Male Meadow Voles Research Articles

Increased sperm numbers in the vas deferens of meadow voles, Microtus pennsylvanicus, in response to odors of conspecific males

Sperm competition occurs when the sperm of two or more males compete to fertilize the egg/s of a particular female. Males of some species respond to a high risk of sperm competition by increasing the number of sperm in their ejaculates. Males may accomplish such a response by increasing the intensity or duration of contraction of the cauda epididymidis and vas deferens. During emission (first phase of the ejaculatory process), the vas deferens receives sperm from the cauda epididymidis and propels the sperm to the urethra. In this paper, we tested the hypothesis that males exposed to a high risk of sperm competition mobilize larger numbers of sperm from the cauda epididymidis to the vas deferens before initiation of copulatory behavior. This accumulation of sperm in the vas deferens would result in a larger number of sperm in the ejaculate. To test this hypothesis, we exposed male meadow voles, Microtus pennsylvanicus, to either low or high risks of sperm competition using soiled bedding of conspecific individuals. At three different times after this exposure (15, 30, or 60 min), we removed both vasa deferentia and counted the sperm within them. We found a significant increase in sperm numbers in the vas deferens of males after 30 min of being exposed to a high risk of sperm competition. The lower sperm numbers after 15 and 60 min of exposure suggest that the observed response is relatively slow and that sperm mobilized to the vasa deferentia may return to the cauda epididymides if ejaculation does not occur some time after the observed response. Our results indicate that the physiological response that may result in high sperm numbers in the ejaculate in relation to high risk of sperm competition can occur before initiation of copulatory behavior.

Effects of previous interactions and sex on over-marking in meadow voles

AbstractThe effects of winning and losing on over-marking behaviour of mammals, a behaviour associated with competition, are not known. The current study tests the hypothesis that after having a staged dyadic encounter with a same-sex conspecific, individuals adjust the proportion of scent marks they use to over-mark the marks of same-sex conspecifics. Female meadow voles that won their encounter used a higher proportion of their marks to over-mark the marks of female conspecifics than did females that either lost their encounter, were evenly matched, unfamiliar, or had no previous paired encounter. Females that lost their encounter used a lower proportion of their marks to over-mark those of female conspecifics than did females that either won their encounter or females that were evenly matched, unfamiliar, or had no previous paired encounter. Females that were evenly matched, unfamiliar, or had no previous paired encounter used a similar percentage of marks to over-mark those of another female. Male meadow voles, however, independent of whether they won, lost, were evenly matched, unfamiliar, or had no previous paired encounter used a similar proportion of marks to over-mark those of male conspecifics. The role of over-marking and the effects of previous social experience are discussed.

Sex and species differences in tyrosine hydroxylase‐synthesizing cells of the rodent olfactory extended amygdala

The bed nucleus of the stria terminalis (BST) and the medial amygdala (MeA) are anatomically connected sites necessary for chemosensory regulation of social behaviors in rodents. Prairie voles (Microtus ochrogaster) are a valuable model for studying the neural regulation of social behaviors because, unlike many other rodents, they are gregarious, pair bond after copulating, and are biparental. We herein describe sex and species differences in immunoreactivity for tyrosine hydroxylase (TH), the rate-limiting enzyme for catecholamine synthesis, in the BST and MeA. Virgin male prairie voles had a large number of TH-immunoreactive cells in areas analogous to the rat principal nucleus of the BST (pBST) and the posterodorsal medial amygdala (MeAPd). Virgin female prairie voles had far fewer TH-immunoreactive cells in these sites ( approximately 17% of the number of cells as males in the pBST, approximately 35% of the number of cells in the MeAPd). A few TH-immunoreactive cells were found in the BST of male and female hamsters and meadow voles, but not in rats. The MeApd also contained a few TH-immunoreactive cells in male and female hamsters and male meadow voles, but not rats. Castration greatly reduced the number of TH-immunoreactive cells in the male prairie vole pBST and MeAPd, an effect that could be reversed with testosterone. Furthermore, treating ovariectomized females with testosterone substantially increased TH-immunoreactive cells in both sites. Therefore, a species-specific sex difference in TH expression is found in a chemosensory pathway in prairie voles. Expression of TH in these sites is influenced by circulating gonadal hormones in adults, which may be related to changes in their display of social behaviors across the reproductive cycle.

