Sound communication in social voles (subgenus Sumeriomys)

ABSTRACT

The acoustic communication of three species of social voles from the subgenus Sumeriomys – Microtus socialis (two subspecies: M. s. socialis and M. s. goriensis), M. paradoxus and M. hartingi – are described. Vole sound communication includes two main signals: squeaks and singing. The sounds made by M. hartingi have significantly higher frequency parameters than those of other species. Voles of all species squeak in situations of distress, and the males sing during courtship of the females. However, singing in social voles is not a necessary pattern for sexual behaviour: less than half of M. s. socialis and M. paradoxus males sang, M. hartingi sang even more rarely and M. s. goriensis did not demonstrate this behaviour at all. Despite the great similarity of the squeaks, its parameters differ significantly between species and differ from those of the common voles. This introduces one more argument that M. paradoxus and M. socialis are independent species, as are the subgenera Sumeriomys and Microtus.     

Distribution and survival of the social vole in a clayey semidesert of the Trans-Volga region

The social vole (Microtus socialis Pall.) is a landscape species of the Trans-Volga clayey semidesert, which disappeared from the zonal plain in the 1970s but survived in various habitats of lake depressions. In 2009, it settled over the blind plain again. The reasons for the departure and then return of the vole are not known. This phenomenon might be one of the cyclic changes in the specific composition and abundance, which are characteristic of many animals of this region.     

New insights into the taxonomy and phylogeny of social voles inferred from mitochondrial cytochrome b sequences

We sequenced the entire cytochrome b gene in Microtus paradoxus from Turkmenistan and Microtus socialis from Crimea and Kalmykia. Phylogenetic relationships among social voles were reconstructed by the inclusion into analyses of a further 23 published haplotypes belonging to six species. The two probabilistic methods which were used in phylogenetic analyses, the Bayesian inference and Maximum Likelihood, yielded very similar results. Both trees showed two highly divergent lineages which were further subdivided into seven species. The socialis lineage encompassed four species (M. socialis, M. irani, M. anatolicus, and M. paradoxus), and the remaining three species clustered into the guentheri lineage (M. guentheri, M. hartingi, M. dogramacii). The ranges for nucleotide divergences between seven species of social voles (4.95–9.28% and 4.18–8.81% for mean and net divergences, respectively) mainly exceeded 4.3%, which is frequently regarded as the conservative cut-off between sibling species in the specious genus Microtus.     

Pair-bonding and parental care in cricetid rodents: a comparative study

The cricetid rodents (hamsters, voles, and gerbils) show substantial inter-specific variation in their social organization, mating strategies, and patterns of social behavior, including parental care. In the present study, behaviors related to pair-bonding and parental activities were evaluated in male–female pairs of six cricetid species (Cricetulus migratorius Pallas, 1773, Clethrionomys rutilus Pallas, 1779, Microtus arvalis Pallas, 1778, Microtus socialis Pallas, 1773, Lasiopodomys brandti Radde, 1852, and Meriones unguiculatus Milne-Edwards, 1867) observed under laboratory conditions. These species were chosen due to particular differences in their mating strategies and the spatial-and-ethological population structure (Types I–IV). The results of the study show that there is a pronounced tendency towards both reinforcement of pair-bonds and increasing rate of direct parental care, especially paternal one, when solitary or gregarious species (Types I and II—C. migratorius and C. rutilus) are compared with the ones living in family groups (Type III—M. arvalis and M. socialis and Type IV—L. brandti and M. unguiculatus). Parental investment of males is mainly related to additional tactile stimulation of infants. A high level of tactile stimulation of pups promotes an increase in subsequent paternal care and reinforcement of pair-bonding, and, conversely, a deficit of tactile stimulation negatively affects the development of paternal behavior and social relationships. Thus, tactile stimulation can be regarded as one of the proximate mechanisms of socialization that plays an essential role in the evolution of sociality, i.e., transition to a family-group mode of life in rodents.     

