Onychomys Research Articles

Plague-Positive Mouse Fleas on Mice Before Plague Induced Die-Offs in Black-Tailed and White-Tailed Prairie Dogs.

Plague is a lethal zoonotic disease associated with rodents worldwide. In the western United States, plague outbreaks can decimate prairie dog (Cynomys spp.) colonies. However, it is unclear where the causative agent, Yersinia pestis, of this flea-borne disease is maintained between outbreaks, and what triggers plague-induced prairie dog die-offs. Less susceptible rodent hosts, such as mice, could serve to maintain the bacterium, transport infectious fleas across a colony, or introduce the pathogen to other colonies, possibly facilitating an outbreak. Here, we assess the potential role of two short-lived rodent species, North American deer mice (Peromyscus maniculatus) and Northern grasshopper mice (Onychomys leucogaster) in plague dynamics on prairie dog colonies. We live-trapped short-lived rodents and collected their fleas on black-tailed (Cynomys ludovicianus, Montana and South Dakota), white-tailed (Cynomys leucurus, Utah and Wyoming), and Utah prairie dog colonies (Cynomys parvidens, Utah) annually, from 2013 to 2016. Plague outbreaks occurred on colonies of all three species. In all study areas, deer mouse abundance was high the year before plague-induced prairie dog die-offs, but mouse abundance per colony was not predictive of plague die-offs in prairie dogs. We did not detect Y. pestis DNA in mouse fleas during prairie dog die-offs, but in three cases we found it beforehand. On one white-tailed prairie dog colony, we detected Y. pestis positive fleas on one grasshopper mouse and several prairie dogs live-trapped 10 days later, months before visible declines and plague-confirmed mortality of prairie dogs. On one black-tailed prairie dog colony, we detected Y. pestis positive fleas on two deer mice 3 months before evidence of plague was detected in prairie dogs or their fleas and also well before a plague-induced die-off. These observations of plague positive fleas on mice could represent early spillover events of Y. pestis from prairie dogs or an unknown reservoir, or possible movement of infectious fleas by mice.

Additional arvicolines and cricetids from the Fiene local fauna (Irvingtonian) of north-central Kansas

Two cricetids and three arvicolines are added to the Fiene local fauna (Irvingtonian) of north-central Kansas. Cricetids include the harvest mouse, Reithrodontomys moorei and grasshopper mouse, Onychomys sp. Arvicolines include the muskrat, Ondatra annectens, red-backed vole, Myodes gapperi, and bog lemming, Mictomys kansasensis. The latter two; taxa are extralimital and indicate cooler and wetter summers than at present in the area. Likewise, the record of Myodes represents the earliest occurrence of the taxon on the central Plains. The rarity of Onychomys relative to the previously reported abundant microtids in the Fiene local fauna indicates that the transition from a granivorous diet in the Blancan to a primarily insectivorous diet it has today was completed during Irvingtonian II.

SNP variable selection by generalized graph domination.

BackgroundHigh-throughput sequencing technology has revolutionized both medical and biological research by generating exceedingly large numbers of genetic variants. The resulting datasets share a number of common characteristics that might lead to poor generalization capacity. Concerns include noise accumulated due to the large number of predictors, sparse information regarding the p≫n problem, and overfitting and model mis-identification resulting from spurious collinearity. Additionally, complex correlation patterns are present among variables. As a consequence, reliable variable selection techniques play a pivotal role in predictive analysis, generalization capability, and robustness in clustering, as well as interpretability of the derived models.Methods and findingsK-dominating set, a parameterized graph-theoretic generalization model, was used to model SNP (single nucleotide polymorphism) data as a similarity network and searched for representative SNP variables. In particular, each SNP was represented as a vertex in the graph, (dis)similarity measures such as correlation coefficients or pairwise linkage disequilibrium were estimated to describe the relationship between each pair of SNPs; a pair of vertices are adjacent, i.e. joined by an edge, if the pairwise similarity measure exceeds a user-specified threshold. A minimum k-dominating set in the SNP graph was then made as the smallest subset such that every SNP that is excluded from the subset has at least k neighbors in the selected ones. The strength of k-dominating set selection in identifying independent variables, and in culling representative variables that are highly correlated with others, was demonstrated by a simulated dataset. The advantages of k-dominating set variable selection were also illustrated in two applications: pedigree reconstruction using SNP profiles of 1,372 Douglas-fir trees, and species delineation for 226 grasshopper mouse samples. A C++ source code that implements SNP-SELECT and uses Gurobi optimization solver for the k-dominating set variable selection is available (https://github.com/transgenomicsosu/SNP-SELECT).

