A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus,the pine vole M. pinetorum and the prairie vole M. cchrogaster

Paternal care in microtines has been studied infrequently and few studies have compared patterns of direct and indirect paternal investment. The paternal behaviour of three vole species, the meadow vole (Microtus pennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster) was examined in a semi-natural setting. Prairie and pine voles were found to exhibit high levels of paternal care. Prairie vole males contributed the most direct care by remaining in the natal nest for long periods of time in contact with the pups. Pine voles contributed less direct care than prairie voles as they spent less time in the natal nest with their offspring. In addition, both prairie and pine vole males were observed to groom their pups and retrieve them back to the nest area. Prairie vole males also engaged in such indirect forms of care as nest construction and maintenance, while pine voles provided indirect care in the form of tunnel construction and food caching. Meadow vole males were the least paternal of the three species and rarely engaged in either direct or indirect care. These findings support predictions that M. pennsylvanicus is promiscuous and that male and female meadow voles occupy separate territories. They are also consistent with studies which indicate that prairie and pine voles are monogamous and have a structured social organization with members interacting closely with one another.     

布氏田鼠的双亲行为比较

在实验室对布氏田鼠双亲行为和幼仔发育的研究表明, 雌性布氏田鼠的修饰、筑巢和摄食行为显著地多于雄鼠, 且这些差异多集中在幼仔发育的最初9 d 内。雌鼠的修饰、筑巢行为以及在巢内的时间与幼仔发育日龄呈显著地负相关, 而雄鼠的这些行为无显著变化。但雌雄的衔回行为却与幼仔发育日龄呈显著地正相关。据此认为雌性布氏田鼠的双亲行为多于雄鼠, 符合双亲投资的理论。     

Sexual maturation and age-related dynamics of corticosterone in Clethrionomys rutilus and Cl. rufocanus voles (Rodentia, Cricetidae) under experimental conditions

Differences in the mechanisms regulating reproduction between the northern red-backed vole (Clethrionomys rutilus) and large-toothed red-backed vole (Cl. rufocanus) have been revealed under vivarium conditions. In Cl. rufocanus, the date of birth is the most important ??signal?? factor for sexual maturation of male young of the year, while the effect of population density is significant only for males of the spring generation. Males of the summer generation fail to mature in the same year and are completely excluded from reproduction, which may be accounted for by a rise in the level of corticosterone (measured in fecal samples). Such a mechanism for regulating the numbers of reproductive individuals is absent in Cl. rutilus voles. Throughout the breeding season, males of this species respond to high population density by a decrease in the rate of sexual maturation. No definite relationship between sexual maturation and the level of adrenocortical activity has been revealed in Cl. rutilus.     

Gene conversion in the mitochondrial genome on interspecific hybridization in voles of the <Emphasis Type="Italic">Clethrionomys</Emphasis> genus

The phenomenon of interspecific hybridization accompanied by transfer of the mitochondrial genome from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (Cl. glareolus) in northeastern Europe is well known already for 25 years. However, the possibility of recombination between homologous segments of maternal and paternal mtDNAs of the voles during fertilization was not previously studied. Analysis of data on variability of nucleotide sequences of the mitochondrial gene for cytochrome b in populations of red-backed and bank voles in the area of their sympatry has shown that as a result of interspecific hybridization, the mitochondrial gene pool of bank voles contains not only mtDNA haplotypes of red-backed vole females, but also mtDNA haplotypes of bank voles bearing short nucleotide tracts of red-backed vole mtDNA. This finding supports the hypothesis that an incomplete elimination of red-backed vole paternal mtDNA during the interspecific hybridization between bank vole females and red-backed vole males leads to the gene conversion of bank vole maternal mtDNA tracts by homologous ones of mtDNA of red-backed vole males.     