DIFFERENTIAL EFFECTS OF PHOTOPHASE IRRADIANCE ON METABOLIC AND URINARY STRESS HORMONE CONCENTRATIONS IN BLIND AND SIGHTED RODENTS

The effects of different photophase irradiance levels on the daily rhythms of energy expenditure (DEE, calculated from oxygen consumption, VO₂) and urinary metabolites of stress hormones in sighted (Microtus socialis) and blind (Spalax ehrenbergi) rodents were compared. Five groups of each species were exposed to different irradiance levels (73, 147, 293, 366, and 498 μW/cm²) under short photoperiod (8L:16D) condition with constant ambient temperature 25?±?2°C for 21 days before assessments. As light intensity increased from 73 μW/cm², both species reduced DEE, especially among M. socialis. Cosinor analysis revealed significant ultradian rhythms in VO₂ of M. socialis with period length being inversely related to irradiance level. Conversely, in S. ehrenbergi, robust 24 h VO₂ rhythms were detected at all irradiances. In M. socialis, significant 24 h rhythms in urinary output of adrenaline were detected only at 293 μW/cm², whereas for cortisol, unambiguous rhythms were detected at 73 and 147 μW/cm². Distinct adrenaline daily rhythms of S. ehrenbergi were observed at 73 and 293 μW/cm², whereas this species exhibited significant rhythms in cortisol at 147 and 293 μW/cm². Changes in photophase irradiance levels affected stress hormone concentrations in a dose-dependent manner. There were significant negative and positive correlations of M. socialis and S. ehrenbergi stress hormones, respectively, with increasing irradiance. Our results indicate photophase light intensity is another environmental factor that can significantly affect entrainment of mammalian daily rhythms. Both low and high irradiance conditions can trigger stress responses, depending on the species' natural habitat. (Author correspondence: zubidat3@013.net.il)     

Geomorphometric differences among four species of Microtus in Turkey (Mammalia: Rodentia)

In order to determine the phenotypic associations of four morphologically similar species of Microtus occurring in Turkey, we applied landmark-based shape analysis. The skulls of Microtus anatolicus, M. dogramacii, M. guentheri and M. levis (= M. rossiaemeridionalis) were found to differ significantly in terms of both size and shape. M. guentheri had the biggest skull, while M. levis had the smallest. Sexual dimorphism was found in the shape of the skull in M. dogramacii and M. levis. The tympanic bulla area is enlarged in M. anatolicus compared to the other species. Mahalanobis distances (the distance between a point and the group mean, taking into account the within-group covariance-variance matrix) confirm the distinction of the arvalis group (M. levis) and socialis group (Microtus anatolicus, M. dogramacii, M. guentheri).     

Chromosomal variation in social voles: a Robertsonian fusion in Günther’s vole

The study reports on chromosomes in several populations of social voles from south-eastern Europe and the Middle East. The standard karyotypes of individuals of Microtus hartingi and Microtus guentheri originating from both south-eastern Europe and Asia Minor comprised 54 mostly acrocentric chromosomes. However, variation between populations was found in the amount and distribution of C-heterochromatin in certain autosomes and the sex chromosomes. Furthermore, a specific pattern of argyrophilic nucleolar organizer region distribution was recorded in different geographic populations. In a population from Asia Minor, a heterozygous centric fusion of two autosomes was found. The G-banded karyotypes of M. guentheri and Microtus socialis were compared, and tandem fusions of autosomes were suggested as possible mechanism of the divergence. The karyotypes of the nine currently recognized species of social voles are reviewed, and implications of chromosomal data for systematics are evaluated.     

Experimental hybridization of voles of the genus Microtus s.l. M. socialis with species of the group arvalis (Mammalia,Rodentia)

The results of interspecific crosses of the social vole Microtus socialis with the Altai vole M. obscurus, the East European vole M. rossiaemeridionalis, and the Transcaspian vole M. transcaspicus are presented. The role of the sperm head structure in the reproductive isolation of this species was studied. Hybrids were obtained in five of the six crossing combinations. It is established that significant differences in the sperm head shape in the social vole and in arvalis group species do not prevent fertilization. The sterility of hybrids indicates the existence of postcopulative mechanisms of reproductive isolation.     

