Gene expression differences associated with intrinsic hindfoot muscle loss in the jerboa, Jaculus jaculus.

Vertebrate animals that run or jump across sparsely vegetated habitats, such as horses and jerboas, have reduced the number of distal limb bones, and many have lost most or all distal limb muscle. We previously showed that nascent muscles are present in the jerboa hindfoot at birth and that these myofibers are rapidly and completely lost soon after by a process that shares features with pathological skeletal muscle atrophy. Here, we apply an intra- and interspecies differential RNA-Seq approach, comparing jerboa and mouse muscles, to identify gene expression differences associated with the initiation and progression of jerboa hindfoot muscle loss. We show evidence for reduced hepatocyte growth factor and fibroblast growth factor signaling and an imbalance in nitric oxide signaling; all are pathways that are necessary for skeletal muscle development and regeneration. We also find evidence for phagosome formation, which hints at how myofibers may be removed by autophagy or by nonprofessional phagocytes without evidence for cell death or immune cell activation. Last, we show significant overlap between genes associated with jerboa hindfoot muscle loss and genes that are differentially expressed in a variety of human muscle pathologies and rodent models of muscle loss disorders. All together, these data provide molecular insight into the process of evolutionary and developmental muscle loss in jerboa hindfeet.

Immunohistochemical Localization of Glucose Transporter GLUT1 and GLUT3 in the Testes of some Mammals

SUMMARY: Glucose has an essential role in the proliferation and survival of testicular tissue. Glucose transporters (GLUTs) are responsible for glucose uptake across cell membranes. In the present work, two main isoforms GLUT1 and GLUT3 were investigated in the testes of Laboratory mouse (BALB/c), Lesser Egyptian jerboa (Jaculus jaculus), Golden hamster (Mesocricetus auratus), and Desert Hedgehog (Paraechinus aethiopicus). Immunofluorescent localization of GLUT1 and GLUT3 showed considerable species differences. The lowest expression of GLUT1 and GLUT3 was localized in the testis of Laboratory mouse (BALB/c), the highest GLUT1 localization was detected in the testis of Lesser Egyptian jerboa (Jaculus jaculus), and the highest GLUT3 immunofluorescent localization was observed in the testis of Hedgehog (Paraechinus aethiopicus). The results imply that GLUT3 is the principal glucose transporter in the studied testes, which is related to species differences. The different immunolocalization of GLUT in examined testes suggests using various transport systems for energy gain in different species.

La glucosa tiene un papel esencial en la proliferación y supervivencia del tejido testicular. Los transportadores de glucosa (GLUT) son responsables de la absorción de glucosa a través de las membranas celulares. En el presente trabajo, se investigaron dos isoformas principales GLUT1 y GLUT3 en los testículos de un ratón de laboratorio (BALB/c), un jerbo egipcio menor (Jaculus jaculus), un hámster dorado (Mesocricetus auratus) y un erizo del desierto (Paraechinus aethiopicus). La localización inmunofluorescente de GLUT1 y GLUT3 mostró diferencias considerables entre especies. La expresión más baja de GLUT1 y GLUT3 se localizó en el testículo del ratón de laboratorio (BALB/c), la localización más alta de GLUT1 se detectó en el testículo del jerbo egipcio menor (Jaculus jaculus) y la localización inmunofluorescente de GLUT3 más alta se observó en el testículo de Erizo (Paraechinus aethiopicus). Los resultados implican que GLUT3 es el principal transportador de glucosa en los testículos estudiados, lo que está relacionado con diferencias entre especies. La diferente inmunolocalización de GLUT en los testículos examinados sugiere el uso de varios sistemas de transporte para ganar energía en diferentes especies.

Genomic insights into adaptation to bipedal saltation and desert-like habitats of jerboas.

