Meadow Voles (Microtus pennsylvanicus, Arvicolidae) Over-mark and Adjacent-mark the Scent Marks of Same-sex Conspecifics

Scent over-marking occurs when an animal deposits its scent mark on top of the scent mark of a conspecific; adjacent-marking occurs when an animal deposits its scent mark next to the scent mark of a conspecific. Given that male rodents usually scent mark more than females and that animals spend more time investigating the odor of the top-scent donor of an over-mark, I tested the following three hypotheses. First, male meadow voles deposit more scent marks than female meadow voles. Second, male meadow voles will deposit more over-marks and adjacent-marks in response to the scent marks of a same-sex conspecific than females would. Third, meadow voles spend more time investigating the odor of the second vole placed in the arena than that of the first vole placed in the arena. To test these hypotheses, two age-matched, like-sex conspecifics (first vole and second vole) were placed successively into an arena in which they were allowed to freely explore and scent mark for 15 min. The first hypothesis was not supported. The first and second vole, independently of sex, deposited a similar number of scent marks. The second hypothesis was also not supported by the data: more conspecific scent marks were over-marked by the second female than by the second male. The third hypothesis was supported by the data. After investigating a scented arena, males and females spent more time investigating the odor of the second vole than that of the first vole. Sex differences in scent-marking behaviors of meadow voles are unlike those reported for other species of rodents.     

Meadow Voles (Microtus pennsylvanicus) and Prairie Voles (M. ochrogaster) Differ in Their Responses to Over-Marks from Opposite- and Same-Sex Conspecifics

Over‐marking occurs when one individual deposits its scent mark on the scent mark of a conspecific. Previous studies have shown that meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster) that were exposed to an over‐mark of two same‐sex conspecifics, later responded similarly to the top‐scent mark but differed in their response to the bottom‐scent mark. In the present study, we examined the responses of meadow voles and prairie voles to same‐sex and mixed‐sex over‐marks to ascertain whether their responses reflect the different tactics which males and females in promiscuous (meadow voles) and monogamous (prairie voles) species use to attract opposite‐sex conspecifics and to compete with same‐sex conspecifics. Males and females of both species spent more time investigating the mark of the top‐scent donor than that of the bottom‐scent donor of an over‐mark. Meadow voles exposed to a mixed‐sex over‐mark spent more time investigating the mark of the opposite‐sex conspecific independently of whether it was from the top‐ or bottom‐scent donor. In contrast, prairie voles spent more time investigating the mark of the opposite‐sex donor if it was from the top‐scent donor. These results suggest that: (i) over‐marking serves a competitive function; (ii) the scent marks of individuals attract multiple mates in promiscuous species such as the meadow vole; and (iii) the scent marks of individuals establish and maintain pair bonds between familiar opposite‐sex conspecifics in monogamous species such as the prairie vole.     

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.     

Scent Marking in Female Prairie Voles: a Test of Alternative Hypotheses

We conducted three experiments with females in different stages of reproductive condition to test alternative hypotheses for the function of scent marking in female prairie voles, Microtus ochrogaster . The three reproductive categories were isolated females prior to sexual stimulation (anoestrous), sexually stimulated (oestrous) and lactating. Females in different reproductive condition were given the opportunity to scent mark clean unmarked substrate or areas that had previously been marked by adult females or adult males. The numbers of scent marks deposited by females did not differ statistically for females in different reproductive condition. However, there was a trend for anoestrous females to mark the most, oestrous females less, and lactating females the least. The lack of scent marking by lactating females might be to reduce conspicuousness to conspecifics or predators. Oestrous females tended to mark the most in the area marked previously by males, although the difference was not statistically significant.
Our results provide some support for a mate-attraction hypothesis and a territorial-defense hypothesis, but were most consistent with a self-advertisement hypothesis. Over marking was uncommon and did not differ by experiment or sex of previous donor. Our results suggest that the number and placement of scent marks by females are highly variable and function primarily to convey individual identity.     

