Australian Rodents Reveal Conserved Cranial Evolutionary Allometry across 10 Million Years of Murid Evolution.

AbstractAmong vertebrates, placental mammals are particularly variable in the covariance between cranial shape and body size (allometry), with rodents being a major exception. Australian murid rodents allow an assessment of the cause of this anomaly because they radiated on an ecologically diverse continent notably lacking other terrestrial placentals. Here, we use 3D geometric morphometrics to quantify species-level and evolutionary allometries in 38 species (317 crania) from all Australian murid genera. We ask whether ecological opportunity resulted in greater allometric diversity compared with other rodents or whether conserved allometry suggests intrinsic constraints and/or stabilizing selection. We also assess whether cranial shape variation follows the proposed rule of craniofacial evolutionary allometry (CREA), whereby larger species have relatively longer snouts and smaller braincases. To ensure we could differentiate parallel versus nonparallel species-level allometric slopes, we compared the slopes of rarefied samples across all clades. We found exceedingly conserved allometry and CREA-like patterns across the 10-million-year split between Mus and Australian murids. This could support both intrinsic-constraint and stabilizing-selection hypotheses for conserved allometry. Large-bodied frugivores evolved faster than other species along the allometric trajectory, which could suggest stabilizing selection on the shape of the masticatory apparatus as body size changes.

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.

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.

Distributions of GABAergic and glutamatergic neurons in the brains of a diurnal and nocturnal rodent.

Light influences the daily patterning of activity by both synchronizing internal clocks to environmental light-dark cycles and acutely modulating arousal states, a process known as masking. Masking responses are completely reversed in diurnal and nocturnal species. In nocturnal rodents, masking is mediated through a subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) whose projections are similar in diurnal and nocturnal rodents. This raises the possibility that differences in responsivity to signals that these cells release might underlie chronotype differences in masking. We explored one aspect of this hypothesis by examining the distribution of excitatory and inhibitory neuronal populations in many ipRGC target areas of a diurnal species (Nile grass rat) and a nocturnal one (Norway rat). We discovered that while many of these regions were very similar in these two species, there were striking differences in the ventral lateral geniculate nucleus (vLGN; higher density of glutamate cells in Norway rats) and in the lateral habenula (LHb; GABAeric cells present in grass rats, but not Norway rats). These patterns raise the possibility that the vLGN and LHb contribute to differences in masking and/or circadian regulation of diurnal and nocturnal species.

A comparison of the orexin receptor distribution in the brain between diurnal Nile grass rats (Arvicanthis niloticus) and nocturnal mice (Mus musculus).

The neuropeptide orexin/hypocretin regulates a wide range of behaviors and physiology through its receptors OX1R and OX2R, or HCRTR-1 and HCRTR-2. Although the distributions of these receptors have been established in nocturnal rodents, their distributions in the brain of diurnal species have not been studied. In the present study, we examined spatial patterns of OX1R and OX2R mRNA expression in diurnal Nile grass rats (Arvicanthis niloticus) by in situ hybridization and compared them with those in nocturnal mice (Mus musculus). Both receptors showed similar spatial patterns between species in most brain regions. However, species-specific expression was found in several regions that are mainly implicated in regulation of sleep/wakefulness, emotion and cognition. OX1R expression was detected in the caudate putamen and ventral tuberomammillary nucleus only in grass rats, while it was detected in the bed nucleus of the stria terminalis, medial division, posteromedial part only in mice. The distribution of OX2R mRNA was mostly consistent between the two species, although it was more widely expressed in the ventral tuberomammillary nucleus in grass rats compared to mice. These results suggest that neuronal pathways of the orexin system differ between chronotypes, and these differences could underlie the distinct profiles in behaviors and physiology between diurnal and nocturnal species.

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.

Trunk and paw pad skin morphology of the African giant pouched rat (Cricetomys gambianus, Waterhouse-1840)

The gross morphology and histology of the skin of the trunk and paw pads in the African giant pouched rat were investigated to evaluate their role in the adaptation of the rodent to its subterranean environment. Samples were stained with haematoxylin and eosin, Masson’s trichrome, Alcian blue, Verhoeff's haematoxylin counterstained with Van Gieson, and Weigert’s haematoxylin counterstained with Picro-Ponceau stains. Dorsally, fur covering the skin was loosely folded. Fur covered the entire trunk to the level of the radiocarpal and talocrural joints of the forelimb and hindlimbs, respectively. Skin of the dorsum was paler than its grey-coloured fur, while skin of the ventrum was dirty white. There were more hair follicles dorsally then ventrally. The manus and pes had five and six paw pads, respectively. Keratinocytes in the epidermis of the paw pads decreased in number and lost their cellular contents as they migrated towards the stratum lucidum. Metatarsal pads had a significantly (P < 0.001) thicker stratum corneum than metacarpal pads. Elastic fibres were observed in the metatarsal pads. Other results and additional information from the literature were integrated to propose the effect of the structures on the adaptation of the African giant pouched rat to its subterranean environment and tropical climate

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Convergent evolution of aquatic foraging in a new genus and species (Rodentia: Muridae) from Sulawesi Island, Indonesia.

