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Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche

Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour . The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche.

Nature

Ecology and management of plague in diverse communities of rodents and fleas

Plague originated in Asia as a flea-borne zoonosis of mammalian hosts. Today, the disease is distributed nearly worldwide. In western United States of America, plague is maintained, transmitted, and amplified in diverse communities of rodents and fleas. We examined flea diversity on three species of prairie dogs ( Cynomys spp., PDs) and six species of sympatric small rodents in Montana and Utah, United States of America. Among 2896 fleas, 19 species were identified; 13 were found on PDs and 9 were found on small rodents. In Montana, three flea species were found on PDs; the three species parasitize PDs and mice. In Utah, 12 flea species were found on PDs; the 12 species parasitize PDs, mice, voles, chipmunks, ground squirrels, rock squirrels, and marmots. Diverse flea communities and their willingness to parasitize many types of hosts, across multiple seasons and habitats, may favor plague maintenance and transmission. Flea parasitism on Peromyscus deer mice varied directly with elevation. Fleas are prone to desiccation, and might prosper at higher, mesic elevations; in addition, Peromyscus nest characteristics may vary with elevation. Effective management of plague is critical. Plague management is probably most effective when encompassing communities of rodents and fleas. Treatment of PD burrows with 0.05% deltamethrin dust, which suppressed fleas on PDs for >365 days, suppressed fleas on small rodents for at least 58 days. At one site, deltamethrin suppressed fleas on small rodents for at least 383 days. By simultaneously suppressing fleas on PDs and small rodents, deltamethrin should promote ecosystem resilience and One Health objectives.

Montana, Utah

Island history affects faunal composition: the treeshrews (Mammalia: Scandentia: Tupaiidae) from the Mentawai and Batu Islands, Indonesia

The Mentawai and Batu Island groups off the west coast of Sumatra have a complicated geological and biogeographical history. The Batu Islands have shared a connection with the Sumatran ‘mainland’ during periods of lowered sea level, whereas the Mentawai Islands, despite being a similar distance from Sumatra, have remained isolated from Sumatra, and probably from the Batu Islands as well. These contrasting historical relationships to Sumatra have influenced the compositions of the respective mammalian faunas of these island groups. Treeshrews (Scandentia, Tupaiidae) from these islands have, at various times in their history, been recognized as geographically circumscribed populations of a broadly distributed Tupaia glis, subspecies, or distinct species. We used multivariate analyses of measurements from the skull and hands to compare the island populations from Siberut (Mentawai Islands) and Tanahbala (Batu Islands) with the geographically adjacent species from the southern Mentawai Islands (T. chrysogaster) and Sumatra (T. ferruginea). Results from both the skull and manus of the Siberut population show that it is most similar to T. chrysogaster, whereas the Tanahbala population is more similar to T. ferruginea, confirming predictions based on island history. These results are further corroborated by mammae counts. Based on these lines of evidence, we include the Siberut population in T. chrysogaster and the Tanahbala population in T. ferruginea. Our conclusions expand the known distributions of both the Mentawai and Sumatran species. The larger geographical range of the endangered T. chrysogaster has conservation implications for this Mentawai endemic, so populations and habitat should be re-evaluated on each of the islands it inhabits. However, until such a re-evaluation is conducted, we recommend that the IUCN Red List status of this species be changed from ‘Endangered’ to ‘Data Deficient’.

Mentawai;Batu Islands

Book review: The requisite reference for the study of Sirenia

Sirenians often are given little or no notice in texts on marine mammals; whales, dolphins, and seals are what come to mind for most when a marine mammal is imagined. An order of only four extant species, the Sirenia is indeed the “other” frequently overlooked group of marine mammals. Dugongs and manatees remain unknown by much of the world, but to those that study these species, the members are extraordinarily unique and fascinating. The three highly respected authors of this newly published volume are all distinguished researchers, with more than a century of combined expertise in the study of this mammalian order. Their collective experience and insight make this book a captivating and valuable read for students, professionals, and anyone interested in having an all-inclusive reference for learning about the Order Sirenia. Review info: Ecology and conservation of the Sirenia-dugongs and manatees . By H. Marsh, T. J. O'Shea, and J. E. Reynolds, III, 2012. ISBN: 978-0521888288, 521 pp.

