Sexual differences in responses of meadow voles to environmental cues in the presence of mink odor.

In rodents, defensive behaviors increase the chances of survival during a predator encounter. Observable rodent defensive behaviors have been shown to be influenced by the presence of predator odors and nearby environmental cues such as cover, odors from conspecifics and food availability. Our experiment tested whether a predator scent cue influenced refuge preference in meadow voles within a laboratory setting. We placed voles in an experimental apparatus with bedding soaked in mink scent versus olive oil as a control across from four tubes that either contained (a) a dark plastic covering, (b) opposite-sex conspecific odor, (c) a food pellet, or (d) an empty, unscented space. A three-way interaction of tube contents, subject sex, and the presence of mink or olive oil on the preference of meadow voles to spend time in each area of the experimental apparatus and their latency to enter each area of the apparatus revealed sex differences in the environmental preference of meadow voles facing the risk of predation. The environmental preference of female, but not male, meadow voles was altered by the presence of mink urine or olive oil. A similar trend was found in the latency of males and females to enter each area of the experimental apparatus. These differences suggest that each sex utilizes different methods to increase their fitness when experiencing a predation risk. The observed sex differences may be explained by the natural history of voles owing to the differences in territorial range and the dynamics of evasion of terrestrial predators.

Do male meadow voles (Microtus pennsylvanicus) always prefer and signal to 'popular' females? The role of social information context.

For males, the behaviour of rival conspecifics can provide vital information about finding reproductively available females, and which have high-quality phenotypes. While valuable, this information represents sperm competition risk and even the potential for rejection by females. Thus, males should show flexibility in signalling behaviours towards females based on social information acquired with emphasis on the context of that information. We examined male meadow vole scent-marking behaviours and preferences for females based on previously obtained social information across different contexts. Social information context resulted in increased scent marking depending on the social odour pairing. Males scent marked more near a female whose odour had associated with three older rivals than one younger rival. But males marked equally toward a female whose odour had associated with three younger rivals and a female whose odour had associated with one older rival. This demonstrates that social odours are not of all equal value and that males can distinguish differences. Males then use these differences to tailor their signalling towards potentially high-quality phenotype females thereby maximizing their reproductive opportunities.

Conserved transcriptomic profiles underpin monogamy across vertebrates.

Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.

Scent marks of rodents can provide information to conspecifics.

For a scent mark to be informative it must provide a reliable, honest signal that allows individuals that detect it to predict fitness tradeoffs if they choose or not choose to respond to it. I argue that scent marks provide a great deal of information about the sender to receivers. The manner in which an animal uses this information to make decisions will depend on the context and manner in which it encounters these scent marks. Receivers can use the information found in the scent marks and odors to locate the donor, learn its identity, determine the donor's phenotype or genotype, and assess whether the scent marks were encountered earlier by conspecifics. For receivers to make potentially informed decisions, when they encounter the scent marks of conspecifics with whom they have had different experiences across a variety of contexts higher level cognitive processing involving procedural memory, episodic memory, autobiographical memory and making judgements of numerical discrimination would be required. Senders should have some insight into the receivers to increase the likelihood that the targets respond appropriately to the scent mark by reducing uncertainty. The sender's state or the current state of the environment and the context will affect when and where the scent marks were deposited. Decisions to deposit scent marks and respond to them must represent a tradeoff in the benefits and costs to the sender and receivers in terms of their fitness and survival. The actual tradeoff should be context dependent and reflect the experience, physiology, and life history constraints affecting the receiver. Calculating these tradeoffs likely involves some cognitive processing and requires some sort of information transfer between the sender and the receiver.

The response of rodents to scent marks: four broad hypotheses.

This article is part of a Special Issue "Chemosignals and Reproduction". Many terrestrial mammals must be able to distinguish between the myriad of scent marks they encounter in order for them to facilitate or deter direct interactions with their scent donors. I review studies that examine how rodents, mainly meadow voles (Microtus pennsylvanicus), respond when they encounter the scent marks of conspecifics and heterospecifics, and how context, as well as the age and condition of senders and receivers, affect their responses. The review uses four broad hypotheses to discuss the response of rodents to scent marks. The four hypotheses are as follows: 1) Scent marks convey accurate information to the receiver about the sender's state and phenotype and genotype. 2) Scent marks are individually distinct. 3) The response of receivers to scent marks is flexible and would be modulated by the cognitive abilities of receivers. 4) Receivers respond to the information contained or conveyed by the scent mark in a manner that will increase their survival and fitness. The studies cited in this review show that scent marks signal accurate information about the sender's phenotype, genotype, and condition, which receivers use to distinguish among the scent marks of different conspecifics and heterospecifics, and by doing so, receivers tailor their response accordingly to increase their survival and fitness. Thus, the four broad hypotheses may serve as guide to increase our understanding of the response of receivers to scent marks and provide a conceptual framework for future research and the development of additional hypotheses.

