Daily electrical activity in the master circadian clock of a diurnal mammal.

Circadian rhythms in mammals are orchestrated by a central clock within the suprachiasmatic nuclei (SCN). Our understanding of the electrophysiological basis of SCN activity comes overwhelmingly from a small number of nocturnal rodent species, and the extent to which these are retained in day-active animals remains unclear. Here, we recorded the spontaneous and evoked electrical activity of single SCN neurons in the diurnal rodent Rhabdomys pumilio, and developed cutting-edge data assimilation and mathematical modeling approaches to uncover the underlying ionic mechanisms. As in nocturnal rodents, R. pumilio SCN neurons were more excited during daytime hours. By contrast, the evoked activity of R. pumilio neurons included a prominent suppressive response that is not present in the SCN of nocturnal rodents. Our modeling revealed and subsequent experiments confirmed transient subthreshold A-type potassium channels as the primary determinant of this response, and suggest a key role for this ionic mechanism in optimizing SCN function to accommodate R. pumilio's diurnal niche.

Comparative morphometric analysis of lungs of the semifossorial giant pouched rat (Cricetomys gambianus) and the subterranean Nigerian mole rat (Cryptomys foxi).

Lungs of the rodent species, the African giant pouched rat (Cricetomys gambianus) and the Nigerian mole rat (Cryptomys foxi) were investigated. Significant morphometric differences exist between the two species. The volume of the lung per unit body mass was 2.7 times larger; the respiratory surface area 3.4 times greater; the volume of the pulmonary capillary blood 2 times more; the harmonic mean thickness of the blood-gas (tissue) barrier (τht) ~29% thinner and; the total pulmonary morphometric diffusing capacity (DLo2) for O2 2.3 times more in C. foxi. C. gambianus occupies open burrows that are ventilated with air while C. foxi lives in closed burrows. The less morphometrically specialized lungs of C. gambianus may be attributed to its much larger body mass (~6 times more) and possibly lower metabolic rate and its semifossorial life whereas the 'superior' lungs of C. foxi may largely be ascribed to the subterranean hypoxic and hypercapnic environment it occupies. Compared to other rodents species that have been investigated hitherto, the τht was mostly smaller in the lungs of the subterranean species and C. foxi has the highest mass-specific DLo2. The fossorial- and the subterranean rodents have acquired various pulmonary structural specializations that relate to habitats occupied.

USVSEG: A robust method for segmentation of ultrasonic vocalizations in rodents.

Rodents' ultrasonic vocalizations (USVs) provide useful information for assessing their social behaviors. Despite previous efforts in classifying subcategories of time-frequency patterns of USV syllables to study their functional relevance, methods for detecting vocal elements from continuously recorded data have remained sub-optimal. Here, we propose a novel procedure for detecting USV segments in continuous sound data containing background noise recorded during the observation of social behavior. The proposed procedure utilizes a stable version of the sound spectrogram and additional signal processing for better separation of vocal signals by reducing the variation of the background noise. Our procedure also provides precise time tracking of spectral peaks within each syllable. We demonstrated that this procedure can be applied to a variety of USVs obtained from several rodent species. Performance tests showed this method had greater accuracy in detecting USV syllables than conventional detection methods.

Dietary morphology of two island-endemic murid rodent clades is consistent with persistent, incumbent-imposed competitive interactions.

A lineage colonizing a geographic region with no competitors may exhibit rapid diversification due to greater ecological opportunity. The resultant species diversity of this primary-colonizing (incumbent) clade may limit subsequent lineages' ability to persist unless these non-incumbent lineages are ecologically distinct. We compare the diversity in diet-related mandibular morphology of two sympatric murid rodent clades endemic to Luzon Island, Philippines-incumbent Phloeomyini and secondary-colonizing Chrotomyini-to the mandibular morphological diversity of Sahul Hydromyini, the sister clade of Chrotomyini and the incumbent murid lineage on the supercontinent of Sahul. This three-clade comparison allows us to test the hypothesis that incumbent lineages can force persistent ecological distinction of subsequent colonists at the time of colonization and throughout the subsequent history of the two sympatric clades. We find that Chrotomyini forms a subset of the diversity of their clade plus Sahul Hydromyini that minimizes overlap with Phloeomyini. We also infer that this differentiation extends to the stem ancestor of Chrotomyini and Sahul Hydromyini, consistent with a biotic filter imposed by Phloeomyini. Our work illustrates that incumbency has the potential to have a profound influence on the ecomorphological diversity of colonizing lineages at the island scale even when the traits in question are evolving at similar rates among independently colonizing clades.

