would like to delineate the diagnosis of haemonchosis from the identification of the specific pathogen. As a foundation for exploring host and parasite biology, we will examine the evolution of methods for distinguishing H. contortus from other common gastrointestinal nematodes of agriculturally significant and free-ranging wild ruminants using morphological, molecular and/or immunological methods for studies at the species and genus levels., (Copyright © 2016 Elsevier Ltd. All rights reserved.)
- Published
- 2016
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46. Evolution and Biogeography of Haemonchus contortus: Linking Faunal Dynamics in Space and Time.
- Author
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Hoberg EP and Zarlenga DS
- Subjects
- Animal Distribution, Animals, Animals, Domestic parasitology, Biodiversity, Climate, Ecosystem, Haemonchus classification, Host Specificity, Humans, Phylogeography, Time Factors, Biological Evolution, Haemonchus physiology, Host-Parasite Interactions
- Abstract
History is the foundation that informs about the nuances of faunal assembly that are essential in understanding the dynamic nature of the host-parasite interface. All of our knowledge begins and ends with evolution, ecology and biogeography, as these interacting facets determine the history of biodiverse systems. These components, relating to Haemonchus, can inform about the complex history of geographical distribution, host association and the intricacies of host-parasite associations that are played out in physiological and behavioural processes that influence the potential for disease and our capacity for effective control in a rapidly changing world. Origins and evolutionary diversification among species of the genus Haemonchus and Haemonchus contortus occurred in a complex crucible defined by shifts in environmental structure emerging from cycles of climate change and ecological perturbation during the late Tertiary and through the Quaternary. A history of sequential host colonization associated with waves of dispersal bringing assemblages of ungulates from Eurasia into Africa and processes emerging from ecosystems in collision and faunal turnover defined the arena for radiation among 12 recognized species of Haemonchus. Among congeners, the host range for H. contortus is exceptionally broad, including species among artiodactyls of 40 genera representing 5 families (and within 12 tribes of Bovidae). Broad host range is dramatically reflected in the degree to which translocation, introduction and invasion with host switching, has characterized an expanding distribution over time in North America, South America, southern Eurasia, Australia and New Zealand, coincidental with agriculture, husbandry and global colonization by human populations driven particularly by European exploration after the 1500s. African origins in xeric to mesic habitats of the African savannah suggest that historical constraints linked to ecological adaptations (tolerances and developmental thresholds defined by temperature and humidity for larval stages) will be substantial determinants in the potential outcomes for widespread geographical and host colonization which are predicted to unfold over the coming century. Insights about deeper evolutionary events, ecology and biogeography are critical as understanding history informs us about the possible range of responses in complex systems under new regimes of environmental forcing, especially, in this case, ecological perturbation linked to climate change. A deeper history of perturbation is relevant in understanding contemporary systems that are now strongly structured by events of invasion and colonization. The relaxation of abiotic and biotic controls on the occurrence of H. contortus, coincidental with inception and dissemination of anthelmintic resistance may be synergistic, serving to exacerbate challenges to control parasites or to limit the socioeconomic impacts of infection that can influence food security and availability. Studies of haemonchine nematodes contribute directly to an expanding model about the nature of diversity and the evolutionary trajectories for faunal assembly among complex host-parasite systems across considerable spatial and temporal scales., (Copyright © 2016 Elsevier Ltd. All rights reserved.)
- Published
- 2016
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47. Climate Change in the North American Arctic: A One Health Perspective.
- Author
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Dudley JP, Hoberg EP, Jenkins EJ, and Parkinson AJ
- Subjects
- Animals, Animals, Wild, Arctic Regions epidemiology, Ecosystem, Environmental Monitoring, Humans, Indians, North American, North America epidemiology, Population Groups, Acute Disease epidemiology, Chronic Disease epidemiology, Climate Change, Environmental Pollution adverse effects, Foodborne Diseases epidemiology, Waterborne Diseases epidemiology, Zoonoses epidemiology
- Abstract
Climate change is expected to increase the prevalence of acute and chronic diseases among human and animal populations within the Arctic and subarctic latitudes of North America. Warmer temperatures are expected to increase disease risks from food-borne pathogens, water-borne diseases, and vector-borne zoonoses in human and animal populations of Arctic landscapes. Existing high levels of mercury and persistent organic pollutant chemicals circulating within terrestrial and aquatic ecosystems in Arctic latitudes are a major concern for the reproductive health of humans and other mammals, and climate warming will accelerate the mobilization and biological amplification of toxic environmental contaminants. The adverse health impacts of Arctic warming will be especially important for wildlife populations and indigenous peoples dependent upon subsistence food resources from wild plants and animals. Additional research is needed to identify and monitor changes in the prevalence of zoonotic pathogens in humans, domestic dogs, and wildlife species of critical subsistence, cultural, and economic importance to Arctic peoples. The long-term effects of climate warming in the Arctic cannot be adequately predicted or mitigated without a comprehensive understanding of the interactive and synergistic effects between environmental contaminants and pathogens in the health of wildlife and human communities in Arctic ecosystems. The complexity and magnitude of the documented impacts of climate change on Arctic ecosystems, and the intimacy of connections between their human and wildlife communities, makes this region an appropriate area for development of One Health approaches to identify and mitigate the effects of climate warming at the community, ecosystem, and landscape scales.
- Published
- 2015
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48. Understanding Host-Switching by Ecological Fitting.