Neuromuscular organization of the freshwater colonial rotifer, Sinantherina socialis, and its implications for understanding the evolution of coloniality in Rotifera

Coloniality among rotifers is rare, and while the adaptive significance of the lifestyle has been explored previously, there are few details about how it may have influenced the morphology of colony members. In this study, we use confocal laser scanning microscopy combined with cyto- and immunohistochemistry to determine if the colonial rotifer, Sinantherina socialis, differs in neuromuscular organization relative to other colonial and solitary forms. Our observations indicate that the patterns of serotonergic neurons and somatic muscles in S. socialis are broadly similar to other rotifers. At the neuronal level, the distribution of serotonergic (5HT-IR) neurons in S. socialis is most similar to colony-forming species of Conochilus: (1) paired nerve cords extend the length of the body; (2) the cerebral ganglion innervates the corona with paired neurites that form a neuronal ring; and (3) a single pair of neurites innervates the ventral sensory antennae. Unique to S. socialis is the presence of two additional neuronal rings that supply the corona and may function to modulate ciliary beat. At the muscular level, S. socialis displays a typical pattern of somatic muscle organization similar to other rotifers, but diverges from the pattern in three significant ways: (1) somatic circular muscles form complete rings; (2) circular muscles are distinguishable based on their size and position in the body; and (3) transverse muscles are present within the corona and presumably function to modify its shape for feeding and defensive purposes. These differences in neuromuscular organization may be adaptations to the colonial and/or sessile lifestyle, both of which are characteristic of S. socialis.     

Two new species in the Chaetoceros socialis complex (Bacillariophyta): C. sporotruncatus and C. dichatoensis,and characterization of its relatives,C. radicans and C. cinctus

The diatom genus Chaetoceros is one of the most abundant and diverse phytoplankton in marine and brackish waters worldwide. Within this genus, Chaetoceros socialis has been cited as one of the most common species. However, recent studies from different geographic areas have shown the presence of pseudo‐cryptic diversity within the C. socialis complex. Members of this complex are characterized by curved chains (primary colonies) aggregating into globular clusters, where one of the four setae of each cell curves toward the center of the cluster and the other three orient outwards. New light and electron microscopy observations as well as molecular data on marine planktonic diatoms from the coastal waters off Chile revealed the presence of two new species, Chaetoceros sporotruncatus sp. nov. and C. dichatoensis. sp. nov. belonging to the C. socialis complex. The two new species are similar to other members of the complex (i.e., C. socialis and C. gelidus) in the primary and secondary structure of the colony, the orientation pattern of the setae, and the valve ultrastructure. The only morphological characters that can be used to differentiate the species of this complex are aspects related to resting spore morphology. The two newly described species are closely related to each other and form a sister clade to C. gelidus in molecular phylogenies. We also provide a phylogenetic status along with the morphological characterization of C. radicans and C. cintus, which are genetically related to the C. socialis complex.     

Effects of cassava varietal mixtures on the whiteflies Aleurotrachelus socialis and Trialeurodes variabilis in Colombia

The effects of cassava varietal mixtures on the population dynamics of the whiteflies Aleurotrachelus socialis Bondar and Trialeurodes variabilis (Quaintance) were investigated under outbreak conditions in Colombia. A regional variety of cassava (MCOL 2257) was grown in pure stand and mixed with a variety, CMC 40, believed to have partial resistance to T. variabilis. The dominant species in the systems, A. socialis, showed no varietal preference and population levels on the regional cultivar were similar between treatments. Of the two cultivars, CMC 40 was less preferred by T. variabilis and its presence in mixed variety plots lowered populations on the regional cassava. Yield losses, primarily due to A. socialis, were equal for regional cassava mixed with CMC 40 and in pure stand. Nevertheless, the use of CMC 40 in varietal mixtures provides a potential strategy for lowering herbivore load and increasing yields in zones with heavy T. variabilis attack.