Extreme and Variable Climatic Conditions Drive the Evolution of Sociality in Australian Rodents.

Climate change is generating an intensification of extreme environmental conditions, including frequent and severe droughts [1] that have been associated with increased social conflict in vertebrates [2-4], including humans [5]. Yet, fluctuating climatic conditions have been shown to also promote cooperative behavior and the formation of vertebrate societies over both ecological and evolutionary timescales [6]. Determining when climatic uncertainty breeds social discord or promotes cooperative living (or both) is fundamental to predicting how species will respond to anthropogenic climate change. In light of this, our limited understanding of the order of evolutionary events-that is, whether harsh environments drive the evolution of sociality [6] or, alternatively, whether sociality facilitates the invasion of harsh environments [7]-and of how cooperation and conflict coevolve in response to environmental fluctuation represent critical gaps in knowledge. Here, we perform comparative phylogenetic analyses on Australian rodents (Muridae: Hydromyini) and show that sociality evolves only under harsh conditions of low rainfall and high temperature variability and never under relatively benign conditions. Further, we demonstrate that the requirement to cooperate under harsh climatic conditions generates social competition for reproduction within groups (reflected in the degree of sexual dimorphism in traits associated with intrasexual competition [8]), which in turn shapes the evolution of body size dimorphism. Our findings suggest that as the environment becomes more severe [1], the resilience of some species may hinge on their propensity to live socially, but in so doing, this is likely to affect the evolution of traits that mediate social conflict.

Locomotor activity in field captured crepuscular four-striped field mice, Rhabdomys dilectus and nocturnal Namaqua rock mice, Micaelamys namaquensis during a simulated heat wave.

Activity of animals is influenced by ambient temperature and increasing temperatures brought about by climate change may impose a heat stress risk. Previous studies investigating the effect of heat waves on activity usually measure animals at different, but constant temperatures, however, rarely are they studied under a natural temperature cycle. General activity, behavioural flexibility and frequency of water drinking counts during a normal day, hot day and a simulated heat wave temperature cycle were studied in the crepuscular four-striped field mouse, Rhabdomys dilectus, and the nocturnal Namaqua rock mouse, Micaelamys namaquensis. Both R. dilectus and M. namaquensis showed typical daily locomotor activity under control conditions. During the heat wave, peak activity times changed for R. dilectus, but both species exhibited higher bouts of activity for the heat wave during the day compared to the control, which was accompanied by an increased amount of time spent drinking water. The increased activity during the heat wave is likely due to enhanced water requirements and potentially a form of behavioural thermoregulation as animals may be uncomfortable and try to move to cooler areas. Thus, in the absence of a typical microclimate, access to water may allow rodents to overcome heat stress from extreme temperatures without having to shift their temporal active times.

Blue light at night acutely impairs glucose tolerance and increases sugar intake in the diurnal rodent Arvicanthis ansorgei in a sex-dependent manner.

In our modern society, the exposure to light at night (LAN) has increased considerably, which may impact human health negatively. Especially exposure to light at night containing short wavelength emissions (~450-500 nm) can disrupt the normal function of the biological clock, altering sleep-wake cycles and inducing metabolic changes. Recently, we reported that light at night acutely impairs glucose tolerance in nocturnal rats. However, light at night in nocturnal rodents coincides with their activity period, in contrast to artificial light at night exposure in humans. The aim of this study was to evaluate the acute effects of blue (λ = 490 ± 20 nm) artificial light at night (bALAN) on glucose metabolism and food intake in both male and female diurnal Sudanian grass rats (Arvicanthis ansorgei) fed either regular chow or a free choice high-fat high sucrose diet (HFHS). In both chow and HFHS fed male Arvicanthis, 1-hour of bALAN exposure induced a higher glucose response in the oral glucose tolerance test (OGTT) accompanied by a significant decrease in plasma insulin. Furthermore, in HFHS fed animals, bALAN induced an increase in sucrose intake during the dark phase in males but not in females. Additionally, 1-h of bALAN increased the nonfasted glucose levels together with plasma corticosterone in female grass rats. These results provide new and further evidence for the deleterious effects of exposure to short wavelength emission-containing artificial light at night on glucose metabolism in a diurnal rodent in a sex-dependent manner.

