Multimethod Approach to the Early Postnatal Growth of the Mandible in Mice from a Zone of Robertsonian Polymorphism.

The western European house mouse (Mus musculus domesticus) shows high karyotypic diversity owing to Robertsonian translocations. Morphometric studies conducted with adult mice suggest that karyotype evolution due to these chromosomal reorganizations entails variation in the form and the patterns of morphological covariation of the mandible. However, information is much scarcer regarding the effect of these rearrangements on the growth pattern of the mouse mandible over early postnatal ontogeny. Here we compare mandible growth from the second to the eighth week of postnatal life between two ontogenetic series of mice from wild populations, with the standard karyotype and with Robertsonian translocations respectively, reared under the same conditions. A multi-method approach is used, including bone histology analyses of mandible surfaces and cross-sections, as well as geometric morphometric analyses of mandible form. The mandibles of both standard and Robertsonian mice display growth acceleration around weaning, anteroposterior direction of bone maturation, a predominance of bone deposition fields over ontogeny, and relatively greater expansion of the posterior mandible region correlated with the ontogenetic increase in mandible size. Nevertheless, differences exist between the two mouse groups regarding the timing of histological maturation of the mandible, the localization of certain bone remodeling fields, the temporospatial patterns of morphological variation, and the organization into two main modules. The dissimilarities in the process of mandible growth between the two groups of mice become more evident around sexual maturity, and could arise from alterations that Robertsonian translocations may exert on genes involved in the bone remodeling mechanism. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc.

Comparative postnatal histomorphogenesis of the mandible in wild and laboratory mice.

The coordinated activity of bone cells (i.e., osteoblasts and osteoclasts) during ontogeny underlies observed changes in bone growth rates (recorded in bone histology and bone microstructure) and bone remodeling patterns explaining the ontogenetic variation in bone size and shape. Histological cross-sections of the mandible in the C57BL/6J inbred mouse strain were recently examined in order to analyze the bone microstructure, as well as the directions and rates of bone growth according to the patterns of fluorescent labeling, with the aim of description of the early postnatal histomorphogenesis of this skeletal structure. Here we use the same approach to characterize the histomorphogenesis of the mandible in wild specimens of Mus musculus domesticus, from the second to the eighth week of postnatal life, for the first time. In addition, we assess the degree of similarity in this biological process between the wild specimens examined and the C57BL/6J laboratory strain. Bone microstructure data show that M. musculus domesticus and the C57BL/6J strain differ in the temporospatial pattern of histological maturation of the mandible, which particularly precludes the support of mandibular organization into the alveolar region and the ascending ramus modules at the histological level in M. musculus domesticus. The patterns of fluorescent labeling reveal that the mandible of the wild mice exhibits temporospatial differences in the remodeling pattern, as well as higher growth rates particularly after weaning, compared to the laboratory mice. Since the two mouse groups were reared under the same conditions, the dissimilarities found suggest the existence of differences between the groups in the genetic regulation of bone remodeling, probably as a result of their different genetic backgrounds. Despite the usual suitability of inbred mouse strains as model organisms, inferences from them to natural populations regarding bone growth should be made with caution.

Variational modularity at the cell level: insights from the sperm head of the house mouse.

BACKGROUND: Modularity is an important feature in the evolvability of organisms, since it allows the occurrence of complex adaptations at every single level of biological systems. While at the cellular level the modular organization of molecular interactions has been analyzed in detail, the phenotypic modularity (or variational modularity) of cell shape remains unexplored. The mammalian spermatozoon constitutes one of the most complex and specialized cell types found in organisms. The structural heterogeneity found in the sperm head suggests an association between its inner composition, shape and specificity of function. However, little is known about the extent of the connections between these features. Taking advantage of the house mouse sperm morphology, we analyzed the variational modularity of the sperm head by testing several hypotheses related to its structural and functional organization. Because chromosomal rearrangements can affect the genotype-phenotype map of individuals and thus modify the patterns of covariation between traits, we also evaluate the effect of Robertsonian translocations on the modularity pattern of the sperm head. RESULTS: The results indicated that the house mouse sperm head is divided into three variational modules (the acrosomal, post-acrosomal and ventral spur module), which correspond to the main regions of the cytoskeletal mesh beneath the plasma membrane, i.e., the perinuclear theca. Most of the covariation is concentrated between the ventral spur and the acrosomal and post-acrosomal modules. Although the Rb fusions did not alter the main modularity pattern, they did affect the percentages of covariation between pairs of modules. CONCLUSIONS: The structural heterogeneity of the cytoskeleton is responsible for the modular organization of the sperm head shape, corroborating the role that this structure has in maintaining the cell shape. The reduction in percentages of shape covariation between pairs of modules in Rb sperms suggests that chromosomal rearrangements could induce changes in the genotype-phenotype map. Nevertheless, how these variations affect sperm fertilization success is yet to be elucidated.

