Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

Data documenting skeletal development in rodents, the most species-rich ‘order’ of mammals, are at present restricted to a few model species, a shortcoming that hinders exploration of the morphological and ecological diversification of the group. In this study we provide the most comprehensive sampling of rodent ossification sequences to date, with the aim of exploring whether heterochrony is ubiquitous in rodent evolution at the onset of skeletal formation. The onset of ossification in 17 cranial elements and 24 postcranial elements was examined for eight muroid and caviomorph rodent species. New data are provided for two non-model species. For one of these, the African striped mouse, Rhabdomys pumilio, sampling was extended by studying 53 autopodial elements and examining intraspecific variation. The Parsimov method of studying sequence heterochrony was used to explore the role that changes in developmental timing play in early skeletal formation. Few heterochronies were found to diagnose the muroid and caviomorph clades, suggesting conserved patterning in skeletal development. Mechanisms leading to the generation of the wide range of morphological diversity encapsulated within Rodentia may be restricted to later periods in development than those studied in this work. Documentation of skeletogenesis in Rhabdomys indicates that intraspecifc variation in ossification sequence pattern is present, though not extensive. Our study suggests that sequence heterochrony is neither pivotal nor prevalent during early skeletal formation in rodents.     

Geometry and bone mineral density determinants of femoral neck strength changes following exercise

Physical exercise induces spatially heterogeneous adaptation in bone. However, it remains unclear where the changes in BMD and geometry have the greatest impact on femoral neck strength. The aim of this study was to determine the principal BMD-and-geometry changes induced by exercise that have the greatest effect on femoral neck strength. Pre- and post-exercise 3D-DXA images of the proximal femur were collected of male participants from the LIFTMOR-M exercise intervention trial. Meshes with element-by-element correspondence were generated by morphing a template mesh to each bone to calculate changes in BMD and geometry. Finite element (FE) models predicted femoral neck strength changes under single-leg stance and sideways fall load. Partial least squares regression (PLSR) models were developed with BMD-only, geometry-only, and BMD-and-geometry changes to determine the principal modes that explained the greatest variation in neck strength changes. The PLSR models explained over 90% of the strength variation with 3 PLS components using BMD-only (R² > 0.92, RMSE < 0.06 N) and 8 PLS components with geometry-only (R² > 0.93, RMSE < 0.06 N). Changes in the superior neck and distal cortex were most important during single-leg stance while the superior neck, medial head, and lateral trochanter were most important during a sideways fall. Local changes in femoral neck and head geometry could differentiate the exercise groups from the control group. Exercise interventions may target BMD changes in the superior neck, inferior neck, and greater trochanter for improved femoral neck strength in single-leg stance and sideways fall.

     

Pollination and breeding system of the enigmatic South African parasitic plant Mystropetalon thomii (Mystropetalaceae): rodents welcome,but not needed

• Unrelated plants adapted to particular pollinator types tend to exhibit convergent evolution in floral traits. However, inferences about likely pollinators from ‘pollination syndromes’ can be problematic due to trait overlap among some syndromes and unusual floral architecture in some lineages. An example is the rare South African parasitic plant Mystropetalon thomii (Mystropetalaceae), which has highly unusual brush‐like inflorescences that exhibit features of both bird and rodent pollination syndromes.
• We used camera traps to record flower visitors, quantified floral spectral reflectance and nectar and scent production, experimentally determined self‐compatibility and breeding system, and studied pollen dispersal using fluorescent dyes.
• The dark‐red inflorescences are usually monoecious, with female flowers maturing before male flowers, but some inflorescences are purely female (gynoecious). Inflorescences were visited intensively by several rodent species that carried large pollen loads, while visits by birds were extremely rare. Rodents prefer male‐ over female‐phase inflorescences, likely because of the male flowers’ higher nectar and scent production. The floral scent contains several compounds known to attract rodents. Despite the obvious pollen transfer by rodents, we found that flowers on both monoecious and gynoecious inflorescences readily set seed in the absence of rodents and even when all flower visitors are excluded.
• Our findings suggest that seed production occurs at least partially through apomixis and that M. thomii is not ecologically dependent on its rodent pollinators. Our study adds another species and family to the growing list of rodent‐pollinated plants, thus contributing to our understanding of the floral traits associated with pollination by non‐flying mammals.