Functional and anatomical variations in retinorecipient brain areas in Arvicanthis niloticus and Rattus norvegicus: implications for the circadian and masking systems.

Daily rhythms in light exposure influence the expression of behavior by entraining circadian rhythms and through its acute effects on behavior (i.e., masking). Importantly, these effects of light are dependent on the temporal niche of the organism; for diurnal organisms, light increases activity, whereas for nocturnal organisms, the opposite is true. Here we examined the functional and morphological differences between diurnal and nocturnal rodents in retinorecipient brain regions using Nile grass rats (Arvicanthis niloticus) and Sprague-Dawley (SD) rats (Rattus norvegicus), respectively. We established the presence of circadian rhythmicity in cFOS activation in retinorecipient brain regions in nocturnal and diurnal rodents housed in constant dark conditions to highlight different patterns between the temporal niches. We then assessed masking effects by comparing cFOS activation in constant darkness (DD) to that in a 12:12 light/dark (LD) cycle, confirming light responsiveness of these regions during times when masking occurs in nature. The intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPN) exhibited significant variation among time points in DD of both species, but their expression profiles were not identical, as SD rats had very low expression levels for most timepoints. Light presentation in LD conditions induced clear rhythms in the IGL of SD rats but eliminated them in grass rats. Additionally, grass rats were the only species to demonstrate daily rhythms in LD for the habenula and showed a strong response to light in the superior colliculus. Structurally, we also analyzed the volumes of the visual brain regions using anatomical MRI, and we observed a significant increase in the relative size of several visual regions within diurnal grass rats, including the lateral geniculate nucleus, superior colliculus, and optic tract. Altogether, our results suggest that diurnal grass rats devote greater proportions of brain volume to visual regions than nocturnal rodents, and cFOS activation in these brain regions is dependent on temporal niche and lighting conditions.

First levantine fossil murines shed new light on the earliest intercontinental dispersal of mice.

Recent extensive field prospecting conducted in the Upper Miocene of Lebanon resulted in the discovery of several new fossiliferous localities. One of these, situated in the Zahleh area (Bekaa Valley, central Lebanon) has yielded a particularly diverse vertebrate fauna. Micromammals constitute an important part of this assemblage because not only do they represent the first Neogene rodents and insectivores from Lebanon, but they are also the only ones from the early Late Miocene of the Arabian Peninsula and circumambient areas. Analyses of the murines from Zahleh reveal that they belong to a small-sized early Progonomys, which cannot be assigned to any of the species of the genus hitherto described. They are, thereby, shown to represent a new species: Progonomys manolo. Morphometric analyses of the outline of the first upper molars of this species suggest a generalist and omnivorous diet. This record sheds new light onto a major phenomenon in the evolutionary history of rodents, which is the earliest dispersal of mice. It suggests that the arrival of murines in Africa got under way through the Levant rather than via southern Europe and was monitored by the ecological requirements of Progonomys.

Winter Reproduction of Cyclomorphic Mammals: From a Case to the Phenomenon.

In 2010 (a year of drought), the true winter breeding (TWB) of the pygmy wood mouse (S. uralensis) was first recorded in the Southern Urals and confirmed by the morphological parameters and age markers. The young born in winter fulfilled successfully their reproductive potential under favorable climatic conditions. The true winter breeding and the age cross of animals during the year of drought promoted the maximum population growth and enhanced population genetic heterogeneity. In subsequent years, TWB of S. uralensis became common, which is regarded as a climatic pattern. Extreme drought rearranged the rodent community and caused TWB of S. uralensis, which resulted in a higher abundance of the species.

Molecular phylogeographic analyses and species delimitations reveal that Leopoldamys edwardsi (Rodentia: Muridae) is a species complex.