Jerboas is a lineage of small rodents displaying atypical mouse-like morphology with elongated strong hindlimbs and short forelimbs. They have evolved obligate bipedal saltation and acute senses, and been well-adapted to vast desert-like habitats. Using a newly sequenced chromosome-scale genome of the Mongolian five-toed jerboa (Orientallactaga sibirica), our comparative genomic analyses and in vitro functional assays showed that the genetic innovations in both protein-coding and non-coding regions played an important role in jerboa morphological and physiological adaptation. Jerboa-specific amino acid substitutions, and segment insertions/deletions (indels) in conserved non-coding elements (CNEs) were found in components of proteoglycan biosynthesis pathway (XYLT1 and CHSY1), which plays an important role in limb development. Meanwhile, we found specific evolutionary changes functionally associated with energy or water metabolism (e.g., specific amino acid substitutions in ND5 and indels in CNEs physically near ROR2) and senses (e.g., expansion of vomeronasal receptors and the FAM136A gene family) in jerboas. Further dual-luciferase reporter assay verified that some of the CNEs with jerboa-specific segment indels exerted a significantly different influence on luciferase activity, suggesting changes in their regulatory function in jerboas. Our results revealed the potential molecular mechanisms underlying jerboa adaptation since the divergence from the Eocene-Oligocene transition, and provided more resources and new insights to enhance our understanding of the molecular basis underlying the phenotypic diversity and the environmental adaptation of mammals.

Cranial differences in three-toed jerboas (Dipodinae, Dipodidae, Rodentia) according to recent taxonomic revisions.

Recent phylogenetic studies amended the taxonomy of three-toed jerboas (subfamily Dipodinae), including raising subspecies to full species. Here, we use geometric morphometrics to compare scaled-shape differences in dipodine crania while considering their revised taxonomy. We sampled Dipus deasyi, D. sagitta halli, D. s. sowerbyi, Jaculus blanfordi blanfordi, J. hirtipes, J. jaculus, J. loftusi, J. orientalis gerboa, J. o. mauritanicus, and Stylodipus andrewsi. Crania were not sexually dimorphic. Common allometry explained some of the shape variation, for example, reduced braincases in larger specimens. Most operational taxonomic unit pairs differed in both size and shape. Dipus and Stylodipus clustered together based on their cranial shape. Jaculus differed from the aforementioned genera by its larger tympanic bulla, broader braincase, larger infraorbital foramen, along with reduced molars and rostra. Jaculus orientalis differed from other Jaculus by its broader face versus reduced cranial vault. Jaculus blanfordi (subgenus Haltomys) resembles members of the subgenus Jaculus more than its consubgener (J. orientalis). Jaculus loftusi, previously considered a synonym of J. jaculus, clearly differed from the latter by its shorter rostrum, smaller infraorbital foramen, and more caudolaterally expanded tympanic bulla. Jaculus hirtipes, another recent synonym of J. jaculus, resembled J. blanfordi more in scaled cranial shape than it did J. jaculus. Dipus sagitta halli and D. s. sowerbyi were indistinguishable, but they clearly differed from D. deasyi (recently raised to full species) with the latter having a larger molar row, more inflated tympanic bulla, and shorter, slenderer rostrum. Ecological explanations for detected cranial shape differences are considered, including diet and habitat (particularly substrate).

First Report of Two Jaculus Rodents as Potential Reservoir Hosts of Leishmania Parasites in Tunisia.

This study shows, for the first time, natural Leishmania infection among Jaculus spp. in an endemic region of Tataouine, South Tunisia. To better characterize the transmission cycles in this complex focus of mixed transmission, Leishmania detection and species identification were performed by direct examination, internal transcribed spacer-1 (ITS1)-PCR-restriction fragment length polymorphism (RFLP), and sequencing of Jaculus (J.) jaculus (Linnaeus, 1758) and J. hirtipes (Lichtenstein, 1823) rodent species, which are frequently encountered in this area. Leishmania parasites were observed in 19 (41.3%) smears, while DNA parasites were detected in 28 (60.9%) Jaculus spp. spleens; among them, 12 (54.5%) were from 22 J. jaculus individuals and 16 (66.7%) were from 24 J. hirtipes individuals. Leishmania parasites were confirmed as Leishmania (L.) killicki (syn. L. tropica) in two J. hirtipes individuals (4.3%) and L. major (n = 24; 52.2%) in 10 J. jaculus and 14 J. hirtipes individuals. This finding represents the first evidence of natural infection with Leishmania parasites in rodents belonging to the Jaculus genus, providing the rationale to consider them as potential reservoir hosts of Old World Leishmania parasites in Tunisia and North Africa.