Female meadow voles, Microtus pennsylvanicus, respond differently to the scent marks of multiple male conspecifics.

Many nonhuman animals are capable of discriminating a group or entity containing more objects from one containing less of the same objects. The capacity for making judgments of numerousness may also allow individuals to discriminate between potential mates. Female meadow voles (Microtus pennsylvanicus) may use judgments of relative numerousness to distinguish between potential suitors by selecting males that signal their interest by depositing more scent marks relative to other males. We used a familiarization-discrimination paradigm in the absence of training to test the hypothesis that female voles will discriminate between the different numerosities of scent marks of two male conspecifics that are similar in features of their phenotype and quality. During the exposure phase, we presented female voles with different ratios of feces scent marks from two males. During the test phase, we presented females with a single, fresh fecal scent mark from each of the two male donors, whose marks they had previously encountered during the exposure phase. In both phases, females spent more time investigating the scent mark(s) of the male that deposited more scent marks than that of the male that deposited fewer scent marks provided the difference in the ratio of scent marks provided by the male donors in the exposure phase was ≥2. Our results are consistent with studies on a variety of taxa, suggesting that numerosity discriminations are evolutionarily ancient and spontaneously available to nonhuman animals and humans.

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.

Gonadal hormones modulate sex differences in judgments of relative numerousness in meadow voles, Microtus pennsylvanicus.

Animals in a variety of taxa discriminate between a greater quantity and a lesser quantity of the same object, an ability that is referred to as relative numerousness judgment. For example, meadow voles can distinguish between areas containing more over-marks by one opposite-sex scent donor and fewer over-marks by another opposite-sex scent donor. Females appear to be able to make better discriminations between more or less over-marks than do males. In that gonadal hormones have been implicated in modulating cognitive function associated with spatial tasks, we tested the hypothesis that high titers of testosterone and estradiol are necessary for male and female voles, respectively, to distinguish between the top- and bottom-scent donors in an area containing mixed over-marks. We gonadectomized voles, giving them either gonadal hormone replacement (testosterone for males and estradiol for females) or no hormone replacement, and tested their spontaneous judgments of distinguishing between the top- and bottom-scent donors in an area containing mixed over-marks; a task involving judgments of relative numerousness. Female voles given replacement estradiol performed better than did female voles not given replacement estradiol in determining the top-scent and bottom-scent males in areas containing mixed over-marks. In contrast, males not treated with replacement testosterone performed better than did males treated with testosterone in determining the top-scent and bottom-scent males in areas containing mixed over-marks. Thus, high titers of estradiol and low titers of testosterone are associated with better performance on tasks involving relative numerousness in female and male voles, respectively. The results of this task on relative numerousness judgments are discussed in relation to the effects of gonadal steroid hormone on spatial ability, a closely related cognitive domain, and the social biology of meadow voles.

Odor Communication and Mate Choice in Rodents.

This paper details how chemical communication is affected by ecological challenges such as finding mates. I list several conditions that affect the decision to attract mates, the decision to respond to the signals of potential mates and how the response depends on context. These mate-choice decisions and their outcomes will depend on the life history constraints placed on individuals such as their fecundity, sex, lifespan, opportunities to mate in the future and age at senescence. Consequently, the sender's decision to scent mark or self-groom as well as the receiver's choice of response represents a tradeoff between the current costs of the participant's own survival and future reproduction against that of reproducing now. The decision to scent nark and the response to the scent mark of opposite-sex conspecifics should maximize the fitness of the participants in that context.

Food deprivation and the role of estradiol in mediating sexual behaviors in meadow voles.

Female mammals are particularly sensitive to changes in food availability. The mechanisms that affect sexual behavior and food intake are closely related to one another; chief among the mechanisms that control sexual behaviors in females is estradiol. In order to understand how food deprivation results in inhibition of sexual behavior (attractivity, proceptivity, and receptivity), we measured the effects of food deprivation on circulating concentrations of estradiol. We also determined whether estradiol treatment was sufficient to restore sexual behaviors in food-deprived female meadow voles. We found that estradiol titers of food-deprived female voles are significantly lower than those of ad lib-fed female voles. Further, we found that estradiol treatment was sufficient to restore proceptivity and receptivity in food-deprived, ovariectomized female voles. However, estradiol treatment was not able to overcome the food deprivation-induced inhibition of attractivity. Thus, decreases in estradiol titer of food-deprived female voles may be related to the suppression of their proceptive and receptive behaviors, and may be a mechanism that allows females to avoid mating when conditions are not propitious for their survival and that of their offspring.