Arizona bark scorpion venom resistance in the pallid bat, Antrozous pallidus.

The pallid bat (Antrozous pallidus), a gleaning bat found in the western United States and Mexico, hunts a wide variety of ground-dwelling prey, including scorpions. Anecdotal evidence suggests that the pallid bat is resistant to scorpion venom, but no systematic study has been performed. Here we show with behavioral measures and direct injection of venom that the pallid bat is resistant to venom of the Arizona bark scorpion, Centruroides sculpturatus. Our results show that the pallid bat is stung multiple times during a hunt without any noticeable effect on behavior. In addition, direct injection of venom at mouse LD50 concentrations (1.5 mg/kg) has no effect on bat behavior. At the highest concentration tested (10 mg/kg), three out of four bats showed no effects. One of the four bats showed a transient effect suggesting that additional studies are required to identify potential regional variation in venom tolerance. Scorpion venom is a cocktail of toxins, some of which activate voltage-gated sodium ion channels, causing intense pain. Dorsal root ganglia (DRG) contain nociceptive neurons and are principal targets of scorpion venom toxins. To understand if mutations in specific ion channels contribute to venom resistance, a pallid bat DRG transcriptome was generated. As sodium channels are a major target of scorpion venom, we identified amino acid substitutions present in the pallid bat that may lead to venom resistance. Some of these substitutions are similar to corresponding amino acids in sodium channel isoforms responsible for reduced venom binding activity. The substitution found previously in the grasshopper mouse providing venom resistance to the bark scorpion is not present in the pallid bat, indicating a potentially novel mechanism for venom resistance in the bat that remains to be identified. Taken together, these results indicate that the pallid bat is resistant to venom of the bark scorpion and altered sodium ion channel function may partly underlie such resistance.

Grasshopper mice employ distinct vocal production mechanisms in different social contexts.

Functional changes in vocal organ morphology and motor control facilitate the evolution of acoustic signal diversity. Although many rodents produce vocalizations in a variety of social contexts, few studies have explored the underlying production mechanisms. Here, we describe mechanisms of audible and ultrasonic vocalizations (USVs) produced by grasshopper mice (genus Onychomys). Grasshopper mice are predatory rodents of the desert that produce both loud, long-distance advertisement calls and USVs in close-distance mating contexts. Using live-animal recording in normal air and heliox, laryngeal and vocal tract morphological investigations, and biomechanical modelling, we found that grasshopper mice employ two distinct vocal production mechanisms. In heliox, changes in higher-harmonic amplitudes of long-distance calls indicate an airflow-induced tissue vibration mechanism, whereas changes in fundamental frequency of USVs support a whistle mechanism. Vocal membranes and a thin lamina propria aid in the production of long-distance calls by increasing glottal efficiency and permitting high frequencies, respectively. In addition, tuning of fundamental frequency to the second resonance of a bell-shaped vocal tract increases call amplitude. Our findings indicate that grasshopper mice can dynamically adjust motor control to suit the social context and have novel morphological adaptations that facilitate long-distance communication.

The complete mitochondrial genome of northern grasshopper mouse (Onychomys leucogaster)

In this study, we presented the complete mitochondrial genome of northern grasshopper mouse (Onychomys leucogaster). The circular genome is 16,370 bp in length and contains 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, 2 ribosome RNA genes, and 1 D-loop control regions. The overall nucleotide composition is: 31.2% A, 25.2% T, 29.9% C, and 13.6% G, with a total G + C content of 43.53%. The phylogenetic tree was constructed to validate the taxonomic status of Onychomys leucogaster, exhibiting a closest relationship with Neotoma fuscipes.

