Mandibles and molars of the wood mouse, Apodemus sylvaticus (L.): integrated latitudinal pattern and mosaic insular evolution

Aim The distinct nature of island populations has traditionally been attributed either to adaptation to particular insular conditions or to random genetic effects. In order to assess the relative importance of these two disparate processes, insular effects were addressed in the European wood mouse, Apodemus sylvaticus (Linnaeus, 1758). Location Wood mice from 33 localities on both mainland and various Atlantic and western Mediterranean islands were considered. This sampling covers only part of the latitudinal range of A. sylvaticus but included the two main genetic clades identified by previous studies. Islands encompass a range of geographical conditions (e.g. small islands fringing the continent through large and isolated ones). Methods The insular syndrome primarily invokes variations in body size, but ecological factors such as release from competition, niche widening and food availability should also influence other characters related to diet. In the present study, the morphology of the wood mice was quantified based on two characters involved in feeding: the size and shape of the mandibles and first upper molars. The size of the mandible is also a proxy for the body size of the animal. Patterns of morphological differentiation of both features were estimated using two‐dimensional outline analysis based on Fourier methods. Results Significant differences between mainland and island populations were observed in most cases for both the mandibles and molars. However, molars and mandibles displayed divergent patterns. Mandible shape diverged mostly on islands of intermediate remoteness and competition levels, whereas molars exhibited the greatest shape differentiation on small islands, such as Port‐Cros and Porquerolles. A mosaic pattern was also displayed for size. Body and mandible size increased on Ibiza, but molar size remained similar to mainland populations. Mosaic patterns were, however, not apparent in the mainland populations. Congruent latitudinal variations were evident for the size and shape of both mandibles and molars. Main conclusions Mosaic evolution appears to characterize insular divergence. The molar seems to be more prone to change with reduced population size on small islands, whereas the mandible could be more sensitive to peculiar environmental conditions on large and remote islands.     

Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation

Phenetic relationships among four Apodemus species (A. agrarius, A. epimelas, A. flavicollis and A. sylvaticus) inferred from skull (mandible and cranium) variation were explored using landmark-based geometric morphometrics. Analysis of size variation revealed that mandibles and crania of A. epimelas were the largest, followed by those of A. flavicollis, while A. agrarius and A. sylvaticus had the smallest ones. Phenetic relationships inferred from mandible shape variation better reflected phylogenetic relationships among the analyzed Apodemus species than those inferred from cranial differences. Concerning cranial shape variation, the most differentiated species was A. epimelas, whose ecology clearly differs from the other three species. Thus, differentiation of the mandible provided a pattern fully concordant with the phylogeny, while the cranium differentiation was in agreement with ecology expectations. The most evident shape changes of mandible and cranium involved the angular process and facial region, respectively. We also found that allometry had a significant influence on shape variation and that size-dependent shape variation differed among the analyzed species. Moreover, mandible and cranium are differently influenced by allometric changes. Different phenetic relationships inferred from mandible and cranium shape variation imply that phylogeny, ecology, together with factors related to size differences are all involved in the observed morphological divergence among the analyzed Apodemus species.     

Revision of the species composition of the wood mice from the genus <Emphasis Type="Italic">Sylvaemus</Emphasis> from the territory of Rostov oblast using karyological,allozyme and molecular genetic analysis

Using karyological, allozyme, and molecular genetic analysis, habitation of the four Sylvaemus wood mice species, pygmy wood mouse (S. uralensis), wood mouse (S. sylvaticus), yellow-necked mouse (S. flavicollis), and yellow-bellied mouse (S. fulvipectus) in Rostov oblast was demonstrated. Sylvaemus uralensis was distributed nearly over the whole territory of the oblast; S. sylvaticus was found in the central and western parts of the oblast on the right bank area of Don River; S. flavicollis inhabited northern and central parts of Rostov oblast on the right bank area of Don River; S. fulvipectus was found in the southern parts of the oblast, in the left bank area of Don River. Using the chromosome C-banding technique, it was demonstrated that the pygmy wood mice living in Rostov oblast in the right bank areas of Manych River and Don River in its low course, belonged to the eastern European chromosomal form of S. uralensis. The pygmy wood mice from the outskirts of the town of Salsk, the left bank area of Manych River, were probably hybrids between eastern European and southern European chromosomal forms. Based on the mitochondrial DNA cytochrome b gene fragment sequencing and chromosome C-banding, it was suggested that the wood mice inhabiting Rostov oblast belonged to the southern lineage of S. sylvaticus, living on Apennine Peninsula, Balkan Peninsula, and nearly throughout Ukraine.     

Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients

Two species of field mice, Apodemus argenteus and A. speciosus, occur in sympatry across the Japanese archipelago. The inter- and intraspecific patterns of morphological differentiation have been evaluated, using a Fourier analysis of the mandible outline. The relative importance of the effect of insular isolation and latitudinal climatic gradient on the size and shape of the two species was assessed by a comparison of the populations from the large island of Honshu and the surrounding small-island populations. The size variation in A. argenteus is correlated with the climatic gradient whilst the shape variation corresponds mainly to a random differentiation of the small-island populations from a Honshu-like basic morphological pattern. A. speciosus displays increased size on small islands, and its shape variation is related to both the climatic gradient and insularity. Finally, the two species are differentiated by both the size and shape of the mandible across the Japanese archipelago, suggesting that interspecific competition between both species is reduced via niche partitioning. Our results emphasize the importance of insular isolation on shape differentiation, but a part of the morphological differentiation is also related to the latitudinal climatic gradient. Isolation on small islands could have favoured such a response to environmental factors by lowering the gene flow that prevents almost any significant differentiation within Honshu populations.     

Evolution of MHC-<Emphasis Type="Italic">DRB</Emphasis> class II polymorphism in the genus <Emphasis Type="Italic">Apodemus</Emphasis> and a comparison of <Emphasis Type="Italic">DRB</Emphasis> sequences within the family Muridae (Mammalia: Rodentia)

Allelic diversity at major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection over long periods of time, even across multiple speciation events. Trans-species sharing of MHC alleles among genera has been supported by many studies on mammals and fish, but in rodents, the results are ambiguous. We investigated natural levels of MHC-DRB variability and evolutionary processes in the wood mouse (Apodemus sylvaticus) and the yellow-necked mouse (Apodemus flavicollis), which are common, sympatric murid rodents in European forests. Using single-strand conformation polymorphism analysis and DNA sequencing, 38 DRB exon 2 alleles were detected among 162 A. sylvaticus from nine different locations in Germany and Switzerland, and 15 DRB exon 2 alleles were detected among 60 A. flavicollis from three different locations in northern Germany. There was evidence for balancing selection in both species. Phylogenetic analysis, including additional murid taxa, showed that the DRB exon 2 sequences did not separate according to species, consistent with trans-species evolution of the MHC in these taxa.     

Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics

We analysed mandible shape of the orders Dasyuromorpha, Didelphimorphia, and Carnivora using two‐dimensional geometric morphometrics, in order to explore the relationship between shape, size, and phylogeny. We studied 541 specimens, covering most of the genera of the terrestrial Carnivora (115 species) and a wide sample of marsupials (36 species). The observed shape variation had an ecological component. As an example, omnivorous carnivores have thick mandibles and large talonids in the carnassials, while hypercarnivores possess short mandibles and reduced talonids. There is also a discrimination between different taxonomic groups (i.e. marsupials and Carnivora), indicating some kind of constraint. Size explains a large percentage of total variance (large species had shorter and stronger mandibles, with anteriorly displaced carnassials), was significant when phylogeny was taken into account with a comparative method, but not when size and shape were optimized on the phylogeny. Carnivora presents a larger disparity and variation in body size, which could be related to the difference in teeth replacement. The optimization of mandible shape on the phylogenetic tree indicates that functional aspects, such as diet, are a key factor in the evolution of the carnivore mandible, but also that there is a phylogenetic pattern that cannot be explained by differences in diet alone. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 836–855.     

Additional mandibles of Rangwapithecus gordoni,an early Miocene catarrhine from the Tinderet localities of Western Kenya

Two catarrhine mandibles and five isolated teeth have been discovered from Early Miocene localities in Western Kenya. One mandible comes from the well‐known locality of Songhor whereas the other is from a newly discovered locality, Lower Kapurtay, located near Songhor. The mandibles both can clearly be assigned to the species Rangwapithecus gordoni based on molar morphology, which is unique among Early Miocene catarrhines. The isolated specimens can be assigned to Rangwapithecus based on their similarities in morphology to the homologues preserved in the two mandibles. These specimens provide important new information about the dentognathic morphology of Rangwapithecus, which is described in detail. The mandible from Songhor (KNM‐SO 22228) represents the first definitive female mandible of Rangwapithecus. The Lower Kapurtay mandible (KNM‐KT 31234) appears to be male but is much smaller than another recently described male mandible of this species (KNM‐SO 17500) and the type maxilla (KNM‐SO 700). These specimens enable a reassessment of the attributions of all other mandibles and isolated lower teeth of Rangwapithecus, and we present a complete hypodigm of the mandibular and lower dental material for the species. Finally, we provide some additions to the diagnosis of Rangwapithecus gordoni based on previously unknown morphology. Am J Phys Anthropol 153:341–352, 2014. © 2013 Wiley Periodicals, Inc.     