Exploring the potential roles of some rodents in the transmission of the Middle East respiratory syndrome coronavirus.

Middle East respiratory syndrome coronavirus (MERS-CoV) is one of the recently identified zoonotic coronaviruses. The one-hump camels are believed to play important roles in the evolution and transmission of the virus. The animal-to-animal, as well as the animal-to-human transmission in the context of MERS-CoV infection, were reported. The camels shed the virus in some of their secretions, especially the nasal tract. However, there are many aspects of the transmission cycle of the virus from animals to humans that are still not fully understood. Rodents played important roles in the transmission of many pathogens, including viruses and bacteria. They have been implicated in the evolution of many human coronaviruses, especially HCoV-OC43 and HCoV-HKU1. However, the role of rodents in the transmission of MERS-CoV still requires more exploration. To achieve this goal, we identified MERS-CoV that naturally infected dromedary camel by molecular surveillance. We captured 15 of the common rodents (rats, mice, and jerboa) sharing the habitat with these animals. We collected both oral and rectal swabs from these animals and then tested them by the commercial MERS-CoV real-time-PCR kits using two targets. Despite the detection of the viral shedding in the nasal swabs of some of the dromedary camels, none of the rodents tested positive for the virus during the tenure of this study. We concluded that these species of rodents did not harbor the virus and are most unlikely to contribute to the transmission of the MERS-CoV. However, further large-scale studies are required to confirm the potential roles of rodents in the context of the MERS-CoV transmission cycle, if any.

Activity strategy and pattern of the Siberian jerboa (Orientallactaga sibirica) in the Alxa desert region, China.

Rodents exhibit seasonal changes in their activity patterns as an essential survival strategy. We studied the activity patterns and strategies of the Siberian jerboa (Orientallactaga sibirica) in the Alxa desert region to better understand the habitats and behavioural ecology of xeric rodents. We conducted an experiment using three plots to monitor the duration, time, and frequency of the active period of the Siberian jerboa using infrared cameras in the Alxa field workstation, Inner Mongolia, China in 2017. The relationships between the activity time and frequency, biological factors (perceived predation risk, food resources, and species composition), and abiotic factors (temperature, air moisture, wind speed) were analysed using Redundancy Analysis (RDA). Our results showed that: (1) relative humidity mainly affected activities in the springtime; temperature, relative humidity and interspecific competition mainly affected activities in the summertime; relative humidity and perceived predation risk mainly influenced activities in the autumn. (2) The activity pattern of the Siberian jerboa altered depending on the season. The activity of the Siberian jerboa was found to be bimodal in spring and summer, and was trimodal in autumn. The activity time and frequency in autumn were significantly lower than the spring. (3) Animals possess the ability to integrate disparate sources of information about danger to optimize energy gain. The jerboa adapted different responses to predation risks and competition in different seasons according to the demand for food resources.

Secondary ossification center induces and protects growth plate structure.

Growth plate and articular cartilage constitute a single anatomical entity early in development but later separate into two distinct structures by the secondary ossification center (SOC). The reason for such separation remains unknown. We found that evolutionarily SOC appears in animals conquering the land - amniotes. Analysis of the ossification pattern in mammals with specialized extremities (whales, bats, jerboa) revealed that SOC development correlates with the extent of mechanical loads. Mathematical modeling revealed that SOC reduces mechanical stress within the growth plate. Functional experiments revealed the high vulnerability of hypertrophic chondrocytes to mechanical stress and showed that SOC protects these cells from apoptosis caused by extensive loading. Atomic force microscopy showed that hypertrophic chondrocytes are the least mechanically stiff cells within the growth plate. Altogether, these findings suggest that SOC has evolved to protect the hypertrophic chondrocytes from the high mechanical stress encountered in the terrestrial environment.