Flea and Small Mammal Species Composition in Mixed-Grass Prairies: Implications for the Maintenance ofYersinia pestis

Maintenance of sylvatic plague in prairie dogs (Cynomis spp.) was once thought unlikely due to high mortality rates; yet more recent findings indicate that low-level enzootic plague may be maintained in susceptible prairie dog populations. Another hypothesis for the maintenance of sylvatic plague involves small mammals, other than prairie dogs, as an alternative reservoir in the sylvatic plague system. These hypotheses, however, are not mutually exclusive, as both prairie dogs and small mammals could together be driving sylvatic cycles of plague. The concept of a bridging vector has been used to explain the transmission of pathogens from one host species to another. In the case of sylvatic plague, this would require overlap in fleas between small mammals and prairie dogs, and potentially other species such as carnivores. Our goal was to evaluate the level of flea sharing between black-tailed prairie dogs (Cynomis ludovicianus) and other small mammals in a mixed-grass prairie in South Dakota. We investigated the species richness of small mammals and small-mammal fleas in a mixed-grass prairie system and compared findings with previous studies from a short-grass ecosystem in Colorado. Over the summer field seasons 2014-2016 we live-trapped small mammals, collected fleas, and showed differences between both the flea and small mammal composition of the two systems. We also recorded higher densities of deer mice and lower densities of northern grasshopper mice in mixed versus shortgrass prairies. We confirmed, as is the case in shortgrass prairies, a lack of substantial flea species overlap on small mammal hosts and fleas from prairie dogs and their burrows. Moreover this study demonstrates that although small mammals may not play a large part in interepizootic plague cycling in shortgrass prairie ecosystems, their role in mixed-grass prairies requires further evaluation.

Sonoran Desert rodent abundance response to surface temperature derived from remote sensing

Nocturnal rodents play a key role in the Sonoran Desert ecosystem as consumers, prey and reservoirs of disease-yet rodent distribution remains poorly mapped. We use surface temperature extracted from the Landsat Thematic Mapper thermal infrared band to model rodent abundance obtained from trapping data at the Organ Pipe Cactus National Monument in southwest Arizona. We produce response curves that describe the effects of surface temperature on species abundance. Daytime surface temperature derived from images collected in June across thirty rodent trapping grids ranged from 318 K (45.0 °C) to 332 K (59.2 °C). Results show peak seasonal surface temperature splits high species abundances into two groups: Merriam's kangaroo rat, Arizona pocket mouse, desert pocket mouse and southern grasshopper mouse species prefer habitat characterized by higher surface temperatures; and white-throated wood rat, cactus mouse, rock pocket mouse and Bailey's pocket mouse species prefer habitat characterized by lower temperatures. Abundances for the high and low temperature habitat groupings correlate linearly with surface temperature (r = +0.66 and −0.75, respectively, p < 0.001). Surface temperature integrates multiple landscape characteristics (e.g. topography, vegetation cover and soil properties) that define the dominant habitats of ORPI rodents. These results prove that simple models can inform complex ecological processes.

Functional characterization and spatial clustering of visual cortical neurons in the predatory grasshopper mouse Onychomys arenicola.

Mammalian neocortical circuits are functionally organized such that the selectivity of individual neurons systematically shifts across the cortical surface, forming a continuous map. Maps of the sensory space exist in cortex, such as retinotopic maps in the visual system or tonotopic maps in the auditory system, but other functional response properties also may be similarly organized. For example, many carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas mice, rabbits, and the gray squirrel lack orientation maps. In this report we show that a carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola), lacks a canonical columnar organization of orientation preference in V1; however, neighboring neurons within 50 μm exhibit related tuning preference. Using a combination of two-photon microscopy and extracellular electrophysiology, we demonstrate that the functional organization of visual cortical neurons in the grasshopper mouse is largely the same as in the C57/BL6 laboratory mouse. We also find similarity in the selectivity for stimulus orientation, direction, and spatial frequency. Our results suggest that the properties of V1 neurons across rodent species are largely conserved.NEW & NOTEWORTHY Carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas rodents and lagomorphs lack this organization. We examine, for the first time, V1 of a wild carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola). We demonstrate the cellular organization of V1 in the grasshopper mouse is largely the same as the C57/BL6 laboratory mouse, suggesting that V1 neuron properties across rodent species are largely conserved.