A novel approach to field identification of cryptic Apodemus wood mice: calls differ more than morphology

Field identification of European wood mice Apodemus spp. is challenging due to their morphological resemblance and frequent sympatry. We developed discriminant functions based on body mass and acoustic variables of distress calls to identify three cryptic species of wood mice (Apodemus alpicola, Apodemus flavicollis and Apodemus sylvaticus) in Italy. We achieved an overall correct classification rate of 86–98%; the best results (100% correct classification) were obtained for Apodemus sylvaticus calls. This minimally invasive, effective and low‐cost method highlights the potential role of bioacoustics as a powerful tool for field discrimination of cryptic species of terrestrial mammals.     

Variation in mandible shape and body size of house mice Mus musculus in five separate New Zealand forest habitats

This study investigates variation in house mouse Mus musculus body size and mandible shape across New Zealand, using geometric morphometrics and biomechanical advantage analyses. The Mus phylogroups currently known in New Zealand include Mus musculus domesticus, M. m. musculus and M. m. castaneus. We examined samples of house mice inhabiting five different podocarp and beech forest environments across the North and South Islands (Pureora Forest, Zealandia Wildlife Sanctuary, Craigieburn Forest Park, Eglinton Valley and Hollyford Valley). Significant variation in mandible shape and body size was found between all five forest populations. South Island mice had larger bodies and greater mechanical advantage in the temporalis muscle compared with their North Island counterparts. Zealandia Sanctuary mouse mandibles were broader and shorter than South Island mouse mandibles, and had greater masseter muscle advantage. Centroid size and body weight, but not head-body length, varied significantly with two distinct genetic haplotypes. Finally, annual rainfall was the most significant covariate with mandible shape. Higher rainfall locations were generally associated with soft-food related mandible shapes, while lower rainfall correlated with hard-food mandible shapes. This preliminary investigation provides the framework for further research into mandible shape and body size variation in New Zealand house mice.     

Strong selection on mandible and nest features in a carpenter bee that nests in two sympatric host plants

Host plants are used by herbivorous insects as feeding or nesting resources. In wood‐boring insects, host plants features may impose selective forces leading to phenotypic differentiation on traits related to nest construction. Carpenter bees build their nests in dead stems or dry twigs of shrubs and trees; thus, mandibles are essential for the nesting process, and the nest is required for egg laying and offspring survival. We explored the shape and intensity of natural selection on phenotypic variation on three size measures of the bees (intertegular width, wing length, and mandible area) and two nest architecture measures (tunnel length and diameter) on bees using the native species Chusquea quila (Poaceae), and the alloctonous species Rubus ulmifolius (Rosaceae), in central Chile. Our results showed significant and positive linear selection gradients for tunnel length on both hosts, indicating that bees building long nests have more offspring. Bees with broader mandibles show greater fitness on C. quila but not on R. ulmifolius. Considering that C. quila represents a selective force on mandible area, we hypothesized a high adaptive value of this trait, resulting in higher fitness values when nesting on this host, despite its wood is denser and hence more difficult to be bored.     

Small mammals in new farm woodlands

A number of recently planted farm woodlands, along with adjacent agricultural land and hedgerows were surveyed using live traps to compare their importance for small mammals. Small mammal numbers were far higher in newly planted woodlands than in both hedgerows and agricultural land. Seven species were trapped in farm woods compared with five in hedgerows and two in agricultural land. The most frequently trapped species in the establishing woodlands was the harvest mouse Micromys minutus, followed by the wood mouse Apodemus sylvaticus. The potential importance of newly planted farm woodlands for small mammals is discussed.     

Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation

The respective roles of the phylogenetic and ecological components in an adaptive radiation are tested on a sample of Old World rats and mice (Muridae, Murinae). Phylogeny was established on nuclear and mitochondrial genes and reconstructed by maximum likelihood and Bayesian methods. This phylogeny is congruent with previous larger scale ones recently published, but includes some new results: Bandicota and Nesokia are sister taxa and Micromys would be closely related to the Rattus group. The ecological diversification is investigated through one factor, the diet, and the mandible outline provides the morphological marker. Elliptic and radial Fourier transforms are used for quantifying size and shape differences among species. Univariate size and shape parameters indicate that phylogeny is more influential on size than diet, and the reverse occurs for shape and robust patterns are recognized by multivariate analyses of the data sets provided by the Fourier methods. Omnivorous and herbivorous groups are well separated despite some overlapping, as well as are other Murinae with a specialized diet (insects, seeds). Phylogeny is also influential as shown by the segregation of several groups (Praomys, Arvicanthini, Rattus, Apodemus). Allometric shape variation was investigated, and although present it does not overwhelm effects of either phylogeny or diet. Massive mandibles characterize herbivorous Murinae and slender mandibles, the insectivorous ones. A strong angular process relative to the coronoid process characterizes seedeaters, and the reverse characterized Murinae with a diet based largely on animal matter. Such changes in morphology are clearly in relation with the functioning of the mandible, and with the forces required by the nature of the food: the need of a stronger occlusal force in herbivorous species would explain massive mandibles, and an increase of the grasping and piercing function of incisors in insectivorous species would explain slender mandibles.     

Morphological and ecological characteristics of moose, <Emphasis Type="Italic">Alces</Emphasis> cf. <Emphasis Type="Italic">alces</Emphasis> (Artiodactyla), from the southeast of Western Siberia in the Late Neopleistocene and Holocene

Fossil, subfossil, and recent materials of moose from the southeast of Western Siberia, including the remains of the skull, antlers, mandibles, and postcranial skeleton, has been analyzed. Adaptive features revealed in the structure of the mandible (a high pars dentalis) suggest that forests were a less typical habitat for ancient moose, compared to recent A. a. alces. The high pars dentalis of the mandible and the shape of antlers, with a long basal part and bifurcated spatula, are indicative of their close relation to A. americanus from Eastern Siberia. Thus, moose from the Late Neopleistocene and Holocene appear to represent the same species as A. americanus. It cannot be excluded, however, that A. cf. alces is a special type of European A. a. alces moose in which the characters convergent to Eastern Siberian A. americanus developed independently, due to habitation in similar open (forest-steppe and steppe) landscapes.     

Different patterns of retinal cone topography in two genera of rodents,Mus and Apodemus

Recently, we have reported the peculiar topographic separation of shortwave- and middlewave-sensitive (S and M) cones in the retina of the common house mouse (Mus musculus) and in a number of inbred laboratory mouse strains derived from the same species. In an attempt to follow the phylogeny of the complementary cone fields, we have investigated the retina of other mouse-like rodents. Two monoclonal anti-visual pigment antibodies, OS-2 and COS-1, specific to the S and M cones, respectively, have been used to identify the two cone types. Immunocytochemistry on retinal sections and on whole-mount preparations have shown that, as in the house mouse, the two cone types in the mound builder mouse (Mus spicileugus) occupy opposite halves of the retina. In contrast, in the wood mouse (Apodemus sylvaticus), both cone types are scattered uniformly across the whole retinal surface. Another distinguishing feature between the two genera is the frequency of the S cones. Whereas their density in the Mus species is above 7 000/mm² in the S-field, the maximum density of the S cones in A. sylvaticus is one order of magnitude smaller. In another species of this genus (the herb field mouse, A. microps), the S cones are completely missing.     

Effects of urban habitat fragmentation on common small mammals: species versus communities

There is an increasing interest in understanding how species respond to the modifications of habitat attributes in urban areas. Patterns in the occurrence and abundance of small mammal communities in 15 isolated patches of remnant natural and semi-natural habitat of Porto Metropolitan Area (Portugal) were assessed against environmental characteristics (from both the patch and the surrounding matrix) of each patch using multiple regressions and canonical correspondence analysis. Four species of common small mammals were found: wood mouse (Apodemus sylvaticus), greater white-toothed shrew (Crocidura russula), Algerian mouse (Mus spretus) and house mouse (Mus musculus). Our results showed that both relative abundance and species richness were negatively affected by urbanization. The species richness also displayed a negative association with the increase of forest around the patch but relative abundance showed the opposite trend. At the species level, the relative abundance of A. sylvaticus and C. russula showed a negative association with urbanization. Our results reveal that these two species also benefit from a mosaic of habitats and pervious areas in the surrounding matrix. The relative abundance of M. spretus and M. musculus showed a negative effect of forest area around the patch. Understanding how the increase of urbanization affects small mammals will be particularly useful for the managers of urban landscapes, as these animals occupy a pivotal position in the ecosystems.     