Leopoldamys edwardsi is a species with wide distribution ranges in southern China but is not discussed in studies on geographic variation and species differentiation. We used 2 mitochondrial (Cytb, CO1) and 3 nuclear (GHR, IRBP and RAG1) genes to clarify species phylogeography and geographical differentiation. Maximum likelihood (ML) and Bayesian phylogenetic inference (BI) trees consistently indicated that L. edwardsi is a species complex containing 3 main lineages with high Kimura-2-parameter (K2P) divergences (i.e. lineages LN , LS and LHN ) found in the northern and southern China and Hainan Island, respectively. The 3 species delimitation methods, automated barcoding gap discovery, Bayesian poisson tree process analysis and Bayesian phylogenetics and phylogeography, consistently supported the existence of cryptic species. Divergence times among the main lineages were inferred to be during the Pleistocene, with LHN /LS split at 1.33 Ma and LN /(LHN +LS ) at 2.61 Ma; the diversifications of L. edwardsi complex might be caused by the rapid uplifts of Tibetan Plateau, paleoclimate change and complex topography. The divergence between LHN and LS was probably related to the separation of Hainan Island from the mainland via the formation of the Qiongzhou Strait. Lineages LN and (LS +LHN ) likely diverged due to the Wuyi-Nanling mountain range forming a dispersal barrier. Our results suggested that L. edwardsi complex contains at least 3 distinct species: LHN represents L. hainanensis, endemic to Hainan Island and previously considered as a subspecies L. e. hainanensis; LS represents a cryptic species distributed throughout the southern Chinese continent; and LN represents the nominotypical species L. edwardsi.

Fitness effects of interspecific competition between two species of desert rodents.

Many factors affect individual fitness, but while some factors, such as resource availability, have received strong experimental support, others including interspecific competition have rarely been quantified. Nevertheless, interspecific competition is commonly mentioned in the context of reproductive success and fitness. In general, when reproduction is likely to fail, reproductive suppression may occur. We studied the golden spiny mouse (Acomys russatus) and the common spiny mouse (A. cahirinus; however, recent molecular analysis in spiny mice from Jordan and Sinai suggests this species is A. dimidiatus (Frynta et al., 2010), as a model for the effect of competition on reproduction in four field enclosures: two populated only by A. russatus individuals, and two populated by individuals of both species. In presence of A. cahirinus, fitness of A. russatus was lower: the number of A. rusatus offspring was significantly lower; more males had regressed testes (indicating reproductive depression); more A. russatus young had damaged tails. However, no clear effect was evident in A. russatus female vaginal smear cytology. We conclude that the presence of A. cahirinus impairs fitness and reproductive success of A. russatus. While various direct and/or indirect mechanisms may be responsible for the effect of competition on reproduction, a plausible mechanism is increased use of torpor induced by the presence of A. cahirinus previously documented in A. russatus.

Adaptive Transcriptome Profiling of Subterranean Zokor, Myospalax baileyi, to High- Altitude Stresses in Tibet.

Animals living at high altitudes have evolved distinct phenotypic and genotypic adaptations against stressful environments. We studied the adaptive patterns of altitudinal stresses on transcriptome turnover in subterranean plateau zokors (Myospalax baileyi) in the high-altitude Qinghai-Tibetan Plateau. Transcriptomes of zokors from three populations with distinct altitudes and ecologies (Low: 2846 m, Middle: 3282 m, High: 3,714 m) were sequenced and compared. Phylogenetic and principal component analyses classified them into three divergent altitudinal population clusters. Genetic polymorphisms showed that the population at H, approaching the uppermost species boundary, harbors the highest genetic polymorphism. Moreover, 1056 highly up-regulated UniGenes were identified from M to H. Gene ontologies reveal genes like EPAS1 and COX1 were overexpressed under hypoxia conditions. EPAS1, EGLN1, and COX1 were convergent in high-altitude adaptation against stresses in other species. The fixation indices (F ST and G ST )-based outlier analysis identified 191 and 211 genes, highly differentiated among L, M, and H. We observed adaptive transcriptome changes in Myospalax baileyi, across a few hundred meters, near the uppermost species boundary, regardless of their relatively stable underground burrows' microclimate. The highly variant genes identified in Myospalax were involved in hypoxia tolerance, hypercapnia tolerance, ATP-pathway energetics, and temperature changes.

Skull Size and Biomechanics are Good Estimators of In Vivo Bite Force in Murid Rodents.