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Résumé L'influence du mélange de différentes variétés de manioc sur A. socialis Bondar et T. variabilis Quaintance a été examinée dans des conditions de pullulation en Colombie. Une variété régionale (MCOL 2257) a été cultivée seule ou mélangée avec une variété (CMC 40), considérée comme ayant une résistance partielle à T. variabilis. A. socialis, espèce dominante dans la biocénose, n'a pas montré de préférence variétale et son niveau de population sur MCOL 2557 était le même quelles que soient les conditions de culture. T. variabilis a moins préféré CMC 40, dont la présence en culture mixte a réduit le niveau des populations sur manioc local. Les dégâts sur CMC 40, dus d'abord à A. socialis, ont été les mêmes, qu'il ait été seul ou mélangé à MCOL 2257. Les dégats sur MCOL 2257, dus avant tout à A. socialis ont été les mêmes en culture pure ou en mélange avec CMC 40. Quoi qu'il en soit, la culture de CMC 40 en association variétale constitue une méthode qui abaisse potentiellement le fardeau des herbivores en augmentant les récoltes dans les zones à forte contamination par T. variabilis.

     

Urea Recycling in Muroid Rodents

The results of urease activity studies in the digestive tract of muroid rodents Microtus socialis and Meriones meridianus are considered. It was noted that the absolute values of urease activity turned out to be comparable with those of lagomorphs, but were less than the results obtained for ungulates. The pronounced postgastric character of urealytic fermentation was shown. The possibility of significant urea recycling in muroid rodents aimed at compensating for dietary nitrogen deficiency and water conservation is considered.     

GLANDULAR HAIRS IN THE ARBUTUS XALAPENSIS COMPLEX IN RELATION TO HERBIVORY

The morphological boundaries between Arbutus xalapensis and A. glandulosa are diffuse. Many individuals share traits of both species. The character most commonly used to distinguish the species is the presence of glandular hairs in A. glandulosa. Comparisons in the field of the number of colonies and level of defoliation by Eucheira socialis (Lepidoptera, Pieridae), an Arbutus-specific herbivore, showed that the damage is greater for glabrous than pilose trees and greater for pilose than glandular trees. Additionally, the geographic distribution of glandular trees is strongly correlated with that of E. socialis while that of non-glandular trees is not. We suggest that the glandular and non-glandular forms could belong to one single polymorphic species in which the glandular characteristic is maintained by differential herbivory.     

Inflated organelle genomes and a circular-mapping mtDNA probably existed at the origin of coloniality in volvocine green algae

The volvocine lineage is a monophyletic grouping of unicellular, colonial and multicellular algae, and a model for studying the evolution of multicellularity. In addition to being morphologically diverse, volvocine algae boast a surprising amount of organelle genomic variation. Moreover, volvocine organelle genome complexity appears to scale positively with organismal complexity. However, the organelle DNA architecture at the origin of colonial living is not known. To examine this issue, we sequenced the plastid and mitochondrial DNAs (ptDNA and mtDNA) of the 4-celled alga Tetrabaena socialis, which is basal to the colonial and multicellular volvocines.

Tetrabaena socialis has a circular-mapping mitochondrial genome, contrasting with the linear mtDNA architecture of its relative Chlamydomonas reinhardtii. This suggests that a circular-mapping mtDNA conformation emerged at or near the transition to group living in the volvocines, or represents the ancestral state of the lineage as a whole. The T. socialis ptDNA is very large (>405 kb) and dense with repeats, supporting the idea that a shift from a unicellular to a colonial existence coincided with organelle genomic expansion, potentially as a result of increased random genetic drift. These data reinforce the idea that volvocine algae harbour some of the most expanded plastid chromosomes from the eukaryotic tree of life. Circular-mapping mtDNAs are turning out to be more common within volvocines than originally thought, particularly for colonial and multicellular species. Altogether, volvocine organelle genomes became markedly more inflated during the evolution of multicellularity, but complex organelle genomes appear to have existed at the very beginning of colonial living.     

Documenting the biogeographic history of Microtus cabrerae through its fossil record

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