Whole mitochondrial genome sequence and phylogenetic relationships of Williams's jerboa (Scarturus williamsi) from Turkey.

Williams's jerboa (Scarturus williamsi), a medium-sized jerboa distributed in Anatolia and its adjacent regions, is a member of the four- and five-toed jerboas found mostly in Asia. Disagreements about the taxonomy of this taxon at the genus/species level continue to exist. Here, we report the first effort to sequence and assemble the mitochondrial genome of Williams's jerboa from Turkey. The mitochondrial genome of S. williamsi was 16,653 bp in total length and contained 13 protein-coding genes (PCGs), 22 transfer RNAs (tRNAs), two ribosomal RNAs (rRNAs), and two non-coding regions (the D-loop and OL region) with intergenic spacer. All of the genes, except ND6 and eight tRNAs, were encoded on the heavy chain strand, similar to the features of mitogenomes of other rodents. When compared with all available rodent mitochondrial genomes, Williams's jerboa showed (1) a serine deletion at the 3'-end of the ATP8 gene, (2) the ND5 gene terminated with a TAG codon and (3) a tandem repeat cluster (273 bp in length) in the control region. Williams's jerboa and Siberian jerboa grouped as sister taxa despite the high genetic distance (17.6%) between them, belonging to Allactaginae. This result is consistent with the latest pre-revision, which suggests that Williams's jerboa and the Siberian jerboa may belong to separate genera, as Scarturus and Orientallactaga, respectively. The present study provides a reference mitochondrial genome for Williams's jerboa for further molecular studies of other species of Dipodoidea and Rodentia.

Effects of artificial light at night on foraging behavior and vigilance in a nocturnal rodent.

Artificial light at night has greatly changed the physical environment for many organisms on a global scale. As an energy efficient light resource, light emitting diodes (LEDs) have been widely used in recent years. As LEDs often have a broad spectrum, many biological processes may be potentially affected. In this study, we conducted manipulated experiments in rat-proof enclosures to explore the effects of LED night lighting on behavior of a nocturnal rodent, the Mongolian five-toed jerboa (Allactaga sibirica). We adopted the giving-up density (GUD) method and camera video trapping to study behavioral responses in terms of patch use, searching efficiency and vigilance. With the presence of white LED lighting, jerboas spent less time in patches, foraged less intensively (with higher GUDs) and became vigilant more frequently, while their searching efficiency was higher than under dark treatment. Although both positive and negative effects of LEDs on foraging were detected, the net effect of LEDs on jerboas is negative, which may further translate into changes in population dynamics, inter-specific interaction and community structure. To our knowledge, this is the first field study to explore how LED lighting affect foraging behavior and searching efficiency in rodents. Our results may have potential implications for practices such as pest control.

Evolutionary loss of foot muscle during development with characteristics of atrophy and no evidence of cell death.

Many species that run or leap across sparsely vegetated habitats, including horses and deer, evolved the severe reduction or complete loss of foot muscles as skeletal elements elongated and digits were lost, and yet the developmental mechanisms remain unknown. Here, we report the natural loss of foot muscles in the bipedal jerboa, Jaculus jaculus. Although adults have no muscles in their feet, newborn animals have muscles that rapidly disappear soon after birth. We were surprised to find no evidence of apoptotic or necrotic cell death during stages of peak myofiber loss, countering well-supported assumptions of developmental tissue remodeling. We instead see hallmarks of muscle atrophy, including an ordered disassembly of the sarcomere associated with upregulation of the E3 ubiquitin ligases, MuRF1 and Atrogin-1. We propose that the natural loss of muscle, which remodeled foot anatomy during evolution and development, involves cellular mechanisms that are typically associated with disease or injury.