Changes in home range size during growth and maturation of the wood mouse (Apodemus sylvaticus) and the bank vole (Clethrionomys glareolus)

Summary A field study was carried out during winter and spring of 1982/83 to determine changes in home range size with increasing body weight and maturation in the wood mouse (Apodemus sylvaticus) and the bank vole (Clethrionomys glareolus). Individual home range sizes in males increased and in females decreased with increasing body weight. Relating these changes to changed energetic requirements failed. In these species behavioral aspects seem to be a more important determinant of home range size than body weight.     

Mitochondrial phylogeography of the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region

We sequenced 965 base pairs of the mitochondrial DNA cytochrome b from 102 woodmice (Apodemus sylvaticus) collected from 40 European localities. The aims of the study were to answer the following questions. (i) Did the Mediterranean peninsulas play a role as refuge for woodmice? (ii) Is genetic variability of A. sylvaticus higher in the Mediterranean region compared with northern Europe? (iii) Are the patterns of the postglacial colonization of Europe by woodmice similar to those presently recognized for other European species? The results provide a clear picture of the impact of the Quaternary glaciations on the genetic and geographical structure of the woodmouse. Our analyses indicate a higher genetic variability of woodmice in the Mediterranean peninsulas compared to northern Europe, suggesting a role of the former as refuge regions for this small mammal. An original pattern of postglacial colonization is proposed where the Iberian and southern France refuge populations colonized almost all European regions. The Sicilian population appears to be very differentiated and highly variable. This emphasizes the importance of this island as a ‘hot spot’ for the intraspecific genetic diversity of the woodmouse. Finally, woodmice in North Africa originated from southwestern Europe, most probably as a result of a recent anthropogenic introduction.     

Comparative study of the phylogenetic structure in six Apodemus species (Mammalia,Rodentia) inferred from ISSR-PCR data

The utility of the Inter Simple Sequence Repeat-Polymerase Chain Reaction (ISSR-PCR) was explored in order to determine genetic variation in six species of the genus Apodemus (A. flavicollis, A. sylvaticus, A. uralensis, A. agrarius, A. mystacinus and A. epimelas) at the individual level, population level, in separate geographic samples and in the species as a whole. Six optimized primers produced highly reproducible and polymorphic DNA markers with 98.3% polymorphic bands on a total sample of 91 individuals from 32 localities in Europe and Asia. Moreover, each primer allowed for an exact diagnosis of each of the six Apodemus species and thus provides a simple and reliable tool for the hitherto problematic discrimination of species from the subgenus Sylvaemus. Genetic distances between species ranged from 0.079, among the closely related A. flavicollis and A. sylvaticus, to 0.203 between A. mystacinus and A. agrarius. A. flavicollis, A. uralensis and A. sylvaticus display a strong population substructure. The range of genetic distances among geographic samples within last two species reaches the values obtained for closely related species. ISSR markers proved to be a simple and reliable tool for species diagnosis, as well as for estimating genetic diversity below the species level and for closely related species, but they showed questionable reliability for larger genetic distances.     

Ecogeographical patterns of morphological variation in pygmy shrews Sorex minutus (Soricomorpha: Soricinae) within a phylogeographical and continental‐and‐island framework

Ecogeographical patterns of morphological variation were studied in the Eurasian pygmy shrew Sorex minutus aiming to understand the species’ morphological diversity in a continental and island setting, and within the context of previous detailed phylogeographical studies. In total, 568 mandibles and 377 skulls of S. minutus from continental and island populations from Europe and Atlantic islands were examined using a geometric morphometrics approach, and the general relationships of mandible and skull size and shape with geographical and environmental variables were studied. Samples were then pooled into predefined geographical groups to evaluate the morphological differences among them using analyses of variance, aiming to contrast the morphological and genetic relationships based on morphological and genetic distances and ancestral state reconstructions, as well as assess the correlations of morphological, genetic, and geographical distances with Mantel tests. We found significant relationships of mandible size with geographical and environmental variables, fitting the converse Bergmann's rule; however, for skull size, this was less evident. Continental groups of S. minutus could not readily be differentiated from each other by shape. Most island groups of S. minutus were easily discriminated from the continental groups by being larger, indicative of an island effect. Moreover, morphological and genetic distances differed substantially and, again, island groups were distinctive morphologically. Morphological and geographical distances were significantly correlated, although this was not the case for morphological and genetic distances, indicating that morphological variation does not reflect genetic subdivision in S. minutus. Our analyses showed that environmental variables and insularity had important effects on the morphological differentiation of S. minutus.