Risk of sperm competition does not influence copulatory behavior in the promiscuous meadow vole (Microtus pennsylvanicus)

It is not clear whether males in all mammalian species adjust their copulatory behavior when faced with risk of sperm competition (RSC). Previous work on meadow voles, Microtus pennsylvanicus, indicated that males increase their sperm expenditure but not the number of ejaculations in the presence of odors of a conspecific male. The present study follows up on this work and asks whether male meadow voles modify any aspect of their copulatory behavior when they face a RSC. We examined 46 variables of copulatory behavior and found that the presence of odors from a conspecific male did not affect any of these variables. Thus, male meadow voles, unlike some other species of mammals, do not adjust their copulatory behavior when exposed to cues associated with an elevated RSC.

Social Dominance among Male Meadow Voles is Inversely Related to Reproductive Success

AbstractIntrasexual selection can occur through direct aggressive interactions between males for access to females. We tested the relationship between social dominance and male reproductive success among meadow voles, Microtus pennsylvanicus. Dominance ranks of wild‐caught males were determined using neutral arena trials, with the winner of two of three trials considered dominant. These males were then released into field enclosures and allowed to visit females housed in nestboxes for 8 wk, and males’ home range sizes were determined using weekly grid trapping. Male reproductive success was determined using molecular paternity analysis (six microsatellite primers) for all pups born during the field experiment. Males with higher dominance ranks had larger home ranges. However, male dominance rank was not predictive of the number of total visits to females’ nestboxes or the number of visits to each male's most frequently visited nestbox. Males that made more visits to nestboxes sired more litters. Males that had higher dominance ranks sired fewer litters. These results suggest that there is a reproductive disadvantage to having higher dominance rank among male meadow voles.

Do captive male meadow voles experience acute stress in response to weasel odour?

The hormonal stress response is adapted to deal with acute (short-term) stressors; however, chronic (long-term) stressors have negative effects on survival and fitness. Field and laboratory evidence suggest that voles respond behaviourally to predator odours. However, it is unknown whether voles mount an acute hormonal stress response to predator odour. We determined whether reproductively active, captive male meadow voles ( Microtus pennsylvanicus (Ord, 1815)) mounted a more pronounced hormonal stress response to weasel odour (ermine, Mustela erminea L., 1758), one of their principal mammalian predators, than to nonpredator and control odours. We compared the corticosterone response of captive voles to weasel, jumping mouse ( Zapus hudsonius (Zimmermann, 1780)), and control odours following acute (20 min) exposure. The hormonal stress response to the treatment odours did not differ, indicating that captive male voles in the reproductive season do not mount an acute stress response to predator odour. We hypothesize that voles do not respond to weasel odour because, independent of other stimuli, olfactory signals are not reliable enough to outweigh the costs, such as suppression of reproduction and reproductive behaviour, associated with a response.

Male meadow voles respond differently to risk and intensity of sperm competition

There are 2 models of male adjustment of sperm investment in the ejaculate in relation to sperm competition. The “risk model” predicts that as “risk” of sperm competition increases, sperm investment also increases. This prediction has been supported in many species, including mammals. The “intensity model” involves the number of competing males copulating with the same female and predicts that males will allocate the highest sperm investment at low sperm competition intensity (SCI) and then decreasing sperm investments as SCI increases. Two alternative outcomes are that sperm investment is unaffected by SCI and that sperm investment increases as SCI increases. There are studies supporting all 3 possible outcomes in relation to SCI but no data on mammals. The present paper presents the first study of SCI in a mammal species, the meadow vole, Microtus pennsylvanicus. We used odors of conspecific males to simulate low and high intensities of sperm competition. We found that males allocate the highest sperm investment at low SCI and decrease significantly their sperm investment at high SCI. We also found that males allocate the lowest sperm investment at low sperm competition risk (SCR) and the highest sperm investment at high SCR. All these results agree with current theoretical models of sperm competition.

Species differences in anxiety-related responses in male prairie and meadow voles: The effects of social isolation

Prairie ( Microtus ochrogaster) and meadow voles ( M. pennsylvanicus) are closely related species that differ in life strategy and social behaviors, and thus provide an excellent comparative model for the study of neuronal and hormonal mechanisms underlying behavior. In the present study using the elevated plus maze (EPM) test, we found that male prairie voles entered the open arms of the EPM more and remained there longer, and showed a higher level of overall locomotor activity than did male meadow voles. In addition, two weeks of social isolation induced an increase in open arm entries in prairie, but not meadow, voles. Prairie voles also had a higher level of circulating corticosterone compared to meadow voles, and the EPM test increased circulating corticosterone in prairie voles. Finally, social isolation coupled with the EPM test influenced Fos-immunoreactive expression in several brain areas, including the medial preoptic area, ventromedial hypothalamus, amygdala, and prefrontal cortex differently between the two species. Together, these data indicate a neural circuit involved in mediating anxiety-associated behavior in voles, and that the functioning of this circuit is influenced by social environment differently between social and non-social species.