Journal of Mammalian Evolution

Are traditional methods of determining nest predators and nest fates reliable? An experiment with Wood Thrushes ( Hylocichla mustelina ) using miniature video cameras

We used miniature infrared video cameras to monitor Wood Thrush ( Hylocichla mustelina ) nests during 1998–2000. We documented nest predators and examined whether evidence at nests can be used to predict predator identities and nest fates. Fifty-six nests were monitored; 26 failed, with 3 abandoned and 23 depredated. We predicted predator class (avian, mammalian, snake) prior to review of video footage and were incorrect 57% of the time. Birds and mammals were underrepresented whereas snakes were over-represented in our predictions. We documented ≥9 nest-predator species, with the southern flying squirrel ( Glaucomys volans ) taking the most nests ( n = 8). During 2000, we predicted fate (fledge or fail) of 27 nests; 23 were classified correctly. Traditional methods of monitoring nests appear to be effective for classifying success or failure of nests, but ineffective at classifying nest predators.

The Auk

Animal population dynamics: Identification of critical components

There is a growing interest in the use of population dynamics models in environmental risk assessment and the promulgation of environmental regulatory policies. Unfortunately, because of species and areal differences in the physical and biotic influences on population dynamics, such models must almost inevitably be both complex and species- or site-specific. Given the emormous variety of species and sites of potential concern, this fact presents a problem; it simply is not possible to construct models for all species and circumstances. Therefore, it is useful, before building predictive population models, to discover what input parameters are of critical importance to the desired output. This information should enable the construction of simpler and more generalizable models. As a first step, it is useful to consider population models as composed to two, partly separable classes, one comprising the purely mechanical descriptors of dynamics from given demographic parameter values, and the other describing the modulation of the demographic parameters by environmental factors (changes in physical environment, species interactions, pathogens, xenobiotic chemicals). This division permits sensitivity analyses to be run on the first of these classes, providing guidance for subsequent model simplification. We here apply such a sensitivity analysis to network models of mammalian and avian population dynamics.

Ecological Modelling

Fossil shrews from Honduras and their significance for late glacial evolution in body size (Mammalia: Soricidae: Cryptotis)

Our study of mammalian remains excavated in the 1940s from McGrew Cave, north of Copán, Honduras, yielded an assemblage of 29 taxa that probably accumulated predominantly as the result of predation by owls. Among the taxa present are three species of small-eared shrews, genus Cryptotis . One species, Cryptotis merriami , is relatively rare among the fossil remains. The other two shrews, Cryptotis goodwini and Cryptotis orophila , are abundant and exhibit morphometrical variation distinguishing them from modern populations. Fossils of C. goodwini are distinctly and consistently smaller than modern members of the species. To quantify the size differences, we derived common measures of body size for fossil C. goodwini using regression models based on modern samples of shrews in the Cryptotis mexicana -group. Estimated mean length of head and body for the fossil sample is 72–79 mm, and estimated mean mass is 7.6–9.6 g. These numbers indicate that the fossil sample averaged 6–14% smaller in head and body length and 39–52% less in mass than the modern sample and that increases of 6–17% in head and body length and 65–108% in mass occurred to achieve the mean body size of the modern sample. Conservative estimates of fresh (wet) food intake based on mass indicate that such a size increase would require a 37–58% increase in daily food consumption. In contrast to C. goodwini , fossil C. orophila from the cave is not different in mean body size from modern samples. The fossil sample does, however, show slightly greater variation in size than is currently present throughout the modern geographical distribution of the taxon. Moreover, variation in some other dental and mandibular characters is more constrained, exhibiting a more direct relationship to overall size. Our study of these species indicates that North American shrews have not all been static in size through time, as suggested by some previous work with fossil soricids. Lack of stratigraphic control within the site and our failure to obtain reliable radiometric dates on remains restrict our opportunities to place the site in a firm temporal context. However, the morphometrical differences we document for fossil C. orophila and C. goodwini show them to be distinct from modern populations of these shrews. Some other species of fossil mammals from McGrew Cave exhibit distinct size changes of the magnitudes experienced by many northern North American and some Mexican mammals during the transition from late glacial to Holocene environmental conditions, and it is likely that at least some of the remains from the cave are late Pleistocene in age. One curious factor is that, whereas most mainland mammals that exhibit large-scale size shifts during the late glacial/postglacial transition experienced dwarfing, C. goodwini increased in size. The lack of clinal variation in modern C. goodwini supports the hypothesis that size evolution can result from local selection rather than from cline translocation. Models of size change in mammals indicate that increased size, such as that observed for C. goodwini , are a likely consequence of increased availability of resources and, thereby, a relaxation of selection during critical times of the year.