Chronic exposure to environmental stressors induces fluctuating asymmetry in shrews inhabiting protected Mediterranean sites.

Many ecotoxicological studies have addressed the effects of contaminant exposure at various levels of biological organization. However, little information exists on the effects of toxicants on wildlife populations. Here we examined exposure of populations of the greater white-toothed shrew Crocidura russula (Soricomorpha, Soricidae) occupying two protected Mediterranean sites (a polluted area, the Ebro Delta, and a control site, Garraf Massif). Bioaccumulation of selected elements (Pb, Hg, Cd, Zn, Cu, Fe, Mn, Cr, Mo, Sr, Ba, and B), a body condition index (BCI) and fluctuating asymmetry (FA) were used to assess the chronic exposure to environmental pollution. BCI was correlated neither to metal concentrations nor to FA, suggesting that this fitness measure only reflects environmental disturbances at a local level. However, shrews from the polluted area showed higher concentrations of metals and metalloids (Pb, Hg, B, and Sr) and greater shape FA than specimens from the reference area. A correlation between FA was found for both first and second principal component vectors suggesting that developmental instability increases as a result of exposure to multiple pollutants. Our results corroborate the suitability of C. russula as a bioindicator of environmental quality and show that FA is an appropriate index to examine impact of developmental stressors in populations inhabiting disturbed areas.

Staggered chromosomal hybrid zones in the house mouse: relevance to reticulate evolution and speciation.

In the house mouse there are numerous chromosomal races distinguished by different combinations of metacentric chromosomes. These may come into contact with each other and with the ancestral all-acrocentric race, and form hybrid zones. The chromosomal clines that make up these hybrid zones may be coincident or separated from each other (staggered). Such staggered hybrid zones are interesting because they may include populations of individuals homozygous for a mix of features of the hybridising races. We review the characteristics of four staggered hybrid zones in the house mouse and discuss whether they are examples of primary or secondary contact and whether they represent reticulate evolution or not. However, the most important aspect of staggered hybrid zones is that the homozygous populations within the zones have the potential to expand their distributions and become new races (a process termed 'zonal raciation'). In this way they can add to the total 'stock' of chromosomal races in the species concerned. Speciation is an infrequent phenomenon that may involve an unusual set of circumstances. Each one of the products of zonal raciation has the potential to become a new species and by having more races increases the chance of a speciation event.

Cornea, retina, and lens morphology in five Soricidae species (Soricomorpha: Mammalia).

We analyzed the cornea, retina, and lens of five species of Soricidae (pygmy shrew, Sorex minutus; common shrew, Sorex araneus; Millet's shrew, Sorex coronatus; water shrew, Neomys fodiens; greater white-toothed shrew, Crocidura russula) by light and electron microscopy. In all of these species, the corneal epithelium showed a dead cell layer, which may increase the refractive power of the cornea, thereby reducing the hypermetropy that would be expected in a small eye. Moreover, the anterior surface of the lens was more curved than the posterior, thus minimizing spherical aberrations. The thicker lens and its smaller radii of curvature indicated that Sorex species and N. fodiens have a higher refractive lens power than the most nocturnal species, C. russula. In addition, only in the retina cone inner segments of the most diurnal species (genus Sorex) did we find megamitochondria that might act as microlenses to enhance the efficiency of cones. In C. russula, the scarcity of cones and the relatively small yet abundant rod nuclei were found to be consistent with its habits. The flat lens and its more anterior arrangement, together with the lack of megamitochondria in the retina of C. russula, indicated that this species has less visual acuity than the other shrews studied here.

Metal and metalloid accumulation in shrews (Soricomorpha, Mammalia) from two protected Mediterranean coastal sites.