Food Sorting by Collared Lemmings (Dicrostonyx groenlandicus) and Prairie Voles (Microtus ochrogaster): A Cautionary Note for Digestibility Studies

Small herbivores are often confronted with poor quality diets; in response to this situation, they may sort their food to increase diet quality. Neutral detergent fiber (NDF) levels were measured in three pelleted diets fed to collared lemmings (Dicrostonyx groenlandicus) and prairie voles (Microtus ochrogaster) and compared to levels in orts collected from the same diets and animals. Lemmings sorted and discarded the fibrous parts of food pellets on all three diets (17.3% to 25.9% higher NDF in orts), whereas voles sorted out fibrous particles on only one diet. Calculations of NDF digestibility were significantly reduced by particle sorting (up to 16.9% decrease in digestibility). In reviewing the literature, we found that in more than half of studies examined, orts may not have been analyzed for these differences. Researchers must carefully consider such effects, especially when conducting digestibility studies with herbivores on pelleted diets.     

Clusters of Repetitive DNA Sequences in Chromosomes of Voles of the Subgenus Microtus (Microtus,Arvicolidae)

Russian Journal of Genetics - The study is focused on the analysis of the mechanisms underlying the formation and distribution of repeat clusters in mammalian chromosomes, as exemplified by a group...     

A Translocated Mitochondrial Cytochrome b Pseudogene in Voles (Rodentia: Microtus)

A full-length cytochrome b pseudogene was found in rodents; it has apparently been translocated from a mitochondrion to the nuclear genome in the subfamily Arvicolinae. The pseudogene (ψcytb) differed from its mitochondrial counterpart at 201 of 1143 sites (17.6%) and by four indels. Cumulative evidence suggests that the pseudogene has been translocated to the nucleus. Phylogenetic reconstruction indicates that the pseudogene arose before the diversification of M. arvalis/M. rossiaemeridionalis from M. oeconomus, but after the divergence of the peromyscine/sigmodontine/arvicoline clades some ∼10 MYA. Published rates of divergence between mitochondrial genes and their nuclear pseudogenes suggest that the translocation of this mitochondrial gene to the nuclear genome occurred some 6 MYA, in agreement with the phylogenetic evidence. Received: 16 January 1998 / Accepted: 18 July 1998     

Mating System and Population Fluctuations of the Prairie Vole, Microtus ochrogaster

The basic mating system of the prairie vole, Microtus ochrogaster,consists of monogamous breeding units comprised of one reproductivefemale and male and their offspring. Most surviving young remainat the natal nest; those that do so normally remain non-reproductive.Of 281 total breeding units monitored in free-living populations50.2% were monogamous. Twenty-seven percent consisted of a singlereproductive female that apparently has lost her mate. Theremaining22.8% of the breeding units included two or more unrelated adultsmales and/or females (=‘complex’ breeding units).In general, monogamy was the predominant type of breeding unitat the highest (>100 adults/ha) as well as at low (>20adults/ha) population densities. There was no consistent relationshipbetween the number of residents of a breeding unit and populationdensity. Significantly more young females remaining at the natalnest became reproductive at high rather than at low populationdensities (77.1 and 17.6%, respectively). Monogamy was prevalentduring the winter as well as during the other seasons; however,there were significantly more complex breeding units duringthe winter than during other seasons. Breeding unit size wassignificantly larger during the winter than at other seasons.There was no difference in the proportions of breeding unittypes or the number of residents of a breeding unit during breedingand nonbreeding seasons. Increased breeding unit size appearsrelated to low temperatures and associated physiological stressesduring the winter rather than to population density.     

Morphological variation in root vole Microtus oeconomus pallas (Rodentia, Arvicolidae) in the Baikal region

Morphological variation in root vole was studied in 10 samples from the Baikal islands and shore regions. The island samples differed from the continental ones by a set of cranial characters as well as by a higher complexity and asymmetry of morphotypes of the third upper molar. A possible role of biotopic and microclimatic conditions in the formation of a specific morphological pattern of island micropopulations of this species is discussed.     