Rodentia is a species-rich group with diversified modes of life and diets. Although rodent skull morphology has been the focus of a voluminous literature, the functional significance of its variations has yet to be explored in live animals. Myomorphous rodents, including murids, have been suggested to represent "high-performance generalists." We measured in vivo bite force in 14 species of wild and lab-reared murid rodents of various sizes and diets to investigate potential morphofunctional differences between them. We dissected their skulls and computed a biomechanical model to estimate bite force. We first tested if our model allowed good estimation of in vivo data. Then, using morphological, in vivo and estimated bite force data in a phylogenetic context, we aimed to find the drivers of bite force differences among species. Estimated and in vivo bite forces were strongly correlated, which indicates that (a) biomechanical models allow a good estimation of real performance, and that (b) size and muscular changes (increased mass, fiber length, and PCSA) are the main drivers of bite performance differences. Myomorphous rodents, therefore, may have evolved high bite force through a combination of changes in size and musculature, which gave them a great versatility in their ability to process food. We found mixed results at the intraspecific level, with only some species displaying a good fit between estimated and in vivo measurements. We suggest that limited variation in size and muscular organization, and increased behavioral variation might decrease the precision of bite force estimates within species. Anat Rec, 301:256-266, 2018. © 2018 Wiley Periodicals, Inc.

Protein deficiency decreases stereotypic behavior frequency and prevalence and activity in the striped mouse Rhabdomys dilectus chakae.

Diverse motivational triggers, including diet, elicit stereotypic behavior. We investigated whether diets comprised of different protein levels but similar levels of energy were associated with the occurrence of locomotor stereotypies in the striped mouse Rhabdomys dilectus chakae. In a first experiment, 20 stereotypic and 20 non-stereotypic (10 subjects per sex and per group) juvenile (40 days old) subjects were placed on baseline (BP), high (HP) or low protein (LP) diet treatments (120 subjects in total). All subjects initially identified as stereotypic displayed stereotypic behavior in the BP and HP treatments on Days 60-63 and Days 80-83 compared to 35% and 12.5% of LP subjects, respectively. Moreover, LP subjects displayed lower levels of activity and stereotypic behavior than BP and HP subjects. Those identified as non-stereotypic never displayed stereotypy. In a second experiment, 48 individuals, bred and reared on LP and whose parents were stereotypic, were assigned to either HP (13 males, 12 females) or LP (12 males, 11 females) treatments at 50 days of age for 30 days. Stereotypy was three times less likely to occur in the LP than the HP treatment, and activity was greater in LP-HP individuals than LP-LP individuals. In both experiments, LP individuals had the lowest body mass. Striped mice adjusted their behaviors in response to dietary protein levels. Protein deficiency reduced activity and stereotypic behavior and prevalence, possibly related to an energy or neurological deficit.

Tuberculosis detection by pouched rats: Opportunities for reinforcement under low-prevalence conditions.

Giant African pouched rats (Cricetomys ansorgei) have been employed successfully in two operational tuberculosis-detection projects in which they sniff sputum samples from symptomatic individuals who have visited tuberculosis clinics. The prevalence of pulmonary tuberculosis in this population is high, approximately 20% in the regions where the rats have been used. If the rats are to be used to screen individuals from lower-prevalence populations, their performance under such conditions must first be evaluated. In this study, the prevalence of tuberculosis-positive samples presented to eight pouched rats was reduced to approximately 5%, and the percentage of known-positive samples included as opportunities for reinforcement was varied in sequence from 10 to 8, 6, 4, 2, 4, and 2. Liquid food reinforcers were delivered for identification responses to known-positive samples and at no other time. The rats' accuracy was clinically and statistically significantly lower at 2% than at the other values. These results indicate that the rats can perform well in low-prevalence scenarios but, if they are used under the conditions of the present study, at least 4% of the samples presented to them must be opportunities for reinforcement.

Arboreal Locomotion in Eurasian Harvest Mice Micromys Minutus (Rodentia: Muridae): The Gaits of Small Mammals.