     

Microhabitat choice and diet of rodents in Maynugus irrigation field, northern Ethiopia

An ecological study on the choice of microhabitat and diet of small mammals was carried out in Maynugus irrigation field of the Tigray region in northern Ethiopia. Abundance of rodents was high during the reproductive phase of the agricultural plants. Mastomys erythroleucus occurred more frequently in vegetable fields, whereas Arvicanthis dembeensis was more frequent in habitats with monocot plants. Scrotal males and reproductive females consumed more food by weight than abdominal males and quiescent females. Arvicanthis dembeensis consumed more food than M. erythroleucus. Both the species consumed more food during the main rainy season. All the cultivated plants were attacked by these rodents with a degree of difference in relation to season, species, sex, age and sexual condition. As rodent attack was more intense during the fruiting phase of the plants, rodent control management should be carried out during the flowering phase.     

Comparative forelimb morphology of scratch-digging and chisel-tooth digging African mole-rat species

Bathyergus suillus (Cape dune mole-rat) and Heterocephalus glaber (naked mole-rat) are two species of subterranean burrowing rodents. Bathyergus suillus occurs in soft sandy soils and is regarded as a scratch-digger, while H. glaber is found in hard, compact soils and is a chisel-tooth digging species. The present study aimed to determine musculoskeletal differences in the forelimb of these two species. The muscles of the forelimb, back and neck were dissected to the points of origin and insertion in the left and right forelimbs, B. suillus (n = 7) and H. glaber (n = 5). Dissected muscles were photographed before maceration to demonstrate muscle attachments. The scapular spine, acromion process and clavicle were relatively straight in B. suillus. In comparison a curved scapular spine, acromion process and clavicle were observed in H. glaber. In both species, the clavicle rested on the greater tuberosity of the humerus. In B. suillus, the deltoid tuberosity was prominent and situated more distally on the humeral shaft compared to the indistinct, more proximally situated deltoid tuberosity in H. glaber. A prominent bony structure underlying the thenar pad as well as a cartilaginous protrusion beneath the hypothenar pad were observed on the palmar surface of the manus in B. suillus. Prominent claws were observed in B. suillus. A robust m. sternohyoideus was observed in H. glaber while mm. tensor fasciae antebrachii and coracobrachialis were absent. The flexors of the antebrachium of B. suillus had additional and enlarged attachment sites. The forelimb of B. suillus may be morphologically adapted for scratch-digging with relatively large and additional forelimb muscles and robust bones. In comparison, H. glaber had a reduction in the relative size, amount of muscles as well as number of attachment sites in the forelimb muscles, while the well-developed ventral neck muscles may facilitate neck and head stabilisation during chisel-tooth digging.     

Sperm competition and the evolution of the sperm hook in house mice

Sperm morphology varies considerably both between and within species. The sperm of many muroid rodents bear an apical hook at the proximal end of the head. The curvature of the sperm hook varies greatly across species, however the adaptive significance of the sperm hook is currently not known. In wood mice the apical hooks intertwine to form sperm ‘trains’, which exhibit faster swimming velocities than single cells. Thus, it has been suggested that if sperm ‘trains’ were advantageous in a competitive situation, then the apical sperm hook might be an evolutionary product of selection via sperm competition. A comparative study of rodent species provided support for the hypothesis, and showed that species with higher levels of sperm competition had more reflected sperm hooks. Here, we tested this hypothesis at the intraspecific level. We quantified sperm hook morphology from seven house mouse populations, and found that interpopulation variation in hook curvature was not explained by variation in sperm competition risk. Furthermore, observations of ejaculated sperm revealed that sperm groups are not a common characteristic of mouse ejaculates. We suggest that selection for sperm attachment to the oviduct epithelium, and thus better retainment of sperm fertilizing potential, may provide a more general explanation of the evolutionary relationship between sperm competition risk and the curvature of the sperm hook among rodents, and provide a phylogenetic comparison among rodent species that supports our hypothesis.     

Development of epiphyseal structure and function in Didelphis virginiana (Marsupiala,Didelphidae)