Although ecotoxicological data on heavy metals are abundant, information on other potentially toxic elements with attributed deficiency and/or toxic disturbances is scarce. Here we quantify zinc, copper, iron, manganese, chromium, molybdenum, strontium, barium, and boron in bones of greater white-toothed shrews, Crocidura russula, inhabiting two protected Mediterranean coastal sites: the Ebro Delta, a wetland impacted by human activities, and the Medas Islands, a reference site. Natural and anthropogenic inputs significantly increase Fe, Mn, Mo, Sr, Ba, and B in specimens from the Ebro Delta, whereas Cu and Cr were higher in Medas' shrews. Principal component analysis allowed complete separation between sites along the first two axes in particular due to B, Sr, and Cu. This study provides metal reference values in bones of insectivores, explores their variability and bioaccumulation patterns in depth, and assesses the potential environmental risk and toxicity for biota exposed to the above elements.

Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation.

We quantified bioaccumulation of lead, mercury, and cadmium in bones from 105 greater white-toothed shrews (Crocidura russula) collected at the Ebro Delta, a polluted area, and the Medas Islands, a control site. Lead and mercury levels varied with site, age, and sex, although statistical significances depended on each factor. Globally, shrews from the polluted area exhibited significantly higher concentrations of Pb and Hg. Increment of Pb with age was particularly remarkable in wetland animals and was interpreted in relation to human activities, namely hunting. Unlike males, females from the Ebro Delta maintained low Hg levels, which were associated with gestation and lactation. Cadmium levels did not differ between sites, sexes, or ages. This study provides the first data on heavy metals in mammals from this wetland and suggests that C. russula is a good bioindicator of metal pollution. We concluded that sex and age may represent an important source of variation in the bioaccumulation of these metals in wild populations.

Rb(7.17), a rare Robertsonian fusion in wild populations of the house mouse.

Robertsonian (Rb) translocation is the largest source of chromosomal diversity in the western European house mouse (Mus musculus domesticus). Recently, the fusion Rb(7.17) was found in the chromosomal polymorphic zone of this subspecies in the north-east of the Iberian Peninsula. This fusion has not been reported in any other European population. Here we give data on the distribution and frequency of this mutation in this region. Results revealed that Rb(7.17) is restricted to a small geographic area, and that, in comparison with other fusions in this polymorphic zone, it occurs at low frequencies. We suggest some possible explanations for the distribution of this translocation.

Effect of Robertsonian translocations on the motor activity rhythm in the house mouse.

Here we studied the circadian rhythm of motor activity in two groups of wild house mice from the chromosomal polymorphic zone of Barcelona, which differed in diploid number (2n): standard (2n = 40), with all acrocentric chromosomes, and Robertsonian (2n = 29-32), with several Robertsonian translocations. Motor activity under three lighting conditions, light-dark cycle, constant darkness, and constant light, was recorded for each mouse. The motor activity rhythm was examined by Fourier analysis and the daily power spectra were obtained. On the basis of the mean power spectrum of each animal and under each lighting condition, stepwise discriminant analyses were performed to classify the two chromosomal groups. This method allowed the correct classification of a large number of animals, the rhythms of about 2-2.6 hour periods being the most significant, with higher values in Robertsonian than in standard mice. Our results indicate that the daily motor activity pattern differs between the two chromosomal groups and its analysis may have a valuable interest for behavioral investigations on Robertsonian polymorphic zones of this species.

Giant mitochondria in the retina cone inner segments of shrews of genus Sorex (Insectivora, Soricidae).

The retinas of three species of shrews (Sorex araneus, S. coronatus, and S. minutus) were analyzed. Two kinds of photoreceptors were identified according to (among other characteristics) the traits of the mitochondria of their inner segments. The rod inner segments contained several round or oval mitochondria distributed longitudinally inside the ellipsoid. The cone inner segment showed a few mitochondria, which we classified as megamitochondria (maximum length = 4.22 microm in S. araneus, 5.68 microm in S. coronatus, and 2.42 microm in S. minutus). An analysis of serial thin sections in S. coronatus showed that these large organelles occurred in the apical and central portions of the ellipsoid. In the peripheral and basal regions of the ellipsoid, megamitochondria were frequently accompanied by smaller mitochondria. The giant mitochondria were irregular in form and densely packed, and a reduced cytosol was observed between each mitochondria. In general, they exhibited an electron-dense matrix and a complex system of cristae, which varied in length and array. In mammalian retina, megamitochondria have only been described in the ellipsoid of the tree shrews Tupaia glis and T. belangeri, two diurnal Scandentia with a rich-cone retina. In general terms, Sorex megamitochondria are morphologically very similar to those reported for Tupaia, especially in their arrangement in the cone ellipsoid. However, they differ in the orientation of the cristae. We propose that the ellipsoid of Sorex may serve two functions: as a source of energy for receptor cells, and as a device for improving the cone outer segment optics.