Body size imposes significant constraints on arboreal locomotion. Despite the wealth of research in larger arboreal mammals, there is a lack of data on arboreal gaits of small mammals. In this context, the present study explores arboreal locomotion in one of the smallest rodents, the Eurasian harvest mice Micromys minutus (∼10 g). We examined gait metrics (i.e., diagonality, duty factor [DF], DF index, velocity, stride length, and stride frequency) of six adult male mice on simulated arboreal substrates of different sizes (2, 5, 10, and 25 mm) and inclinations (00 and 450 ). Micromys minutus employed slow, lateral sequence symmetrical gaits on the smaller substrates, which shifted to progressively faster symmetrical gaits of higher diagonality on larger substrates. Both ascents and descents were associated with a higher diagonality, and ascents with a higher DF index compared to horizontal locomotion, underscoring the role of the grasping hind feet. Velocity increase was brought about primarily by an increase in stride frequency, a pattern often encountered in other small mammals, with a secondary and significant contribution of stride length. These findings indicate that, except for velocity and the way it is regulated, there are no significant differences in gait metrics between larger and smaller arboreal mammals. Moreover, the locomotor adaptations of Eurasian harvest mice represent behavioral mechanisms that promote stable, safe, and continuous navigation along slender substrates and ultimately contribute to the successful exploitation of the arboreal milieu.

The contribution of the pineal gland on daily rhythms and masking in diurnal grass rats, Arvicanthis niloticus.

Melatonin is a hormone rhythmically secreted at night by the pineal gland in vertebrates. In diurnal mammals, melatonin is present during the inactive phase of the rest/activity cycle, and in primates it directly facilitates sleep and decreases body temperature. However, the role of the pineal gland for the promotion of sleep at night has not yet been studied in non-primate diurnal mammalian species. Here, the authors directly examined the hypothesis that the pineal gland contributes to diurnality in Nile grass rats by decreasing activity and increasing sleep at night, and that this could occur via effects on circadian mechanisms or masking, or both. Removing the pineal gland had no effect on the hourly distribution of activity across a 12:12 light-dark (LD) cycle or on the patterns of sleep-like behavior at night. Masking effects of light at night on activity were also not significantly different in pinealectomized and control grass rats, as 1h pulses of light stimulated increases in activity of sham and pinealectomized animals to a similar extent. In addition, the circadian regulation of activity was unaffected by the surgical condition of the animals. Our results suggest that the pineal gland does not contribute to diurnality in the grass rat, thus highlighting the complexity of temporal niche transitions. The current data raise interesting questions about how and why genetic and neural mechanisms linking melatonin to sleep regulatory systems might vary among mammals that reached a diurnal niche via parallel and independent pathways.

A decrease in heat insulation of the black-clawed brush-furred rat (Lophuromys melanonyx, Petter) during adaptation to high altitudes.

The results of the body-surface infrared thermography of rodents of the genus Lophuromys suggest that heat insulation of the black-clawed brush-furred rat L. melanonyx, a large specialized species of the AfroAlpine zone, is worse than that of the related smaller species, the golden-footed (L. chrysopus) and shorttailed (L. brevicaudus) brush-furred rats, that inhabit tropical forest and Erica shrub, respectively. A decrease in heat insulation of the alpine species may facilitate the use of solar radiation for supporting heat balance of these diurnal animals.

Repeated evolution of carnivory among Indo-Australian rodents.

Convergent evolution, often observed in island archipelagos, provides compelling evidence for the importance of natural selection as a generator of species and ecological diversity. The Indo-Australian Archipelago (IAA) is the world's largest island system and encompasses distinct biogeographic units, including the Asian (Sunda) and Australian (Sahul) continental shelves, which together bracket the oceanic archipelagos of the Philippines and Wallacea. Each of these biogeographic units houses numerous endemic rodents in the family Muridae. Carnivorous murids, that is those that feed on animals, have evolved independently in Sunda, Sulawesi (part of Wallacea), the Philippines, and Sahul, but the number of origins of carnivory among IAA murids is unknown. We conducted a comprehensive phylogenetic analysis of carnivorous murids of the IAA, combined with estimates of ancestral states for broad diet categories (herbivore, omnivore, and carnivore) and geographic ranges. These analyses demonstrate that carnivory evolved independently four times after overwater colonization, including in situ origins on the Philippines, Sulawesi, and Sahul. In each biogeographic unit the origin of carnivory was followed by evolution of more specialized carnivorous ecomorphs such as vermivores, insectivores, and amphibious rats.