Cross-fostering alters advertisement vocalizations of grasshopper mice (Onychomys): Evidence for the developmental stress hypothesis

Nutritional stress can have lasting impacts on the development of traits involved in vocal production. Cross-fostering experiments are often used to examine the propensity for vocal learning in a variety of taxa, but few studies assess the influence of malnourishment that can occur as a byproduct of this technique. In this study, we reciprocally cross-fostered sister taxa of voluble grasshopper mice (genus Onychomys) to explore their propensity for vocal learning. Vocalizations of Onychomys leucogaster did not differ between control and cross-fostered animals, but cross-fostered Onychomys arenicola produced vocalizations that were higher in frequency in a direction away from tutors. These same animals exhibited a transient reduction in body mass early in development, indicative of malnutrition. Our findings simultaneously refute vocal learning and support the developmental stress hypothesis to highlight the importance of early ontogeny on the production of vocalizations later in life.

Asymmetric energetic costs in reciprocal-cross hybrids between carnivorous mice (Onychomys).

Aerobic respiration is a fundamental physiological trait dependent on coordinated interactions between gene products of the mitochondrial and nuclear genomes. Mitonuclear mismatch in interspecific hybrids may contribute to reproductive isolation by inducing reduced viability (or even complete inviability) due to increased metabolic costs. However, few studies have tested for effects of mitonuclear mismatch on respiration at the whole-organism level. We explored how hybridization affects metabolic rate in closely related species of grasshopper mice (genus Onychomys) to better understand the role of metabolic costs in reproductive isolation. We measured metabolic rate across a range of temperatures to calculate basal metabolic rate (BMR) and cold-induced metabolic rate (MRc) in O. leucogaster, O. torridus and O. arenicola, and in reciprocal F1 hybrids between the latter two species. Within the genus, we found a negative correlation between mass-specific BMR and body mass. Although O. arenicola was smaller than O. torridus, hybrids from both directions of the cross resembled O. arenicola in body mass. In contrast, hybrid BMR was strongly influenced by the direction of the cross: reciprocal F1 hybrids were different from each other but indistinguishable from the maternal species. In addition, MRc was not significantly different between hybrids and either parental species. These patterns indicate that metabolic costs are not increased in Onychomys F1 hybrids and, while exposure of incompatibilities in F2 hybrids cannot be ruled out, suggest that mitonuclear mismatch does not act as a primary barrier to gene flow. Maternal matching of BMR is suggestive of a strong effect of mitochondrial genotype on metabolism in hybrids. Together, our findings provide insight into the metabolic consequences of hybridization, a topic that is understudied in mammals.

Predatory grasshopper mice

A Quick Guide on grasshopper mice which, contrary to the great majority of mouse species, are obligate carnivores.

The neurobiology of predation: sensory adaptations to carnivory (89.3)

Study objective: We investigated the central and peripheral nervous systems of northern grasshopper mice (Onychomys leucogaster), the most highly carnivorous rodents in North America, in order to explore potential neural correlates of the transition to carnivory.Methods: Multiunit electrophysiological recordings combined with analysis of flattened sections of neocortex processed for cytochrome oxidase were used to determine the topography of primary somatosensory cortex (S1) and the location and size of both the visual and auditory cortex. These findings were then related to flattened cortical sections of juvenile grasshopper mice labeled with the serotonin transporter (SERT) antibody. The number of myelinated axons in trigeminal, cochlear, and optic nerves were also quantified.Results: An enlarged forepaw representation was discovered within S1. Primary visual cortex (V1) also appeared to be larger in flattened cortex preparations compared to other rodents. Whereas the trigeminal and cochlear nerves were comparable to other rodents, the optic nerve contained a large number of axons.Conclusions: Grasshopper mice utilize a more specialized repertoire of attacks that rely on the forelimb, which perhaps corresponds to a magnification of this representation in S1 relative to other rodents. Enlargements of the optic nerve and V1 may also optimize processing of visual cues to enhance predatory success.Grant Funding Source: Supported by NIH grant # DE016061 and NSF grant # 0844743 to K.C.C.

Bite Me!

Grasshopper mice use the scorpion’s strength against it—instead of inducing pain, scorpion venom blocks pain.

Voltage-Gated Sodium Channel in Grasshopper Mice Defends Against Bark Scorpion Toxin

Painful venoms are used to deter predators. Pain itself, however, can signal damage and thus serves an important adaptive function. Evolution to reduce general pain responses, although valuable for preying on venomous species, is rare, likely because it comes with the risk of reduced response to tissue damage. Bark scorpions capitalize on the protective pain pathway of predators by inflicting intensely painful stings. However, grasshopper mice regularly attack and consume bark scorpions, grooming only briefly when stung. Bark scorpion venom induces pain in many mammals (house mice, rats, humans) by activating the voltage-gated Na(+) channel Nav1.7, but has no effect on Nav1.8. Grasshopper mice Nav1.8 has amino acid variants that bind bark scorpion toxins and inhibit Na(+) currents, blocking action potential propagation and inducing analgesia. Thus, grasshopper mice have solved the predator-pain problem by using a toxin bound to a nontarget channel to block transmission of the pain signals the venom itself is initiating.