Changes in Paternal Responsiveness of Prairie Voles (Microtus ochrogaster) in Response to Olfactory Cues and Continuous Physical Contact with a Female

In mammals, paternal care is rarely displayed, and we know little about the mechanisms regulating this behavior. Prairie voles (Microtus ochrogaster) are ideal mammals for the study of paternal behavior because they are a monogamous, bi‐parental species that is easily raised in the laboratory. Paternal responsiveness occurs at moderate levels in sexually‐naive voles and is heightened following a short cohabitation period of 72 h with a female. To determine how increased levels of paternal care are maintained after the initial cohabitation period, we tested the paternal behavior of males that were housed in isolation, were in physical contact with a female, or were exposed to various olfactory cues. The results indicate that the absence of odor cues from a female did not diminish the male’s motivation to care for infants following the initial cohabitation period. In contrast, odor cues from a male appeared to negatively influence the male’s paternal tendencies. The data also show that males that had continuous physical contact with a female spent more time responding paternally and more time hovering over the young compared to males that were housed alone. Together, these results suggest that although paternal behavior is maximized in response to continuous physical contact with females, olfactory cues may not be necessary for the maintenance of heightened paternal behavior.     

Genetic variation and phylogeography of the bank vole (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>, Arvicolinae,Rodentia) in Russia with special reference to the introgression of the mtDNA of a closely related species,red-backed vole (<Emphasis Type="Italic">Cl. rutilus</Emphasis>)

Totally, 294 bank voles (Clethrionomys glareolus) and 18 red-backed voles (Cl. rutilus) from 62 sites of European Russia were studied. Incomplete sequences (967 bp) of the mitochondrial cytochrome b gene were determined for 93 Cl. glareolus individuals from 56 sites and 18 Cl. rutilus individuals from the same habitats. Analysis of the cytochrome b gene variation has demonstrated that practically the entire European part of Russia, Ural, and a considerable part of Western Europe are inhabited by bank voles of the same phylogroup, displaying an extremely low genetic differentiation. Our data suggest that Cl. glareolus very rapidly colonized over the presently occupied territory in the post-Pleistocene period from no more than two (central European and western European) refugia from ancestral populations with a small effective size. PCR typing of the mitochondrial cytochrome b gene allowed us to assess the scale of mtDNA introgression from a closely related species, Cl. rutilus, and to outline the geographical zone of this introgression. Comparison with the red-backed vole haplotypes in the habitats shared by both species favors the hypothesis of an ancient hybridization event (mid-Holocene) and a subsequent introgression. These results suggest that the hybridization took place in the southern and middle Pre-Ural region.     

Central Vasopressin Administration Regulates the Onset of Facultative Paternal Behavior in Microtus pennsylvanicus (Meadow Voles)

Pharmacological experiments have implicated a role for central arginine vasopressin (AVP) in regulating paternal behavior in monogamous prairie voles. Although nonmonogamous meadow voles exhibit appreciable paternal care when housed under winter, short day lengths (SD), no research has examined whether the same neurobiological systems are involved in regulating paternal behavior in a nonmonogamous species when it behaves paternally. The goal of these experiments was to determine whether central administration of AVP, but not cerebrospinal fluid (CSF), affected the suppression of pup-directed aggression and/or the onset of paternal behavior in meadow voles. Data from experiment 1 implicated a role for AVP in facilitating changes in male behavior: central administration of 1 ng of AVP (but not 3 ng or CSF) inhibited pup-directed aggression in previously pup-aggressive males, and 3 ng of AVP (but not 1 ng or CSF) induced paternal behavior in previously nonpaternal males. In contrast, AVP (1 and 3 ng) did not enhance paternal behavior in already paternal males. Experiment 2 tested the specificity of AVP. Previous research indicated that 24 h of unmated cohabitation with a female reliably induced paternal behavior in SD males. Hence, experiment 2 examined whether administration of a V_1a AVP antagonist (AVPA), but not CSF, prior to 24 h of unmated cohabitation would block the onset of paternal behavior. Males that received CSF displayed paternal behavior faster and engaged in more investigatory and paternal behaviors than males that received AVPA. Thus, pharmacological experiments support the hypothesis that AVP likely regulates paternal behavior in both facultatively and consistently paternal vole species.     