McGraw Cave

Small-mammal data on early and middle Holocene climates and biotic communities in the Bonneville Basin, USA

Archaeological investigations in Camels Back Cave, western Utah, recovered a series of small-mammal bone assemblages from stratified deposits dating between ca. 12,000 and 500 14C yr B.P. The cave's early Holocene fauna includes a number of species adapted to montane or mesic habitats containing grasses and/or sagebrush (e.g., Lepus townsendii, Marmota flaviventris, Reithrodontomys megalotis, and Brachylagus idahoensis) which suggest that the region was relatively cool and moist until after 8800 14C yr B.P. Between ca. 8600 and 8100 14C yr B.P. these mammals became locally extinct, taxonomic diversity declined, and there was an increase in species well-adapted to xeric, low-elevation habitats, including ground squirrels, Lepus californicus and Neotoma lepida. The early small-mammal record from Camels Back Cave is similar to the 11,300-6000 14C yr B.P. mammalian sequence from Homestead Cave, northwestern Utah, and provides corroborative data on Bonneville Basin paleoenvironments and mammalian responses to middle Holocene desertification. ?? 2002 University of Washington.

Quaternary Research

Nest spacing, habitat selection, and behavior of waterfowl on Miller Lake Island, North Dakota

The nesting behavior of a concentration of nesting mallards ( Anas platyrhynchos ) and gadwalls ( A. strepera ) was studied on a 4.5-ha island in Miller Lake, North Dakota, in 1977. A single 0.59-ha clump of thick shrub contained 225 simultaneously active mallard nests on 10 May. During the peak nesting period, mallard nests were spaced an average of 2.7 m from conspecifics. Active nests of all species peaked at 327, spaced an average of 2.1 m apart. Nests were clustered in thick shrub with moderate numbers in open shrub and few in grassland. Nest placement was significantly related to the amount of vegetative screening although mammalian predators were absent on the island. Cover density appeared to be important to the nesting hens as vegetation screened nests from potential avian predators and from harassment by other conspecific nesting hens and drakes. Mallards and gadwalls nesting on this island used wetlands in >100 km2 around Miller Lake. During daylight hours in late April 1978, an average of 4.9 mallards/minute arrived at the island; a peak of 17.2 mallards/minute arrived at 0800. In late April 1978, as many as 26 mallard pairs/ha occurred on favored wetlands and behavioral aggression was intense. Yet, most mallard hens maintained adequate space to acquire food and other requisites. Mallards and gadwalls were sufficiently adaptable to successfully exploit the Miller Lake island and environments that resulted in high reproductive success. Other local breeding Anatidae because of behavioral constraints were unable to exploit the same situation.

North Dakota

A novel member of the family Hepeviridae from cutthroat trout ( Oncorhynchus clarkii )