Natural Selection and Pain Meet at a Sodium Channel

Grasshopper mice can feed on toxic bark scorpions because they have evolved resistance to the pain normally caused by the toxin in the scorpion sting. [Also see Research Article by Rowe et al. ]

Movements and burrow use by northern grasshopper mice as a possible mechanism of plague spread in prairie dog colonies

Abstract Northern grasshopper mice (Onychomys leucogaster) have been implicated as a potential reservoir for plague, which causes local extinction of black-tailed prairie dog (Cynomys ludovicianus) colonies. To identify mechanisms by which grasshopper mice could facilitate plague spread, we measured burrow use, movements, and flea burdens of mice in colonies in northern Colorado. At the microhabitat scale, powder-tracked mice (n = 41) used both prairie dog mounds and burrows extensively, entering an average of 5.3 burrows per 100 m traveled. Burrow use did not differ between active and inactive mounds, or vary with mouse age, sex, or reproductive status. Radiotracking revealed that mice occupied larger ranges (X = 3.84 ha) than reported off colonies, which we estimated would overlap 12–23 prairie dog coterie territories. Mice also harbored high flea burdens (8.1 fleas/mouse), including fleas associated with prairie dogs, which we attributed to their frequent use of burrows. Our results support the conten...

Landscape-scale features affecting small mammal assemblages on the northern Great Plains of North America

Abstract Little is known about the macrohabitat associations of rodents and shrews in prairie landscapes because of the logistic constraints of conventional trapping. We used the remains of 60,972 small mammals in owl pellets to assess factors affecting small mammal composition across 4.3 million hectares of the northern Great Plains of North America. Cropland with clay soils was dominated by deer mice (Peromyscus maniculatus), whereas areas with higher proportions of native grassland and moderately sandy soils supported communities with more sagebrush voles (Lemmiscus curtatus). Areas with clay soils and higher annual precipitation were associated with higher proportions of house mice (Mus musculus), meadow voles (Microtus pennsylvanicus), and shrews (Blarina brevicauda and Sorex species), whereas drier areas with sandier soils and lower annual precipitation were dominated by olive-backed pocket mice (Perognathus fasciatus) and northern grasshopper mice (Onychomys leucogaster). Contrary to extrapolations...

Marginal Record of the Southern Grasshopper MouseOnychomys torridusin Baja California, México

ABSTRACT. A specimen of an adult male of the southern grasshopper mouse Onychomys torridus was collected in Punta Choros, 25 km SE of Bahia de los Angeles, Baja California, Mexico. This record extends the species' distribution 330 km SE of the prior southernmost locality on the peninsula.

Vocal stereotypy in the rodent genera Peromyscus and Onychomys (Neotominae): taxonomic signature and call design

Stereotypic behaviour, such as territorial calls and songs, is thought to be evolutionarily conserved, and therefore useful in discerning systematic relationships. We examined vocalizations of several species of Peromyscus and Onychomys, a monophyletic group of rodents (Peromyscini). We report stereotypic vocal signals occurring in both sexes of the deer mice Peromyscus californicus, P. eremicus, P. leucopus, P. melanophrys, P. polionotus, and the grasshopper mice Onychomys arenicola and O. leucogaster. The stereotypic vocalizations of P. eremicus, P. leucopus, and P. polionotus are confined to frequencies greater than 20 kHz, unlike those of Onychomys, which are clearly audible, or P. californicus and P. melanophrys, which generate lower frequency vocalizations than the other Peromyscus. We did not observe stereotypic vocalizations in P. aztecus. Intensity, context and consistency suggest that these vocalizations serve an announcement function. Distribution of spectral energy distinguishes genera and most species, and some use of frequency is correlated to body size. There is a dichotomy between Onychomys and Peromyscus in the use of frequency, a genus-specific pattern identified previously among other peromyscine lineages.