A Comparison of the Maternal Care of Females within Prairie Vole (Microtus ochrogaster) Communal Groups

Communal rearing, the shared rearing of offspring by multiple individuals or mothers, may improve the fitness of individuals in group‐living species. To date, many studies have focused on these potential fitness consequences. Fewer studies have emphasized the relative contributions to care of offspring by mothers and non‐breeding alloparents in singularly breeding groups (i.e., one female breeds) and mothers within plurally breeding groups (i.e., more than one female breeds). We compared the care provided by prairie vole (Microtus ochrogaster) mothers and alloparents in singularly breeding groups and mothers in plurally breeding groups. Subjects were littermate siblings in both types of social groups. Specifically, we quantified the amount of time that mothers and alloparents were away from pups during 6 h observational trials and the amount of time that females tactilely stimulated pups (licking and grooming) during 20 min trials. We also compared the quality of milk, measured as total solids, produced by mothers in plurally breeding groups. In singularly breeding groups, mothers spent significantly more time out of the nest but tactilely stimulated pups more than alloparents. In plurally breeding groups, focal mothers (i.e., the first mother to produce a litter) spent significantly more time out of the nest than second mothers (i.e., the second female to produce a litter) but licked and groomed pups an equal amount as second mothers. In plurally breeding groups, focal and second mothers produced milk with a similar concentration of total solids. These results suggest that communal rearing in groups is more beneficial to focal mothers than to other breeding or non‐breeding adult females. We discuss fitness‐based hypotheses that may explain the observed differences in the amount of care provided by mothers and alloparents.     

mtDNA analysis reveals the ongoing speciation on Greek populations of Microtus (Terricola) thomasi (Arvicolidae,Rodentia)

The present article extends our previous work on the phylogenetic history of Microtus (Terricola) thomasi, analysing cytochrome b, 12S rRNA, 16S rRNA and the control region in 65 Greek populations. The analysis revealed three clades: one grouping the populations from Peloponnisos (Southern Greece); the second, the populations from Agios (Ag.) Stefanos and Evvoia island (Central East Greece); and the third, all the remaining populations with no geographical substructure. Genetic distances were low for most populations, with only the populations of Evvoia and Ag. Stefanos being substantially distant. Thus, although this species has a recent colonization history and probably descends from a highly polymorphic ancestor, a monophyletic and highly differentiated lineage is formed in Greece and is distributed in Ag. Stefanos and Evvoia. Molecular differentiation, distinct geographical distribution and restriction of gene flow between this lineage and the rest of the Greek populations provide evidence for its probable subspecific status, Microtus (Tericola) thomasi atticus. A possible mechanism leading the differentiation process of the proposed subspecies is suggested, based on the displacement of this species in central Greece by its congeneric, probably better‐fitted Microtus (Microtus) guentheri and the subsequent separation of Ag. Stefanos and Evvoia from the remaining Greek populations. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 117–130.     