This study addressed the question of how the epiphyses of growing mammals change their external shape and internal architecture during postnatal development. Ontogenetic transformations in the external form and internal structure of the fore‐ and hindlimb epiphyses were examined in a mixed cross‐sectional sample of Didelphis virginiana using two methods: morphometric analysis of linear epiphyseal dimensions and histological staining of serially sectioned epiphyses. Metric data indicate that Virginia opossums are born with relatively short hindlimbs and long forelimbs, but by the time they are weaned their hindlimbs are longer than their forelimbs. Functional integration of the locomotor system in D. virginiana involves a decoupling of fore‐ and hindlimb growth rates so that between birth and weaning, femoral length, diaphyseal cross‐sectional area, and articular surface area increase at a significantly faster rate than the corresponding humeral dimensions. Histological results demonstrate that these differences in growth rate are reflected in morphology of the humeral and femoral growth plate and epiphyseal cartilages. The humeral cartilages exhibit a level of cellular organization characteristic of more mature limb elements at earlier developmental stages compared to the femoral cartilages, which assume this anisotropic structure relatively later in postnatal development. Results presented here also reveal that the formation of articular cartilage and the initiation of epiphyseal ossification in D. virginiana are both correlated with the development of independent positional behaviors prior to weaning. These histological data, therefore, suggest that mechanical loading associated with the postnatal onset of locomotor and postural development may provide an important stimulus for the progression of ossification and the formation of articular cartilage in the epiphyses of growing mammals. J. Morphol. 239:283–296, 1999. © 1999 Wiley‐Liss, Inc.     

Femoral neck structure and function in early hominins

All early (Pliocene–Early Pleistocene) hominins exhibit some differences in proximal femoral morphology from modern humans, including a long femoral neck and a low neck‐shaft angle. In addition, australopiths (Au. afarensis, Au. africanus, Au. boisei, Paranthropus boisei), but not early Homo, have an “anteroposteriorly compressed” femoral neck and a small femoral head relative to femoral shaft breadth. Superoinferior asymmetry of cortical bone in the femoral neck has been claimed to be human‐like in australopiths. In this study, we measured superior and inferior cortical thicknesses at the middle and base of the femoral neck using computed tomography in six Au. africanus and two P. robustus specimens. Cortical asymmetry in the fossils is closer overall to that of modern humans than to apes, although many values are intermediate between humans and apes, or even more ape‐like in the midneck. Comparisons of external femoral neck and head dimensions were carried out for a more comprehensive sample of South and East African australopiths (n = 17) and two early Homo specimens. These show that compared with modern humans, femoral neck superoinferior, but not anteroposterior breadth, is larger relative to femoral head breadth in australopiths, but not in early Homo. Both internal and external characteristics of the australopith femoral neck indicate adaptation to relatively increased superoinferior bending loads, compared with both modern humans and early Homo. These observations, and a relatively small femoral head, are consistent with a slightly altered gait pattern in australopiths, involving more lateral deviation of the body center of mass over the stance limb. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Low individual-level dietary plasticity in an island-invasive generalist forager

The ability of invasive mammals to adjust their diet in response to new or variable resources is often proposed to explain their invasion success on islands with differing environmental conditions, especially islands with strong spatiotemporal changes in the nature and abundance of their resources. In this study, we investigated how habitat heterogeneity and seasonal fluctuation in resource quality affect dietary breadth and plasticity in an island-invasive rodent, the black rat Rattus rattus, on a small Mediterranean island. We tested for dietary plasticity of rats at both the individual and population levels by using traditional dietary and stable isotope analyses at successively increasing time scales, coupled with a long-term study of individual rats in three habitats of close proximity. Dietary and movement analyses both indicated that R. rattus is able to exploit a wide range of resources and habitats. However, dietary plasticity and habitat breadth were far narrower at the individual level. Results revealed that rats exclusively used resources found in their local habitat, and very few individuals moved among adjacent habitats in pursuit of higher-quality resources, despite those resources being abundant in their immediate environment. This counterintuitive finding suggests that intraspecific interactions must restrict rat mobility. Our results suggest that even on small islands, accessibility of patchy and high-quality resources to individuals from the entire population is not systematic. This result has important implications when quantifying invasive rodent impacts on patchily distributed species, especially when studies use indirect methods such as dietary analyses as a substitute for direct observations of predatory behavior.     

How Quaternary geologic and climatic events in the southeastern margin of the Tibetan Plateau influence the genetic structure of small mammals: inferences from phylogeography of two rodents, <Emphasis Type="Italic">Neodon irene</Emphasis> and <Emphasis Type="Italic">Apodemus latronum</Emphasis>

Phylogeographical studies that focus on the southeastern margin of the Tibetan Plateau are limited. The complex terrain and unique geological history make it a particularly unusual region of the Tibetan Plateau. We carried out a phylogeographical study of two rodent species Neodon irene and Apodemus latronum using the mitochondrial cytochrome b gene sequences. High genetic diversities and deep phylogenetic splits were detected in both rodents. Some haplotypes from one sampling region fell into different evolutionary clades, but most haplotypes from the same sampling regions were clustered together with each other. The results of isolation by distance analysis further substantiated that their genetic diversities were structured along geography. Thus, there were high levels of geographical structure for both rodents. Demographic analyses implied a relatively constant population size for all samples of N. irene and A. latronum in history. However, clade B of N. irene and clade 3 of A. latronum experienced population expansions at 105–32 and 156–47 Kya, respectively. Through comparison with previous studies, we suggest the high mitochondrial DNA diversities in them are probably not a species-specific feature, but a common pattern for small mammals in this unique area. Details of the historical demography of these rodents revealed in this study could provide new insights into how rodents and possibly other small mammals in this region responded to the geological and climatic events.     