Beginning in 1988, the Chinook salmon embryo (CHSE-214) cell line was used to isolate a novel virus from spawning adult trout in the state of California, USA. Termed the cutthroat trout ( Oncorhynchus clarkii ) virus (CTV), the small, round virus was not associated with disease, but was subsequently found to be present in an increasing number of trout populations in the western USA, likely by a combination of improved surveillance activities and the shipment of infected eggs to new locations. Here, we report that the full length genome of the 1988 Heenan Lake isolate of CTV consisted of 7269 nucleotides of positive-sense, single-stranded RNA beginning with a 5' untranslated region (UTR), followed by three open reading frames (ORFs), a 3' UTR and ending in a polyA tail. The genome of CTV was similar in size and organization to that of Hepatitis E virus (HEV) with which it shared the highest nucleotide and amino acid sequence identities. Similar to the genomes of human, rodent or avian hepeviruses, ORF 1 encoded a large, non-structural polyprotein that included conserved methyltransferase, protease, helicase and polymerase domains, while ORF 2 encoded the structural capsid protein and ORF 3 the phosphoprotein. Together, our data indicated that CTV was clearly a member of the family Hepeviridae , although the level of amino acid sequence identity with the ORFs of mammalian or avian hepeviruses (13-27%) may be sufficiently low to warrant the creation of a novel genus. We also performed a phylogenetic analysis using a 262. nt region within ORF 1 for 63 isolates of CTV obtained from seven species of trout reared in various geographic locations in the western USA. While the sequences fell into two genetic clades, the overall nucleotide diversity was low (less than 8.4%) and many isolates differed by only 1-2 nucleotides, suggesting an epidemiological link. Finally, we showed that CTV was able to form persistently infected cultures of the CHSE-214 cell line that may have use in research on the biology or treatment of hepevirus infections of humans or other animals.

Virus Research

Boron Hazards to Fish, Wildlife, and Invertebrates: A Synoptic Review

Ecological and toxicological aspects of boron (B) in the environment are reviewed, with emphasis on natural resources. Subtopics covered include environmental chemistry, background concentrations, effects, and current recommendations for the protection of living resources. Boron is not now considered essential in mammalian nutrition, although low dietary levels protect against fluorosis and bone demineralization. Excessive consumption (i.e., >1,000 mg B/kg diet, >15 mg B/kg body weight daily, >1.0 mg B/L drinking water, or >210 mg B/kg body weight in a single dose) adversely affects growth, survival, or reproduction in sensitive mammals. Boron and its compounds are potent teratogens when applied directly to the mammalian embryo, but there is no evidence of mutagenicity or carcinogenicity. Boron`s unique affinity for cancerous tissues has been exploited in neutron capture radiation therapy of malignant human brain tumors. Current boron criteria recommended for the protection of sensitive species include <0.3 mg B/L in crop irrigation waters, <1.0 mg B/L for aquatic life, <5.0 mg B/L in livestock drinking waters, <30 mg B/kg in waterfowl diets, and <100 mg B/kg in livestock diets.

Contaminant Hazard Reviews

Epizootic plague in prairie dogs: Correlates and control with deltamethrin

The plague bacterium, Yersinia pestis , is a generalist pathogen of flea (Siphonaptera) vectors and mammalian hosts. In colonies of prairie dogs (PDs, Cynomys spp.), Y. pestis causes occasional epizootics, killing ≥90% of PDs within weeks to several months. We evaluated the effectiveness of deltamethrin, a pyrethroid insecticide, as a tool for preventing plague epizootics among three PD species. Specifically, we studied PD population growth on paired plots treated with deltamethrin for flea control or left untreated as baselines. We also evaluated PD population growth relative to flea abundance and PD density. All epizootics occurred on nontreated plots. Epizootics occurred on plots with very low PD densities as well as high densities. Mean population change, assessed by comparing visual counts of PDs in years before and during epizootics, was +88% for treated plots and −97% for nontreated plots. For comparison, an experimental oral vaccine against plague had an average change in population index or estimate during epizootics of −69% on vaccine plots compared with −83% for associated nontreated (placebo) plots. In our study and on plots not treated with deltamethrin, PD population growth was negatively correlated with flea abundance in the year before the epizootic, lending support to the hypothesis that flea abundance plays a critical role in plague transmission under natural conditions. Generally speaking, deltamethrin is a highly effective tool for plague management on PD colonies. That said, continued study is needed to refine deltamethrin treatments and to develop a more integrated strategy for plague management.