Autonomic Substrates of the Response to Pups in Male Prairie Voles

Caregiving by nonparents (alloparenting) and fathers is a defining aspect of human social behavior, yet this phenomenon is rare among mammals. Male prairie voles (Microtus ochrogaster) spontaneously exhibit high levels of alloparental care, even in the absence of reproductive experience. In previous studies, exposure to a pup was selectively associated with increased activity in oxytocin and vasopressin neurons along with decreased plasma corticosterone. In the present study, physiological, pharmacological and neuroanatomical methods were used to explore the autonomic and behavioral consequences of exposing male prairie voles to a pup. Reproductively naïve, adult male prairie voles were implanted with radiotransmitters used for recording ECG, temperature and activity. Males responded with a sustained increase in heart-rate during pup exposure. This prolonged increase in heart rate was not explained by novelty, locomotion or thermoregulation. Although heart rate was elevated during pup exposure, respiratory sinus arrhythmia (RSA) did not differ between these males and males exposed to control stimuli indicating that vagal inhibition of the heart was maintained. Blockade of beta-adrenergic receptors with atenolol abolished the pup-induced heart rate increase, implicating sympathetic activity in the pup-induced increase in heart rate. Blockade of vagal input to the heart delayed the males’ approach to the pup. Increased activity in brainstem autonomic regulatory nuclei was also observed in males exposed to pups. Together, these findings suggest that exposure to a pup activates both vagal and sympathetic systems. This unique physiological state (i.e. increased sympathetic excitation of the heart, while maintaining some vagal cardiac tone) associated with male caregiving behavior may allow males to both nurture and protect infants.     

The Reproductive State of Female Voles Affects their Scent Marking Behavior and the Responses of Male Conspecifics to Such Marks

During the breeding season, the reproductive condition of female mammals changes. Females may or may not be sexually receptive. We conducted a series of experiments to determine whether reproductive condition of female meadow voles affects their scent marking behavior as well as the scent marking behavior of male conspecifics. In expt 1, females in postpartum estrus (PPE females) deposited more scent marks than females that were neither pregnant nor lactating (REF females) or ovariectomized females (OVX females). In expt 2, male voles scent marked more and deposited more over‐marks in areas marked by PPE females than by REF and OVX females. In expt 3, PPE females deposited more scent marks and over‐marks in areas marked by males than did females in the other reproductive states. The results of these experiments showed that male and female voles may vary in the number, type and location of scent marks they deposit in areas scented by particular conspecifics.     

An application of common principal component analysis to cranial morphometry of Microtus californicus and M. ochrogaster(Mammalia, Rodentia)

Principal component analysis (PCA) is a one-group method. Its purpose is to transform correlated variables into uncorrelated ones and to find linear combinations accounting for a relatively large amount of the total variability, thus reducing the number of original variables to a few components only.
In the simultaneous analysis of different groups, similarities between the principal component structures can often be modelled by the methods of common principal components (CPCs) or partial CPCs. These methods assume that either all components or only some of them are common to all groups, the discrepancies being due mainly to sampling error.
Previous authors have dealt with the k-group situation either by pooling the data of all groups, or by pooling the within-group variance-covariance matrices before performing a PCA. The latter technique is known as multiple group principal component analysis or MGPCA (Thorpe, 1983a). We argue that CPC- or partial CPC-analysis is often more appropriate than these previous methods.
A morphometrical example using males and females of Microtus californicus and M. ochrogaster is presented, comparing PCA, CPC and partial CPC analyses. It is shown that the new methods yield estimated components having smaller standard errors than when groupwise analyses are performed. Formulas are given for estimating standard errors of the eigenvalues and eigenvectors, as well as for computing the likelihood ratio statistic used to test the appropriateness of the CPC- or partial CPC-model.     

Persistence of the Attractiveness of Two Sex-specific Scents in Meadow Voles,Microtus pennsylvanicus

The function of an odour may be reflected in its fade-out time in the environment. In this study, we investigated fade-out times of two specific odours, the anogenital area scent and that of the posterolateral region. These two odours support opposite-sex preferences in male and female meadow voles, Microtus pennsylvanicus, but convey nonidentical information to conspecifics during the breeding season. The first experiment tested whether meadow voles respond preferentially to scents that were aged for 15 min (fresh) to 30 d. Males preferred female anogenital area scent to male anogenital area scent if both scents were ≤ 10 d old. By comparison, females preferred male anogenital area scent to female anogenital area scent if the scents were ≤ 25 d old. However, male and female voles preferred the posterolateral scent of males to that of females if the scents were ≤ 1 d old. Thus, fade-out times for these two scents differ for males and females, suggesting different functions. In the second experiment, male and female voles preferred fresh anogenital area scent and fresh posterolateral region scent compared with those same scents that were older. This result suggests that older scents may have lost information over time about the sex of the donor. Overall, data from both experiments indicate that voles may use specific scents for communication in different social contexts.     