- Author
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Araujo SB, Braga MP, Brooks DR, Agosta SJ, Hoberg EP, von Hartenthal FW, and Boeger WA
- Subjects
- Animals, Ecology, Host-Parasite Interactions
- Abstract
Despite the fact that parasites are highly specialized with respect to their hosts, empirical evidence demonstrates that host switching rather than co-speciation is the dominant factor influencing the diversification of host-parasite associations. Ecological fitting in sloppy fitness space has been proposed as a mechanism allowing ecological specialists to host-switch readily. That proposal is tested herein using an individual-based model of host switching. The model considers a parasite species exposed to multiple host resources. Through time host range expansion can occur readily without the prior evolution of novel genetic capacities. It also produces non-linear variation in the size of the fitness space. The capacity for host colonization is strongly influenced by propagule pressure early in the process and by the size of the fitness space later. The simulations suggest that co-adaptation may be initiated by the temporary loss of less fit phenotypes. Further, parasites can persist for extended periods in sub-optimal hosts, and thus may colonize distantly related hosts by a "stepping-stone" process.
- Published
- 2015
- Full Text
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49. A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts.
- Author
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Budischak SA, Hoberg EP, Abrams A, Jolles AE, and Ezenwa VO
- Subjects
- Animals, Animals, Wild, Helminthiasis diagnosis, Helminthiasis parasitology, Helminthiasis, Animal diagnosis, Intestinal Diseases, Parasitic diagnosis, Intestinal Diseases, Parasitic parasitology, Molecular Diagnostic Techniques methods, Molecular Sequence Data, Nematoda genetics, Nematode Infections diagnosis, Nematode Infections parasitology, Parasite Load, Selection Bias, Sequence Analysis, DNA, Specimen Handling, Buffaloes parasitology, DNA Barcoding, Taxonomic methods, Helminthiasis, Animal parasitology, Intestinal Diseases, Parasitic veterinary, Nematoda classification, Nematoda isolation & purification, Nematode Infections veterinary
- Abstract
Most hosts are concurrently or sequentially infected with multiple parasites; thus, fully understanding interactions between individual parasite species and their hosts depends on accurate characterization of the parasite community. For parasitic nematodes, noninvasive methods for obtaining quantitative, species-specific infection data in wildlife are often unreliable. Consequently, characterization of gastrointestinal nematode communities of wild hosts has largely relied on lethal sampling to isolate and enumerate adult worms directly from the tissues of dead hosts. The necessity of lethal sampling severely restricts the host species that can be studied, the adequacy of sample sizes to assess diversity, the geographic scope of collections and the research questions that can be addressed. Focusing on gastrointestinal nematodes of wild African buffalo, we evaluated whether accurate characterization of nematode communities could be made using a noninvasive technique that combined conventional parasitological approaches with molecular barcoding. To establish the reliability of this new method, we compared estimates of gastrointestinal nematode abundance, prevalence, richness and community composition derived from lethal sampling with estimates derived from our noninvasive approach. Our noninvasive technique accurately estimated total and species-specific worm abundances, as well as worm prevalence and community composition when compared to the lethal sampling method. Importantly, the rate of parasite species discovery was similar for both methods, and only a modest number of barcoded larvae (n = 10) were needed to capture key aspects of parasite community composition. Overall, this new noninvasive strategy offers numerous advantages over lethal sampling methods for studying nematode-host interactions in wildlife and can readily be applied to a range of study systems., (© 2015 John Wiley & Sons Ltd.)
- Published
- 2015
- Full Text
- View/download PDF
50. Morphological and morphometric differentiation of dorsal-spined first stage larvae of lungworms (Nematoda: Protostrongylidae) infecting muskoxen (Ovibos moschatus) in the central Canadian Arctic.
- Author
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Kafle P, Lejeune M, Verocai GG, Hoberg EP, and Kutz SJ
- Abstract
Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis are the two most common protostrongylid nematodes infecting muskoxen in the North American Arctic and Subarctic. First stage larvae (L1) of these lungworms have considerable morphological similarity that makes their differential diagnosis very difficult. Using light microscopy, we studied in detail the L1 of these two species and identified the key differences in morphological and morphometric attributes. Thirty L1 of each species from naturally infected muskox were heat-killed and then assessed for morphological and morphometric features that could be used for species-level differentiation. Key differentiating features include: length and morphology of the tail extension, curvature of the body, ventral post-anal transverse cuticular striations, and total body length. A laboratory guide for differentiation of L1 based on these species-specific characters was prepared and used by an experienced observer to identify an additional 35 L1 extracted from a different set of fecal samples from free-ranging muskoxen with mixed infections. The identities of these L1 were confirmed by sequence analysis of the ITS-2 region of the nuclear ribosomal DNA. Accuracy of morphological identification was 100 percent, reflecting the reliability of the proposed guide for differentiation. Using the guide, three minimally trained lab assistants each fixed and accurately identified 10 of 10 randomly selected L1. Ability to morphologically differentiate these facilitates the monitoring of overlapping range expansion of both parasites in the Canadian Arctic. Studies enabling species-level parasite identification are also critical for defining biodiversity, detecting mixed infections, and understanding host-parasite interactions. Morphological identification is a simple, reliable and cost-effective alternative to labor and equipment intensive molecular methods and can easily be performed in low resource settings.
- Published
- 2015
- Full Text
- View/download PDF
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