Gene-Geographic Variation and Genetic Differentiation in Red-Backed Voles of the Genus Clethrionomys (Rodentia,Cricetidae) from the Region of the Sea of Okhotsk

Thirteen enzyme systems and three nonenzyme proteins were electrophoretically analyzed in red-backed voles of the genus Clethrionomys. In total, 25 loci were interpreted. Gene-geographic variation was studied and indices of genetic variability and differentiation were determined. By the distribution of electrophoretic variants of hemoglobin, C. rutilus was shown to be divided into two geographical groups (northern and southern). A low level of genetic differentiation was revealed in the island isolates of C. rutilus and C. rufocanus. Separation of C. rufocanus, C. rex, and C. sicotanensisinto a superspecies complex was confirmed. A study of differential G- and C-banding on C. rutilus andC. rufocanus chromosomes did not reveal intraspecific variation of autosomes. In these species, karyotypes of voles from Kamchatka Peninsula were studied for the first time. They appeared to be morphologically similar to the karyotypes continental voles by both autosomes and sex chromosomes.     

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.     

A quantitative field study of paternal care in Ozark hellbenders,North America’s giant salamanders

Paternal care is relatively uncommon in tetrapods but appears to be the rule in the large aquatic salamanders of the primitive family Cryptobranchidae (North America: hellbenders, genus Cryptobranchus; Asia: giant salamanders, genus Andrias). For the Ozark hellbender, C. alleganiensis bishopi, a federally endangered subspecies, anecdotal observations of paternal care have been reported, but no quantitative assessments have been made. We quantified behavior of a guarding male hellbender from video footage collected over 6 weeks in 2008 from a naturally occurring nest. We quantified behavior of the guarding male to help develop hypotheses about costs and benefits of paternal care. Overall, there were high frequencies of tail fanning of the eggs and rocking behaviors (rhythmic, lateral back-and-forth movements of the body), which increase aeration of the nest. The male rarely left the nest unguarded and spent over half of the recorded time at the nest exposed at the nest entrance. Potential egg predators observed included centrarchid, cyprinid, ictalurid, and percid fishes, with centrarchids being the most common and exhibiting the most interest in the nest. The frequency of foraging by the male was low (n?=?8 strikes at identifiable prey), with a 37% success rate. The male was observed to consume seven of his eggs. Our data represent the first systematic analysis of paternal care of Ozark hellbenders and elucidate some of the costs (low foraging success, potential energetic costs of tail fanning and rocking) and benefits (aeration of eggs, protection from egg predators) of paternal care.     

Pup contact promotes paternal responsiveness in male meadow voles

Male meadow voles, Microtus pennsylvanicus, were tested with unrelated pups to determine the social factors that affect the initiation of paternal responsiveness and the inhibition of infanticide. Adult males were initially more responsive to pups if they had been reared as neonates with their fathers rather than with unfamiliar males. Decreased aggression and facilitation of paternal responsiveness occurred most reliably after extensive exposure to pups, even if exposure had occurred more than 2 months before testing. Unlike house mice, neither copulation nor exposure to females enhanced male responsiveness to pups. Given that male meadow voles only nest with females and young during the colder parts of the breeding season, it may be adaptive for paternal responsiveness to be triggered by pup exposure, rather than by some aspect of earlier contact with the female.     

Interactions in family pairs and parental care in captive steppe lemming (Lagurus lagurus)

Partner interactions and parental activities in pair-bonded male and female steppe lemmings (L. lagurus) were estimated under laboratory conditions. Interactions between adults in family pairs were found to be neutral or peaceful with rare agonistic contacts. Compared to other rodent species living in family groups, the frequency and duration of partner grooming in adults were found to be low, indicating relatively weak pair bonding in steppe lemmings. At the same time, males spend much more time with pups in the nest than females, but they are inferior to the latter in grooming (licking) and nest material delivery. Parental behavior of L. lagurus is discussed in comparison with that of other species of the subfamily Microtinae.     