Convergent metatarsal fusion in jerboas and chickens is mediated by similarities and differences in the patterns of osteoblast and osteoclast activities.

In many vertebrate animals that run or leap, the metatarsals and/or metacarpals of the distal limb are fused into a single larger element, likely to resist fracture due to high ground-reaction forces during locomotion. Although metapodial fusion evolved independently in modern birds, ungulates, and jerboas, the developmental basis has only been explored in chickens, which diverged from the mammalian lineage approximately 300 million years ago. Here, we use a bipedal rodent, the lesser Egyptian jerboa (Jaculus jaculus), to understand the cellular processes of metatarsal fusion in a mammal, and we revisit the developing chicken to assess similarities and differences in the localization of osteoblast and osteoclast activities. In both species, adjacent metatarsals align along flat surfaces, osteoblasts cross the periosteal membrane to unite the three elements in a single circumference, and osteoclasts resorb bone at the interfaces leaving a single marrow cavity. However, the pattern of osteoclast activity differs in each species; osteoclasts are highly localized to resorb bone at the interfaces of neighboring jerboa metatarsals and are distributed throughout the endosteum of chicken metatarsals. Each species, therefore, provides an opportunity to understand mechanisms that pattern osteoblast and osteoclast activities to alter bone shape during development and evolution.

Vertical leaping mechanics of the Lesser Egyptian Jerboa reveal specialization for maneuverability rather than elastic energy storage.

BACKGROUND: Numerous historical descriptions of the Lesser Egyptian jerboa, Jaculus jaculus, a small bipedal mammal with elongate hindlimbs, make special note of their extraordinary leaping ability. We observed jerboa locomotion in a laboratory setting and performed inverse dynamics analysis to understand how this small rodent generates such impressive leaps. We combined kinematic data from video, kinetic data from a force platform, and morphometric data from dissections to calculate the relative contributions of each hindlimb muscle and tendon to the total movement. RESULTS: Jerboas leapt in excess of 10 times their hip height. At the maximum recorded leap height (not the maximum observed leap height), peak moments for metatarso-phalangeal, ankle, knee, and hip joints were 13.1, 58.4, 65.1, and 66.9 Nmm, respectively. Muscles acting at the ankle joint contributed the most work (mean 231.6 mJ / kg Body Mass) to produce the energy of vertical leaping, while muscles acting at the metatarso-phalangeal joint produced the most stress (peak 317.1 kPa). The plantaris, digital flexors, and gastrocnemius tendons encountered peak stresses of 25.6, 19.1, and 6.0 MPa, respectively, transmitting the forces of their corresponding muscles (peak force 3.3, 2.0, and 3.8 N, respectively). Notably, we found that the mean elastic energy recovered in the primary tendons of both hindlimbs comprised on average only 4.4% of the energy of the associated leap. CONCLUSIONS: The limited use of tendon elastic energy storage in the jerboa parallels the morphologically similar heteromyid kangaroo rat, Dipodomys spectabilis. When compared to larger saltatory kangaroos and wallabies that sustain hopping over longer periods of time, these small saltatory rodents store and recover less elastic strain energy in their tendons. The large contribution of muscle work, rather than elastic strain energy, to the vertical leap suggests that the fitness benefit of rapid acceleration for predator avoidance dominated over the need to enhance locomotor economy in the evolutionary history of jerboas.

Coordinated seasonal regulation of metabolic and reproductive hypothalamic peptides in the desert jerboa.