An application of common principal component analysis to cranial morphometry of Microtus californicus and M. ochrogaster (Mammalia, Rodentia): further remarks

We welcome Dr Thorpe's interesting discussion (Thorpe, 1988), and we would like to take this opportunity to clarify some points.
Both MGPCA (multiple group principal component analysis) and CPCA (common principal component analysis) serve essentially the same purpose, namely estimation of principal components simultaneously in several groups, based on the assumption of equality of principal component directions across groups, while eigenvalues may differ between groups. However, CPCA has the distinct advantage that this assumption can actually be tested, using the (CPC) statistic. In analyses involving more than two variables, it is usually difficult to decide, without a formal test, whether or not the assumption of common directions of principal components is reasonable.
There is also a conceptual difficulty with MGPCA. In statistical terms, both methods assume that:
(a) a certain set of parameters (namely those determining the eigenvectors) are common to all groups
(b) there are sets of parameters (namely p eigenvalues per group) which are specific to each group.
CPCA sets up a model that reflects this structure and estimates the parameters accordingly. MGPCA, on the other hand, ignores part (b), at least temporarily, by pooling the variance-covariance matrices and extracting eigenvectors from the single pooled matrix. This may lead to reasonable results, but there is no guarantee that it will indeed do so. The reader may find a more familiar analog in the fitting of regression lines when data are in groups. If it is assumed that all regression lines are parallel, one should set up an appropriate model based on a single slope parameter common to all groups, and groupwise intercepts. One should then estimate the parameters of this model, and not simply apply a technique which is appropriate in the one-group case only.     

mtDNA variation and evaluation of phylogenetic relationships among karyotypically polymorphic populations of Microtus (Terricola) thomasi (Arvicolidae, Rodentia) from Greece

The Balkan endemic species Microtus (Terricola) thomasi – Thomas' vole – is widely distributed in the Greek mainland and presents regionally confined karyotypic forms. In order to test the significance of geographical isolation and/or karyological differences in microevolutionary processes at the intraspecific level we used restriction enzymes and partial sequencing to study the polymorphism of the mtDNA d -loop control region in ten Greek populations. An overall high rate of both inter- and intrapopulation polymorphism was observed. The mtDNA diversity was unevenly distributed so that most of the populations studied were very similar and closely related, and only a few of them were clearly differentiated from the others. The mtDNA analysis failed to reveal any clear variation pattern that could be correlated with karyotypic forms or geographical proximity of the populations studied. Instead, the mtDNA phylogeny gave evidence in support of the coexistence of non-polymorphic (2 n  = 44) and polymorphic (2 n  < 44) karyotypic forms within the ancestral Greek M. (T.) thomasi stock. Interestingly, only one population (Agios Stefanos) seemed to significantly diverge from all the others in both methods used, forming a well-supported paraphyletic clade. Allozymic studies have already reported similar results, corroborating the genetic peculiarity of this population.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 55–68.     

First reports of XXY aneuploidy in natural populations of Thomas’ pine vole Microtus thomasi (Rodentia: Arvicolidae) from Greece

As part of an extensive cytological study in natural populations of Thomas’ pine vole Microtus thomasi, two cases of XXY aneuploidy (2n=45, FN=47) from different localities of NW Peloponnesus, Greece were recently recorded. These constitute the first report of sex chromosome aneuploidy for this species, in a sample of 366 individuals from 89 localities of Greece. Both individuals appeared with a male phenotype and normal morphology; however, measurements and histological examination in the testes of one of the two individuals imply a severely impaired fertility. The above findings translate to a relatively high rate of sex chromosome aneuploidy (0.55%) (upper 95% CI 1.96%) for the natural populations of Microtus thomasi and possible reasons for this are discussed.