Patterns of parental care in two cricetid rodents, Onychomys torridus and Peromyscus leucopus

Daily observations were made of the maternal and paternal behaviour of Onychomys torridus and Peromyscus leucopus in laboratory cages. In both species, the females spent more time in the nest area with the young and groomed the young more frequently than their male partners, but the males played a surprisingly active role in nest attendance. Paternal nest attendance was more frequent in O. torridus males than in P. leucopus males. Onychomys males were also more active in grooming the young than Peromyscus males. These species-specific patterns of parental care are discussed in relation to the behavioural and ecological characteristics of Onychomys and Peromyscus.     

Paternal and maternal behaviour in the Mongolian gerbil

Twenty-seven pairs of Mongolian gerbils (Meriones unguiculatus) were observed rearing fifty-five litters in undisturbed conditions. Parental activities were performed by both parents. Males spent more time in the nest but females showed more sniffing and licking of pups and nest building. There was no difference between the parents in the amount of body contact with the pups. The frequency of occurrence of each of these activities changed with the age of the pups. These and other measures of behaviour are discussed in relation to the changing stimulation from the young and the willingness of the female to allow the male to interact with the litter.     

Concordant divergence in proteins and mitochondrial DNA between two vole species in the genusClethrionomys

The bank vole (Clethrionomys glareolus) and the northern red-backed vole (C. rutilus) are two closely related species where interspecific crosses result in fertile female but sterile male offspring. Mitochondrial DNA (mtDNA) fromC. rutilus has passed the species barrier and is found inC. glareolus from northern Fennoscandia. The present report shows that the genetic distance between the two species, calculated from enzyme data (Nei'sD), is 0.64. Isoelectric focusing of muscle proteins resolved around 55 bands, of which each species had 6 or 7 bands not present in the other species. Sequence divergence of mtDNA from the two species is 13.9%. A comparison between protein and mtDNA distances in other species pairs reveals a high correlation between the two measures, indicating that differences in mtDNA between taxa are not random when compared to divergence in protein-coding nuclear genes. The relationship between genetic divergence in proteins and that in mtDNA betweenClethrionomys glareolus andC. rutilus is similar to that found in other species pairs. It is also shown that despite large differences on the protein level it is still, in some cases, possible for species pairs to produce fertile hybrid females.This study was sponsored by the Swedish Natural Science Research Council, the Erik Philip-Sörensen Foundation, and the Nilsson-Ehle Foundation.     

Day length and estradiol affect same-sex affiliative behavior in the female meadow vole

Non-sexual social bonding between adult mammals is poorly understood, despite its importance in many species. Female meadow voles are territorial and nest alone in long summer day lengths when circulating estradiol concentrations are high, but cohabit in groups in short winter photoperiods when estradiol secretion is low. The influence of day length and estradiol on same-sex huddling behavior was assessed in adult female pairs housed together in long day lengths (LDs) or short day lengths (SDs) from weaning. The behavior of intact, ovariectomized, and estradiol-treated ovariectomized females from each photoperiod was assessed during 3 h partner-preference tests. Intact SD voles, unlike intact LD voles, spent the majority of the test in proximity to their cage-mates. Estradiol treatment of SD voles significantly reduced time spent huddling with the partner. Neither ovariectomy nor estradiol treatment significantly affected the amount of time LD females spent in contact with their partners. Low estradiol availability is therefore a necessary but not sufficient condition for maintenance of high levels of huddling. These results establish that ovarian hormones interact with photoperiod to affect same-sex social behavior.     

Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc,and serum oxytocin in mandarin voles

Paternal care is necessary for the healthy development of social behavior in monogamous rodents and social recognition underpins social behavior in these animals. The effects of paternal care on the development of social recognition and underlying neuroendocrine mechanisms, especially the involvement of oxytocin and estrogen pathways, remain poorly understood. We investigated the effects of paternal deprivation (PD: father was removed from neonatal pups and mother alone raised the offspring) on social recognition in mandarin voles (Microtus mandarinus), a socially monogamous rodent. Paternal deprivation was found to inhibit the development of social recognition in female and male offspring according to a habituation–dishabituation paradigm. Paternal deprivation resulted in increased inactivity and reduced investigation during new encounters with other animals. Paternal deprivation reduced oxytocin receptor (OTR) and estrogen receptor α (ERα) mRNA expression in the medial amygdala and nucleus accumbens. Paternal deprivation reduced serum oxytocin (OT) concentration in females, but had no effect on males. Our results provide substantial evidence that paternal deprivation inhibits the development of social recognition in female and male mandarin voles and alters social behavior later in life. This is possibly the result of altered expression of central OTR and ERα and serum OT levels caused by paternal deprivation.     

Olfactory Experience Affects the Response of Meadow Voles to the Opposite‐Sex Scent Donor of Mixed‐Sex Over‐Marks

Scent marking and over‐marking are important forms of communication between the sexes for many terrestrial mammals. Over the course of three experiments, we determined whether the amount of time individuals investigate the scent marks of opposite‐sex conspecifics is affected by 4 d of olfactory experience with those conspecifics. In Experiment 1, female meadow voles, Microtus pennsylvanicus, spent more time investigating the scent mark of the novel male conspecific than that of the familiar male donor, whereas male voles spent similar amounts of time investigating the scent mark of the familiar female and a novel female conspecific. In Experiment 2, voles were exposed to a mixed‐sex over‐mark in which subjects did not have 4 d of olfactory experience with either the top‐scent donor or the bottom‐scent donor. During the test phase, male and female voles spent more time investigating the scent mark of the opposite‐sex conspecific that provided the top‐scent mark than that of a novel, opposite‐sex conspecific. Male and female voles spent similar amounts of time investigating the scent mark of the bottom‐scent donor and that of a novel opposite‐sex conspecific. In Experiment 3, voles were exposed to a mixed‐sex over‐mark that contained the scent mark of an opposite‐sex conspecific with which they had 4 d of olfactory experience. During the test phase, male voles spent more time investigating the mark of the familiar, top‐scent female than the scent mark of a novel female donor but spent similar amounts of time investigating the mark of the familiar, bottom‐scent female and that of a novel female donor. In contrast, female voles spent more time investigating the mark of a novel male donor than that of either the familiar, top‐scent male or that of the familiar, bottom‐scent male. The sex differences in the responses of voles to scent marks and mixed‐sex over‐marks are discussed in relation to the natural history and non‐monogamous mating system of meadow voles.     

Spatial distribution of red-backed voles of the genus <Emphasis Type="Italic">Myodes</Emphasis> in the Khanka Plain,Primorskii Krai

The authors present new data on spatial-temporal distribution of the northern red-backed vole (Myodes rutilus Pallas) and the large-toothed redback vole (M. rufocanus Sundervall) for the main habitat types in the Khanka Plain, Primorskii Krai. Data on seasonal and long-term abundance for 2003-2005 are reported. The study was stimulated by contradictory data on the distribution of the Myodes voles in the Khanka Plain.     

Care of young, aggressiveness, and secretion of testosterone in male rodents: A correlation analysis

To test the current hypotheses on the relationship between the mating system, reproductive strategy, aggression, and secretion of testosterone, a comparative study of interactions in pair encounters, the level of parental care, and the gonadal testosterone level in males was performed in six rodent species (Clethrionomys rutilus, Meriones meridianus, Microtus arvalis, Lagurus lagurus, Lasiopodomys mandarinus, and Meriones unguiculatus) with different types of spatial-and-ethological population structures (SEPSs). It is shown that this dependence is absent in species with promiscuous mating and dominance hierarchy among males (C. rutilus and M. meridianus, SEPS type II). A trade-off, or negative correlation, was found in M. arvalis—a species with weak pair bonds and male competition for receptive females (SEPS type III). In species with persistent pair bonds and structured family groups (L. mandarinus and M. unguiculatus, SEPS type IV), no inverse relationship between the secretion of testosterone and paternal behavior was found either. Moreover, in male L. mandarinus androgens appear to stimulate paternal care.