The role of prolactin and testosterone in mediating seasonal differences in the self-grooming behavior of male meadow voles, Microtus pennsylvanicus

Self-grooming in response to the odors of conspecifics is a form of olfactory communication among meadow voles. The amount of time meadow voles spend self-grooming when they encounter the odors of conspecifics varies seasonally, with males targeting the odors of reproductively active females only during the breeding season. Other odor related behaviors in male voles such as odor preferences for conspecifics and the attractiveness of their odors to conspecifics vary seasonally as well. For male meadow voles, these behaviors are mediated by seasonal variations in testosterone (T) and prolactin (PRL) titers. The objective of this study was to determine whether seasonal differences in the amount of time male meadow voles self-groom in response to odors of conspecifics are mediated by seasonal rhythms in their circulating T and PRL titers. We tested the hypothesis that high titers of both T and PRL are necessary for reproductively active (long-photoperiod; LP) males and sufficient for reproductively quiescent (short-photoperiod; SP) male voles to spend more time self-grooming in response to odors of LP females than to those of other conspecifics. Results of this study demonstrate that high titers of PRL and T are necessary for LP male meadow vole to self-groom more in response to odors of LP females as compared to those of other conspecifics, but were not sufficient to induce SP males to preferentially self-groom to odors of LP females. The endocrine control of self-grooming by LP males appears to depend upon high titers of both PRL and T, which matches the endocrine mediation of other odor related behaviors in male voles. In contrast, the endocrine tissues that underlie self-grooming in SP male meadow voles appear to be refractory to the effects of LP-equivalent titers of PRL and T.

Food-deprivation-induced changes in sexual behaviour of meadow voles, Microtus pennsylvanicus

Food availability affects the reproductive performance of many animals. However, the majority of knowledge pertaining to food-deprivation-induced behavioural changes stems from a few model species. We investigated the effects of food deprivation on the sexual behaviour of male and female meadow voles using a three-component model that included attractivity, proceptivity and receptivity. In both males and females, proceptivity and receptivity were inhibited by food deprivations that lasted 6 h. Attractivity in females was inhibited after 24 h of food deprivation, whereas attractivity of males did not appear to be affected at any duration of food deprivation tested. Both male and female proceptivity were attenuated by food deprivations of 6 h and longer. Finally, female receptivity was inhibited by food deprivations of 6 h or longer. The data support the metabolic fuels hypothesis in females and partially support the metabolic fuels hypothesis in males. Short-term (6–12 h) and moderate (18–24 h) interruptions in food availability had inhibitory effects on all components of sexual behaviour in female meadow voles but not on proceptivity and receptivity in male meadow voles.

Female choice based on male spatial ability and aggressiveness among meadow voles

The way in which female mate choice, scramble competition and contest competition for mates interact to influence the evolution of male traits is poorly understood. We tested female preferences for males that varied in spatial ability and aggressiveness, traits likely to be selected by scramble and contest competition, respectively. Male meadow voles, Microtus pennsylvanicus, were tested for their spatial ability using a series of water maze tests, and their aggressiveness was determined using paired arena trials. Females were given a choice between two tethered males, and their preferences were scored based on relative frequency and duration of visits. Females preferred males with low aggressiveness and good spatial ability to males with high aggressiveness and poor spatial ability. Females showed no preference between males with high aggressiveness and good spatial ability and males with low aggressiveness and poor spatial ability. These results suggest that female choice and scramble competition will favour males with better spatial ability. In contrast, female choice does not seem to favour more aggressive males.

Influence of scramble competition for mates upon the spatial ability of male meadow voles

Scramble competition for mates selects for traits that increase an individual's ability to efficiently locate mates. We tested the hypothesis that scramble competition for mates is the cause of sex differences in spatial ability among meadow voles, Microtus pennsylvanicus. Specifically, we tested the predictions that males with better spatial ability have larger home ranges, visit more females' nests, and achieve greater reproductive success. We also tested the prediction that receptive females would mate with the first male that they contacted. The spatial ability of wild-caught males was quantified using the Morris water maze. Males with known spatial ability were released into enclosures for two field experiments. In the first experiment, we determined the males' home range sizes using radiotelemetry. In the second experiment, we quantified males' visits to nests by housing females in nestboxes with one-way doors and checking the boxes for male visitors twice daily. Paternity was determined by amplifying polymorphic loci using nine microsatellite primers. We found that males with better spatial ability had larger home ranges and made more visits to different nestboxes than did males with poorer spatial ability. Males with better spatial ability did not, however, sire more litters or pups. This finding may have been the result of female mate choice based on traits other than spatial ability. Females also did not always mate with the first male that they encountered.

Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males.

Sperm competition occurs when a female copulates with two or more males and the sperm of those males compete within the female's reproductive tract to fertilize her eggs. The frequent occurrence of sperm competition has forced males of many species to develop different strategies to overcome the sperm of competing males. A prevalent strategy is for males to increase their sperm investment (total number of sperm allocated by a male to a particular female) after detecting a risk of sperm competition. It has been shown that the proportion of sperm that one male contributes to the sperm pool of a female is correlated with the proportion of offspring sired by that male. Therefore, by increasing his sperm investment a male may bias a potential sperm competition in his favour. Here we show that male meadow voles, Microtus pennsylvanicus, increase their sperm investment when they mate in the presence of another male's odours. Such an increase in sperm investment does not occur by augmenting the frequency of ejaculations, but by increasing the amount of sperm in a similar number of ejaculations.

Meadow voles and prairie voles differ in the percentage of conspecific marks they over-mark

Many terrestrial mammals scent mark in areas containing the scent marks of conspecifics, and thus, may deposit their own scent marks on top of those that were deposited previously by conspecifics. This phenomenon, known as over-marking appears to play a role in same-sex competition or mate attraction. The present study determines whether meadow and prairie voles avoid over-marking the scent marks of conspecifics, target the scent marks of conspecifics and over-mark them, or randomly over-mark the scent marks of conspecifics. The data show that meadow and prairie voles adjust the number and location of scent marks that they deposit in areas marked previously by particular conspecifics. Male and female meadow and prairie voles target the scent marks of opposite-sex conspecifics and over-mark them. Female meadow and prairie voles also target the scent marks of female conspecifics. In contrast, male meadow and prairie voles over-mark the scent marks of male conspecifics in a random manner. By differentially over-marking the scent marks of conspecifics, voles may be able to communicate particular information to a variety of conspecifics.

The relationship between dominance rank and spatial ability among male meadow voles (Microtus pennsylvanicus).

Males of many mammalian species exhibit contest competition and scramble competition for mates, but the relationship between these 2 forms of competition remains poorly understood. The authors measured dominance rank and spatial ability as traits likely to be selected by contest and scramble competition, respectively, among male meadow voles (Microtus pennsylvanicus). The spatial ability of males was assessed using water maze tests, and dominance rank was determined using paired trials in a neutral arena. Dominant males had better spatial-learning ability and tended to have quicker learning speed but did not have better spatial memory than less aggressive subordinates. Therefore, the authors found no evidence that contest and scramble competition have favored alternative reproductive phenotypes among male meadow voles.

Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons

This study investigated whether estradiol influenced the survival of new granule neurons, independent of altering cell proliferation, in the adult rodent dentate gyrus and whether estradiol-induced changes in new neuron number relate to any observed changes in hippocampus-dependent behavior. To test whether estradiol specifically promotes the survival of new neurons we injected castrated adult male meadow voles with the cell synthesis marker bromodeoxyuridine (BrdU; 50 mg/kg) twice on day 0 and then injected either estradiol (10 μg) or vehicle for 5 consecutive days either over days 1–5, days 6–10 or days 11–15 and perfused them on day 16. Estradiol doubled the number of hippocampal BrdU-labeled neurons but only when administered during a discrete period (days 6–10; P≤0.01) when most new neurons extend their axons [J Comp Neurol 413 (1999) 146]. To test whether the estradiol-induced increase in new neuron number was related to hippocampus-dependent behavior, males were injected with BrdU twice on day 0 and with estradiol or vehicle over days 6–10 before standard Morris water maze training commenced on day 16, 5 days after the final hormone injection. As in the first study, estradiol-treated males had more BrdU-labeled cells than vehicle-treated males. On a probe trial, estradiol-treated males spent significantly more time in the training quadrant than vehicle-treated males despite similar performance between groups during acquisition and reversal training trials. Thus estradiol enhanced the survival of young neurons but only when administered during their ‘axon extension’ phase and this effect was related to better spatial memory in male voles.

Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles

Reproductive status influences cell proliferation and the survival of new cells in the dentate gyrus of adult laboratory-reared and wild female meadow voles; reproductively inactive (RI) females have more proliferating cells and more labeled cells that survive 5 weeks vs. 2 h than reproductively active (RA) females. However, the effect of season has only been studied in a wild sample of male meadow voles and factors such as age and experience that have been shown to influence neurogenesis in the dentate gyrus of adult mammals cannot be controlled in a wild sample. Therefore, we investigated whether reproductive status regulates neurogenesis (cell proliferation and/or the survival of new cells) in the dentate gyrus of laboratory-reared adult male meadow voles so that confounding variables could be controlled. Males were acclimated to a short- or a long-photoperiod to simulate the non-breeding or breeding season, respectively, and reproductive status was verified by testes mass. The density of labeled cells was similar in RI and RA males ( P=0.20) 2 h after an injection of bromodeoxyuridine (50 mg/kg) but the density of labeled cells was elevated in the RA males relative to the RI males 5 weeks after an injection of [ 3H]thymidine (5 μCi/g; P≤0.04). The results suggest that reproductive status regulates the survival of new cells within the dentate gyrus of adult male meadow voles but not cell proliferation.

High levels of estradiol impair spatial performance in the Morris water maze and increase ‘depressive-like’ behaviors in the female meadow vole

The present study investigated sex differences and the effect of a high level of estradiol in the female meadow vole on performance in the forced swim test (FST) and the Morris water maze in meadow voles. Female meadow voles were ovariectomized (OVX) and administered either vehicle (sesame oil) or estradiol for 2 days prior to performing the FST. Four days following the FST, all animals were run in the Morris water maze. Results indicated that estradiol-injected female meadow voles showed more ‘depressive-like’ behaviors in the FST (greater time spent immobile and less time spent swimming) than vehicle-treated female or male meadow voles. In addition, estradiol-treated females had impaired performance (greater latencies and distance swum to reach the hidden platform) than both vehicle-treated female and male meadow voles, consistent with previous data. Despite the fact that estradiol administration increased ‘depressive-like’ behaviors in the FST and impaired performance in the Morris water maze, there was no correlation between the two behaviors indicating that ‘depressive-like’ behaviors did not account for the differences seen in spatial performance in the Morris water maze. To our knowledge, this is the first demonstration in rodents indicating that estradiol-mediated changes in behavior in the FST is not indicative of subsequent performance in the Morris water maze.

The response of meadow voles to an over-mark in which the two donors differ in gonadal hormone status

Scent over-marking occurs when an animal places its scent mark directly on top of another individual's scent mark. However, situations may arise in which the top- and bottom-scent donors of an over-mark differ in an individual characteristic(s), for example, gonadal hormone titres. We tested the hypothesis that adult meadow voles, Microtus pennsylvanicus, preferentially respond to a gonadectomized donor treated with gonadal steroid hormones over a gonadectomized donor not treated with gonadal steroid hormones, independently of the position of the scent marks in an over-mark. Male meadow voles spent more time investigating the scent marks of gonadectomized females treated with oestradiol than that of gonadectomized females treated with no oestradiol, independently of the position of the two scent marks in the over-mark. Female voles spent more time investigating the scent marks of gonadectomized males treated with testosterone than that of gonadectomized males treated with no testosterone, only when the former males were the top-scent donors. These results suggest that male meadow voles appear to base their preference on the oestradiol titre of females, rather than the position of the female's mark in an over-mark. In contrast, female meadow voles appear to use both the position of the male's scent mark in an over-mark and the male's testosterone titre for the basis of their preference.

SIZE OF THE VOMERONASAL NEUROEPITHELIUM IN TWO SPECIES OFMICROTUSWITH DIFFERING LEVELS OF PATERNAL BEHAVIOR

Abstract Recent studies have suggested that the relatively large size of the vomeronasal neuroepithelium (VNNE) in the male mammal may be related inversely to the amount of parental care contributed. We tested this hypothesis using 2 species of Microtus that differ in reproductive strategies and in level of care of the offspring. We studied the nasal tissues of 8 male meadow voles (Microtus pennsylvanicus) and 8 male prairie voles (M. ochrogaster), captured between June and August, 1998. The heads were prepared histologically for serial sectioning at 10–16 μm, and stained with hematoxylin and eosin. Sections were examined by light microscopy, and the VNNE was quantified for each specimen using a computer 3-dimensional reconstruction technique. Receptor cells also were quantified with a Leica photomicroscope using an ocular grid calibrated by a stage micrometer. No (P > 0.05) differences occurred between species for length or volume of the VNNE when expressed as absolute measures or as ratios of somatic me...