The island of Sulawesi, in Indonesia, lies at the crossroads of the Indo-Australian Archipelago and has remained isolated from the Asian (Sunda) and Australian (Sahul) continental shelves for at least the last 10 million years. Of the 50 native species of rodents on Sulawesi, all are endemic and represent the evolution of a variety of ecological and morphological forms within the Muridae and Sciuridae. Carnivorous rodents have evolved, perhaps independently, in Muridae from the Philippines, Sulawesi, and Sahul, but semi-aquatic murids are only known from Sahul. Here we describe a new genus and species of insectivorous water rat from Sulawesi. Phylogenetic analyses demonstrate that it is related to the shrew rats of Sulawesi and represents an origin of aquatic carnivory that is independent from the evolution of water rats on Sahul. Many areas of Sulawesi have not been surveyed systematically and current lists of mammal species are likely to dramatically underestimate actual diversity.

Ultrastructural features of vagina at different phases of the oestrous cycle in the female African giant rat (Cricetomys gambianus Waterhouse).

The ultrastructures of the vagina at various stages of the oestrous cycle in female African giant rats (Cricetomys gambianus Waterhouse) were described in the present study. At mid-proestrus, late proestrus (LP)/early estrus (EE) and mid-estrus (ME) as well as late metestrus (LM)/early diestrus (ED) and mid-diestrus (MD), complex interface of epithelium and lamina propria were observed. Cells of the stratum basale formed finger-like extensions into the underlying lamina propria and tips of the extensions displayed hemidesmosome while basal lamina followed the contour of the extensions. At mid-metestrus (MM) and late diestrus/early proestrus, well developed, relatively straight basal lamina interfaced between the stratum basale and the lamina propria without finger-like projections. Polygonal cells with indented nuclei and, cytoplasm containing ribosomes, polysomes, intermediate filaments, and mitochondria were observed in stratum spinosum at all the phases of the oestrus cycle. At MM, LM/ED, and MD, the stratum spinosum had numerous desmosomes with tonofilaments, large microvilli that intermingled at the intercellular spaces and evidence of trapped/migrating neutrophils and lymphocytes. The superficial layer displayed short microvilli at mid-proestrus, cornification at LP/EE and desquamation at ME while it showed condensation of intermediate filaments; projections of large microvilli into the luminal surface at MM, and embeddement of neutrophils at LM/ED as well as MD. This study looked into the reproductive biology of female African giant rats to produce baseline information on its reproductive organs and represented the first comprehensive description of the vagina at the ultrastructural level during oestrous cycle.

The comparative gastrointestinal morphology of five species of muroid rodents found in Saudi Arabia.

Meriones rex (King jird), Meriones libycus (Libyan jird), Acomys dimidiatus (Eastern spiny mouse), Acomys cahirinus (Egyptian spiny mouse), and Dipodillus dasyurus (Wagner's dipodil) are five species of small rodents of the superfamily Muroidea with distributions in Eastern Africa, Egypt, and the desert regions of the Arabian Peninsula. Water is scarce in these regions and may result in relatively low-digestible food. The aim of the present study is to describe and compare the gastrointestinal tract morphology and morphometry of these five species in order to elucidate whether morphology is influenced by phylogeny or dietary preference. Each segment of the gastrointestinal tract of each species was macroscopically examined and the length and basal surface area of each segment was measured. Standard histologic procedures were performed to determine a surface enlargement factor to determine the mucosal luminal surface area. A unilocular-hemiglandular stomach was observed in all the species examined. The caeca of all the species were long and arranged into a loose spiral toward the caecal tip with the ileocaecal and caeco-colic openings positioned close together. Two rows of oblique folds could be observed in the proximal colon of all species except in D. dasyurus which had longitudinal folds. Morphometric analysis showed the largest stomach in A. cahirinus and the largest caecum and colon in M. libycus. All the species can be grouped in the family Muridae in two subfamilies and similarities were observed including the hemiglandular stomach and relatively large caecum. It could be concluded that phylogeny plays an important role in determining gastrointestinal morphology while diet plays a subordinate role in the desert rodents in the present study.

Correlated changes in occlusal pattern and diet in stem Murinae during the onset of the radiation of Old World rats and mice.