Impacts of large mammals on movements of the pouched mouse (Saccostomus mearnsi) in central Kenya

Populations of large wild mammals are declining worldwide, while the abundance of livestock is increasing. The absence of large mammals frequently leads to increases in the abundance of small mammals such as rodents, but little is known about how the loss of large mammals affects the behaviour of small mammals. To investigate this question, we analysed long‐term data collected at the Kenya Long‐term Exclosure Experiment, which excludes different combinations of large mammals from a savannah ecosystem in central Kenya. We investigated the effects of excluding large mammals, both wild and domestic, on the movements of the pouched mouse (Saccostomus mearnsi), the most common species of small mammal in this habitat. Mice moved ~20% more in the presence of wildlife, but their movements were not significantly affected by the presence of cattle. An index of intraspecific contacts between mice was higher at higher mouse densities, and these high densities were more likely when wildlife and cattle were absent. The results suggest that the absence of large mammals led to higher densities of small mammals, which resulted in a greater probability of intraspecific contacts, despite lower average movement distances.     

Ecology of a typical West African Sudanian savannah rodent community

The small‐mammal community of a typical Sudanian savannah area of south‐eastern Senegal was studied by way of intensive sampling at the beginning (July) and at the end (November) of the rainy season. A total of 5931 trapnights and 200 pitfallnights yielded 767 small mammals, including 757 rodents of 12 species, as well as a few shrews and hedgehogs. Accumulation curve indicated that the rodent community was well sampled. Murine rodents were far more numerous than gerbilline rodents, and among them, Mastomys erythroleucus was the dominant species, being caught in high numbers in all habitats. Arvicanthis niloticus and Praomys daltoni were also abundant, followed by Mastomys natalensis and Gerbilliscus guineae. Abundances were high at the beginning of the rainy season when reproductive activity was low in all species. At the end of the rainy season, murine rodents were actively involved in reproduction, while gerbilline rodents were at their lowest density. Significant changes in relative abundance among habitats (including human dwellings) were observed between periods in some species, suggesting seasonal trends in habitat preferences. This may help species coexistence in this species‐rich rodent community, in an area likely to be submitted to significant habitat alterations in the years to come.     

New information on the postcranial skeleton of Massetognathus ochagaviae Barberena, 1981 (Eucynodontia,Traversodontidae), from the Middle Triassic of Southern Brazil

New postcranial remains of Massetognathus ochagaviae are described based on a new specimen collected at the Dinodontosaurus Assemblage Zone from the Middle Triassic of Southern Brazil. Several isolated teeth collected together with the postcranial skeleton allowed a taxonomic assignation of the specimen to M. ochagaviae. Its postcranial morphology is quite similar to Massetognathus pascuali, especially regarding the morphology of the transverse process of presacral vertebrae (i.e. laminar in the anterior most and rounded in the posterior most presacral vertebrae); humerus (i.e. the head is dorsally deflected with a ‘fan-shaped’ distal end a deltopectoral crest abruptly ending at the middle of shaft); and femur (with a bulbous and dorsomedially inclined femoral head, lesser trochanter which abruptly begins near the intertrochanteric fossa and extending up to the middle of the femoral shaft and the medial condyle more pronounced and ventrally projected than the lateral one). On the other hand, the clavicle of M. ochagaviae is less lateromedially elongated than in M. pascuali.     

Effect of gestational and postnatal environmental temperature on metabolic rate in the altricial rodent, Phyllotis darwini

1. In the altricial rodent, Phyllotis darwini, we found higher body temperatures and faster developmental rates of the thermoregulatory capacity in neonates born from cold- than warm-acclimated mothers.

2. This difference could be explained by maternal effects on the litter, such as high levels of catecholamines and thyroxin levels, high concentration of the uncoupled protein and larger quantity of brown adipose tissue as a consequence of cold acclimation.