Vector-Borne and Zoonotic Diseases

Characterization of a C3a receptor in rainbow trout and Xenopus: The first identification of C3a receptors in nonmammalian species

Virtually nothing is known about the structure, function, and evolutionary origins of the C3aR in nonmammalian species. Because C3aR and C5aR are thought to have arisen from the same common ancestor, the recent characterization of a C5aR in teleost fish implied the presence of a C3aR in this animal group. In this study we report the cloning of a trout cDNA encoding a 364-aa molecule (TC3aR) that shows a high degree of sequence homology and a strong phylogenetic relationship with mammalian C3aRs. Northern blotting demonstrated that TC3aR was expressed primarily in blood leukocytes. Flow cytometric analysis and immunofluorescence microscopy showed that Abs raised against TC3aR stained to a high degree all blood B lymphocytes and, to a lesser extent, all granulocytes. More importantly, these Abs inhibited trout C3a-mediated intracellular calcium mobilization in trout leukocytes. A fascinating structural feature of TC3aR is the lack of a significant portion of the second extracellular loop (ECL2). In all C3aR molecules characterized to date, the ECL2 is exceptionally large when compared with the same region of C5aR. However, the exact function of the extra portion of ECL2 is unknown. The lack of this segment in TC3aR suggests that the extra piece of ECL2 was not necessary for the interaction of the ancestral C3aR with its ligand. Our findings represent the first C3aR characterized in nonmammalian species and support the hypothesis that if C3aR and C5aR diverged from a common ancestor, this event occurred before the emergence of teleost fish.

Journal of Immunology

Hepeviruses of fish

Originally reported from California, the cutthroat trout virus (CTV) has now been isolated from eight species of salmonids in North America. Early work focused on the replication and physical characteristics of the small, round virus, but not until 20 years later was it determined to be most closely related to viruses causing hepatitis E in humans or infecting avian and mammalian hosts. The genome of CTV consists of 7269 nucleotides of positive-sense, single-stranded RNA with a genome organization similar to other members of the family Hepeviridae , although the amino acid sequence identity appears low enough to support creation of a novel genus. While CTV has not been associated with acute disease in fish, the virus was able to form persistently infected cell cultures that may aid research in treatment of hepatitis E-like viruses affecting humans or other animals. Interestingly, trout exposed to CTV were protected for about a month against subsequent exposure to Infectious hematopoietic necrosis virus . Replicating agents suspected to be CTV can be confirmed by polymerase chain reaction (PCR) and sequencing.

Book chapter

Detection of prions from spiked and free-ranging carnivore feces

Chronic wasting disease (CWD) is a highly contagious, fatal neurodegenerative disease caused by infectious prions (PrP CWD ) affecting wild and captive cervids. Although experimental feeding studies have demonstrated prions in feces of crows ( Corvus brachyrhynchos ), coyotes ( Canis latrans ), and cougars ( Puma concolor ), the role of scavengers and predators in CWD epidemiology remains poorly understood. Here we applied the real-time quaking-induced conversion (RT-QuIC) assay to detect PrP CWD in feces from cervid consumers, to advance surveillance approaches, which could be used to improve disease research and adaptive management of CWD. We assessed recovery and detection of PrP CWD by experimental spiking of PrP CWD into carnivore feces from 9 species sourced from CWD-free populations or captive facilities. We then applied this technique to detect PrP CWD from feces of predators and scavengers in free-ranging populations. Our results demonstrate that spiked PrP CWD is detectable from feces of free-ranging mammalian and avian carnivores using RT-QuIC. Results show that PrP CWD acquired in natural settings is detectable in feces from free-ranging carnivores, and that PrP CWD rates of detection in carnivore feces reflect relative prevalence estimates observed in the corresponding cervid populations. This study adapts an important diagnostic tool for CWD, allowing investigation of the epidemiology of CWD at the community-level.

Scientific Reports

Scaling population density and spatial pattern for terrestrial, mammalian carnivores

A large part of ecological theory has been developed with the assumption that intra- and inter-specific patterns of density and spatial distribution can be consistently and reliably compared, and that these patterns have represented populations across nonstudied landscapes. These assumptions are erroneous. We found that log 10 population density estimates consistently decreased linearly with log 10 spatial extent of study areas for species of terrestrial Carnivora. The size of the study area accounted for most of the variation in population estimates, and study areas increased with the female body mass of the study species. But study sites consistently had higher densities than can be expected for nonstudy sites, regardless of the size of the study area, because study sites are typically chosen based on a priori knowledge of high density. Inter-specific comparisons of density and distribution might provide more insight into community organization after intra-specific density estimates have been scaled by the study areas, and related to the nonstudied landscapes within each species' geographic range.

Oecologia

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

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

Communications Biology