Adaptive radiations in mammals are sometimes associated with the emergence of key dental innovations facilitating food processing and masticatory movements. The dietary aspects of such innovations constitute an important focus in evolutionary biology. Murine rodents, which originated during middle Miocene, currently constitute the largest extant mammalian subfamily. Their adaptive radiation combines an original chewing motion with a peculiar occlusal pattern. The fossil record clearly establishes the timing of acquisitions of those innovations, and the aim of our study was to estimate the dietary changes associated with each of them. Fossil taxa phylogenetically closest to Murinae were investigated through the use of geographic information system applied on maps obtained from first upper molars digitized by X-ray synchrotron microtomography. This methodology enables estimation of quantitative topographic descriptors of the dietary specializations of the molar crown. The peculiar forwardly directed chewing motion acquired by stem Murinae may have been a key innovation allowing the invasion of an insectivorous dietary niche. The further radiation of crown Murinae coincides with the return to the plant-dominated omnivorous dietary niche of their distant ancestors through the acquisition of new morphological traits. The retention of the forwardly directed chewing motion by the crown Murinae could have become a competitive advantage in the context of a more generalist diet.

Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013).

Recently, Balakirev et al. (2013) presented a taxonomic revision of the genus Leopoldamys based on phylogenetic analyses. They identified five main Leopoldamys genetic lineages and suggested to rename several of them. According to these authors, the genetic lineage previously thought to belong to L. edwardsi (lineage L1) should be assigned to L. revertens while L. neilli (lineage L2) should be considered as a junior synonym of L. herberti. Using molecular and morphological data from a large sampling of Leopoldamys specimens, the aim of the present study was to investigate the taxonomic status of L. herberti and L. neilli. This study reveals that, contrary to Balakirev et al.'s statement, both genetic lineages L1 and L2 occur in Nakhon Ratchasima Province, close to the type locality of L. herberti. We also show that the external measurements and color pattern of L. herberti are highly similar to those of L1 specimens but are not consistent with the morphology of L2 specimens. Therefore these results strongly suggest that L. herberti should be assigned to the genetic lineage L1. Consequently L. neilli should not be considered as a junior synonym of L. herberti and this study confirms that the appropriate name of the genetic lineage L2 is L. neilli. Moreover, as our results show that L. herberti should be assigned to the lineage L1, this name has nomenclatural priority over L. revertens, the species name suggested by Balakirev et al. (2013) for this lineage.

Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred from morphological and molecular data, with a special emphasis on the species composition in continental Indochina.

A revision of the genus Leopoldamys is presented, and both the species composition and distribution in Indochina and Sundaic regions is reinvestigated. The phylogeny of the genus is recovered based on Cyt b, COI, and IRBP gene analyses. Five basal and 16 secondary monophyletic phylogenetic lineages were identified. A taxonomic reassessment of the continental and Sundaic populations is performed based on morphological verification of the genetically defined clades. Six clades were recovered in the phylogenetic analyses and correspond to morphologically defined species: L. revertens (distributed in lowlands of eastern and central Indochina), L. herberti (western and central Indochina, northward to northern Vietnam), L. edwardsi (China and northern Vietnam, northward of 21 degrees N), L. milleti (endemic of Dalat Plateau, southern Vietnam), L. sabanus (Borneo), and L. vociferans (lowlands of the Malacca Peninsula, northward to southwestern Thailand). The absence of proper L. sabanus in continental Indochina is revealed. The substitute name for the species known from the majority of Indochina under the name of L. sabanus should be L. revertens. The name L. neilli, which has been ascribed to populations from Thailand and Vietnam, is a junior synonym of L. herberti. Two related but rather divergent clades are found in Sumatra and the Malacca Peninsula. Based on their considerable genetic distances, these forms should be regarded as separate species from the L. sabanus type-bearing populations of Borneo, or as the members of L. sabanus polytypic superspecies. The substitute name for the lineage-bearing taxon from Malacca should be L. vociferans. The continental populations of Leopoldamys can be distinguished from each other by external and cranial characters and may be subdivided into four species. Two of these species (L. revertens and L. milleti) are well distinguished by external and cranial morphology, whereas the other two species (L. herberti and L. edwardsi) may be treated as sibling species that are difficult to distinguish based on morphological characters.

[Correspondence analysis and combination of molecular genetic and morphological data in zoological systematics].

A new algorithmic approach is proposed for correspondence analysis of different types of data in zoological systematics. The algorithm is tested on actual data. A high degree of correspondence is shown for morphometric and genetic distances in the tested set of species. Two directions of variation in both character spaces have clearly appeared. The first direction discriminates families; the second discriminates orders. The characters responsible for these differences have been revealed. After uniting both distance matrixes, the morphological one and the molecular genetic one, into a single matrix, and displaying the summarized distances between species on a plane, the configuration of species remained principally unchanged. The principal directions of variations were preserved and marked the differences between orders, families, and genera.