3. The exposition of mothers and the maintenance of cold condition during the early development might be responsible of the high metabolism and better thermoregulatory capacity of newborns.

Review of negative effects of introduced rodents on small mammals on islands

In this first comprehensive review of negative effects of introduced rodents on insular small mammals, the focal species Rattus rattus, R. norvegicus, R. exulans and Mus musculus are implicated in at least 11 extinctions. Furthermore, removal experiments, eradication campaigns and control programmes provide evidence for negative effects on extant populations. While data are currently insufficient for meaningful generalisation with regard to the most threatening rodents, the most threatened small mammals, and the true extent of the problem, it is interesting that R. rattus is implicated in the majority of impacts. This may be explained by its extensive distribution and ecological plasticity. I conclude with methodological recommendations to guide data collection for impact quantification and the study of impact mechanism. This information should facilitate the prioritisation and justification of eradication campaigns, control programmes and biosecurity measures while ensuring that much-needed attention is paid to the conservation of insular small mammals.     

Species composition,abundance and habitat association of rodents and insectivores from Chilalo–Galama Mountain range,Arsi, Ethiopia

A study on the ecology of rodents and insectivores on Mount Chilalo and the Galama Mountain range was conducted during August, 2007–April, 2008. Study grids were marked in nine randomly selected habitats. Sherman live traps and snap traps were used to capture the small mammals. A total of 2525 (including recaptures) individual rodents and insectivores were captured in 5488 (Sherman) and 1590 (snap) trap‐nights. Among the live‐trapped animals, 2037 (96.2%) and 80 (3.8%) were rodents and insectivores, respectively, that comprised 17 species. These were as follows: Arvicanthis abyssinicus, Arvicanthis blicki, Arvicanthis dembeensis, Lophuromys flavopunctatus, Lophuromys melanonyx, Mastomys natalensis, Mus mahomet, Otomys typus, Rattus rattus, Stenocephalemys albipes, Stenocephalemys albocaudata, Stenocephalemys griseicauda, Crocidura glassi, Crocidura flavescens and Crocidura thalia. Tachyoryctes splendens and Hystrix cristata were sighted but not captured. Endemics to Ethiopia constituted 60% of the trapped small mammals. Lophuromys flavopunctatus was the most abundant and widely distributed rodent species, while M. mahomet was the least. The altitudes between 3301 and 3400 m asl had the highest species composition and abundance although it is second in number of catches per trap‐nights. The majority of rodents and insectivores were associated with montane forest habitat, whereas the least were in the shrubland. Anthropogenic effects were witnessed affecting the distribution of small mammals.     

Interspecific variation of sperm morphology in the Australian rodent genus Zyzomys

The sperm head morphology and tail length of two species of Australian rock rats, Zyzomys argurus and Zyzomys pedunculatus, are presented. In Z. argurus the sperm head has an apical hook together with two ventral processes extending from the upper concave surface that are largely composed of cytoskeletal material, and the sperm tail is about 135 µm in length. By contrast, in Z. pedunculatus the sperm head is paddle‐shaped with the nucleus capped by an acrosome that has a large apical segment and is surrounded by a thin layer of cytoskeletal material, and the sperm tail is only around 85 µm in length. Since the structure of the spermatozoon of Z. argurus is similar to that of most of the old endemic Australian rodents it is presumed to be the ancestral condition within the Zyzomys genus with that of Z. pedunculatus being highly derived and showing convergence with the sperm structure in some other orders of mammals.     

Structure and Evolution of the Mitochondrial DNA Complete Control Region in the Lizard Lacerta dugesii (Lacertidae, Sauria)

Abstract We sequenced the complete control region (CR) and adjacent tRNAs, partial 12S rRNA, and cytochrome b (over 3100 bp) from eight individuals of Madeiran wall lizards, Lacerta dugesii, from four distinct island populations. The tRNAs exhibit a high degree of intraspecific polymorphisms compared to other vertebrates. All CR sequences include a minisatellite that varies in length between populations but is apparently fixed within them. Variation in minisatellite length appears between populations separated by apparently very short evolutionary time spans. Many motifs identified in the CR of other vertebrates are not highly conserved, although conserved blocks are identifiable between the few published reptile CR sequences. Overall there are extensive differences in the internal organization of the reptile CR compared to the more widely studied mammals and birds. Variability in the CR is lower than in cytochrome b, but higher than in 12S rRNA. Phylogenetic analysis of these sequences produces a well-resolved estimate of relationships between populations.