Jerboa (Jaculus orientalis) is a semi-desert rodent displaying strong seasonal variations in biological functions in order to survive harsh conditions. When environmental conditions become unfavorable in early autumn, it shuts down its reproductive axis, increases its body weight, and finally hibernates. In spring, the jerboa displays opposite regulations, with a reactivation of reproduction and reduction in body weight. This study investigated how genes coding for different hypothalamic peptides involved in the central control of reproduction (Rfrp and Kiss1) and energy homeostasis (Pomc, Npy, and Somatostatin) are regulated according to seasons in male jerboas captured in the wild in spring or autumn. Remarkably, a coordinated increase in the mRNA level of Rfrp in the dorso/ventromedial hypothalamus and Kiss1, Pomc, and Somatostatin in the arcuate nucleus was observed in jerboas captured in spring as compared to autumn animals. Only Npy gene expression in the arcuate nucleus displayed no significant variations between the two seasons. These variations appear in line with the jerboa's seasonal physiology, since the spring increase in Rfrp and Kiss1 expression might be related to sexual reactivation, while the spring increase in genes encoding anorexigenic peptides, POMC, and somatostatin may account for the reduced body weight reported at this time of the year. J. Comp. Neurol. 524:3717-3728, 2016. © 2016 Wiley Periodicals, Inc.

Structure and function of the mammalian middle ear. I: Large middle ears in small desert mammals.

Many species of small desert mammals are known to have expanded auditory bullae. The ears of gerbils and heteromyids have been well described, but much less is known about the middle ear anatomy of other desert mammals. In this study, the middle ears of three gerbils (Meriones, Desmodillus and Gerbillurus), two jerboas (Jaculus) and two sengis (elephant-shrews: Macroscelides and Elephantulus) were examined and compared, using micro-computed tomography and light microscopy. Middle ear cavity expansion has occurred in members of all three groups, apparently in association with an essentially 'freely mobile' ossicular morphology and the development of bony tubes for the middle ear arteries. Cavity expansion can occur in different ways, resulting in different subcavity patterns even between different species of gerbils. Having enlarged middle ear cavities aids low-frequency audition, and several adaptive advantages of low-frequency hearing to small desert mammals have been proposed. However, while Macroscelides was found here to have middle ear cavities so large that together they exceed brain volume, the bullae of Elephantulus are considerably smaller. Why middle ear cavities are enlarged in some desert species but not others remains unclear, but it may relate to microhabitat.

Molecular assessment of Hepatozoon (Apicomplexa: Adeleorina) infections in wild canids and rodents from north Africa, with implications for transmission dynamics across taxonomic groups.

Parasites play a major role in ecosystems, and understanding of host-parasite interactions is important for predicting parasite transmission dynamics and epidemiology. However, there is still a lack of knowledge about the distribution, diversity, and impact of parasites in wildlife, especially from remote areas. Hepatozoon is a genus of apicomplexan parasites that is transmitted by ingestion of infected arthropod vectors. However, alternative modes of transmission have been identified such as trophic transmission. Using the 18S rRNA gene as a marker, we provide an assessment of Hepatozoon prevalence in six wild canid and two rodent species collected between 2003 and 2012 from remote areas in North Africa. By combining this with other predator-prey systems in a phylogenetic framework, we investigate Hepatozoon transmission dynamics in distinct host taxa. Prevalence was high overall among host species (African jerboa Jaculus jaculus [17/47, 36%], greater Egyptian jerboa Jaculus orientalis [5/7, 71%], side-striped jackal Canis adustus [1/2, 50%], golden jackal Canis aureus [6/32, 18%], pale fox Vulpes pallida [14/28, 50%], Rüppell's fox Vulpes rueppellii [6/11, 55%], red fox Vulpes vulpes [8/16, 50%], and fennec fox Vulpes zerda [7/11, 42%]). Phylogenetic analysis showed further evidence of occasional transmission of Hepatozoon lineages from prey to canid predators, which seems to occur less frequently than in other predator-prey systems such as between snakes and lizards. Due to the complex nature of the Hepatozoon lifecycle (heteroxenous and vector-borne), future studies on these wild host species need to clarify the dynamics of alternative modes of Hepatozoon transmission and identify reservoir and definitive hosts in natural populations. We also detected putative Babesia spp. (Apicomplexa: Piroplasmida) infections in two canid species from this region, V. pallida (1/28) and V. zerda (1/11).