Reproductive and metabolic responses of desert adapted common spiny male mice (Acomys cahirinus) to vasopressin treatment.

Sufficient amounts of water and food are important cues for reproduction in an unpredictable environment. We previously demonstrated that increased osmolarity levels, or exogenous vasopressin (VP) treatment halt reproduction of desert adapted golden spiny mice Acomys russatus. In this research we studied gonad regulation by VP and food restriction (FR) in desert adapted common spiny mouse (A. cahirinus) males, kept under two different photoperiod regimes-short (SD-8L:16D) and long (LD-16L:8D) days. Mice were treated with VP, FR, and VP+FR for three weeks. Response was assessed from changes in relative testis mass, serum testosterone levels and mRNA receptor gene expression of VP, aldosterone and leptin in treated groups, compared with their controls. SD-acclimation increased testosterone levels, VP treatment decreased expression of aldosterone mRNA receptor in the testes of SD-acclimated males. FR under SD-conditions resulted in testosterone decrease and elevation of VP- receptor gene expression in testes. Aldosterone receptor mRNA expression was also detected in WAT. These results support the idea that water and food availability in the habitat may be used as signals for activating the reproductive system through direct effects of VP, aldosterone and leptin on the testes or through WAT by indirect effects.

A poisonous surprise under the coat of the African crested rat.

Plant toxins are sequestered by many animals and the toxicity is frequently advertised by aposematic displays to deter potential predators. Such 'unpalatability by appropriation' is common in many invertebrate groups and also found in a few vertebrate groups. However, potentially lethal toxicity by acquisition has so far never been reported for a placental mammal. Here, we describe complex morphological structures and behaviours whereby the African crested rat, Lophiomys imhausi, acquires, dispenses and advertises deterrent toxin. Roots and bark of Acokanthera schimperi (Apocynaceae) trees are gnawed, masticated and slavered onto highly specialized hairs that wick up the compound, to be delivered whenever the animal is bitten or mouthed by a predator. The poison is a cardenolide, closely resembling ouabain, one of the active components in a traditional African arrow poison long celebrated for its power to kill elephants.

Late Miocene insular mice from the Tusco-Sardinian palaeobioprovince provide new insights on the palaeoecology of the Oreopithecus faunas.

Oreopithecus bambolii is one of the few hominoids that evolved under insular conditions, resulting in the development of unique adaptations that have fueled an intensive debate. The palaeoenvironment associated with this great ape has been the subject of great controversy as well. On the one hand, palaeobotanical data indicate that Oreopithecus likely inhabited mixed mesophytic forests interrupted by swamps; on the other hand, an abundance of hypsodont bovids points towards the existence of dry and open environments. Here, we provide a new approach based on the ecomorphology of the extinct endemic Muridae (rats and mice) of the so-called Oreopithecus faunas. Our results show that the successive species of endemic insular murids (Huerzelerimys and Anthracomys) evolved a number of adaptations observed only in extant family members that include significant proportions of grass in their diet. While this fits the pattern exhibited by large mammals, it contrasts with the available palaeobotanical information, which indicates that grasses were minor components of the vegetation. This contradiction may be explained because these endemic murids may have been adapted to the consumption of particular food items such as hard parts of aquatic plants (as shown by some extant murid species). However, because it is unlikely that the remaining herbivore mammals were adapted to this diet as well, we favour an alternative hypothesis that takes into account the peculiar ecological conditions of insular ecosystems leading to a density-dependent selective regime with strong competition. Such a regime would promote the selection of dental adaptations to increase feeding efficiency and durability of the dentition (such as hypsodonty) as seen in some fossil insular ruminants. This hypothesis requires further testing, but may partly account for parallel evolution of dental traits in phylogenetically unrelated insular mammals.

Biometric and morphologic studies of the female reproductive organs of the African giant rat (Cricetomys gambianus: Waterhouse).

Different segments of the reproductive tract of 100 adult, non-pregnant, female African giant rats (AGR) were carefully examined, weighed, and measured. The ovaries were observed to be small, pinkish, and kidney-shaped. The uterus of the AGR was found to be uterus duplex. The live weight of the AGR was 999.7 ± 16.86 g. The weight, length, and width of the ovary were 0.095 ± 0.003 g, 0.750 ± 0.01 cm, and 0.01± 0.02 cm, respectively. The length of the oviduct, uterus, and vagina/vestibule were 4.44 ± 0.06 cm, 4.877 ± 0.11 cm, and 4.345 ± 0.07 cm, respectively. The weight and length of the entire tubular organs were 3.171 ± 0.01 g and 13.559 ± 0.18 cm with corresponding range values of 1.61-7.10 g and 7.80-17.40 cm, respectively.