Exogenous melatonin administration affects self-grooming and conspecific odor preferences in long-photoperiod meadow voles (Microtus pennsylvanicus).

For meadow voles, Microtus pennsylvanicus, seasonal differences exist in self-grooming and in odor preferences for conspecifics, two behaviors which facilitate sexual interactions in this species. Both behaviors are mediated by photoperiodically-induced changes in circulating gonadal steroid hormone titers which, in turn, can be transduced by the duration of the melatonin signal that a seasonally breeding animal receives. The goal of this study was to determine whether exogenous melatonin administration affects circulating gonadal steroid hormone titers in meadow voles, and whether it influences their odor preferences and self-grooming behavior to same- and opposite-sex conspecifics. Long-photoperiod voles that did not receive exogenous melatonin had higher testosterone (males) and estradiol (females) titers than did short-photoperiod voles and long-photoperiod voles treated with melatonin for 12 weeks; the latter had similar estradiol and testosterone titers. Long-photoperiod voles that did not receive melatonin preferred the scent marks of long-photoperiod opposite-sex conspecifics and spent more time self-grooming in response to their odors than those of either long-photoperiod same-sex, short-photoperiod same-sex, or short-photoperiod opposite-sex conspecifics. Long-photoperiod voles that received melatonin, however, no longer preferred the marks of long-photoperiod opposite-sex conspecifics and no longer spent more time self-grooming in response to their odors, not unlike the odor preferences and self-grooming behavior of short-photoperiod voles. As a whole, the data suggest that the duration of the melatonin signal is likely involved in mediating the photoperiodically-induced changes in gonadal steroid hormones that mediate a meadow vole's odor preferences for opposite-sex conspecifics and its self-grooming response to those marks.

The Effects of Food Availability on the Sexual Behavior of Meadow Voles.

Two competing hypotheses have been used to explain species and sex differences in the effects of food availability on the sexual behavior of mammals. One hypothesis, the metabolic fuels hypothesis, posits that individuals, primarily females, forgo reproduction when faced with food deprivation and invest their limited resources in behaviors not associated with reproduction. The other hypothesis, the reproduction at all costs hypothesis, states that individuals, males and females, continue to reproduce or increase their reproductive behavior when faced with food deprivation. Results show female voles followed the predictions of the metabolic fuels hypothesis. That is, food-deprived female meadow voles were less attractive, proceptive, and receptive toward males than were female voles that had continuous access to food. Dams that were food deprived late in lactation failed to enter postpartum estrus, a period of heightened sexual receptivity that occurs immediately after parturition. Females that were food deprived during the first or second week of lactation spent less time involved in maternal care compared to dams that were not food deprived. In contrast, male voles mainly followed the reproduction at all costs hypothesis. Food-deprived male voles were as attractive, as proceptive, and as sexually receptive toward females as were males that had continuous access to food.

Similarities between female meadow voles mating during post-partum oestrus and raising two concurrent litters and females raising only one litter.

In many species of small mammals, females undergo post-partum oestrus soon after delivering a litter, becoming pregnant while suckling the previous litter. Females raising two concurrent litters need to allocate many more resources to reproduction than females raising only one litter. Consequently, there may be differences between litters raised concurrently or singly. We investigated this issue in the meadow vole, Microtus pennsylvanicus, a species in which most females in the wild reproduce during post-partum oestrus. Specifically, we tested the hypothesis that the development of pups in two concurrent litters differs from that of pups in a single litter. To test this hypothesis, we measured the following variables for concurrent and singly reared litters: gestation length; litter size; sex ratio; bodyweight of males and females at different ages; total litter weight at weaning; growth rates; and intra-litter variation in body mass. Except for bodyweight of males at 60 days of age, which was higher in the first of the concurrent litters, none of the variables differed among the litters. These results indicate that females are able to adjust to differing loads of maternal care to provide equivalent resources to concurrent litters and singly reared litters.

The amount of time that a meadow vole, Microtus pennsylvanicus, self-grooms is affected by its reproductive state and that of the odor donor.

Many hypotheses have been put forth to account for differences in the amount of time that animals engage self-grooming when exposed to conspecifics or their odors, but most ignore the possibility that self-grooming may be associated with olfactory communication between groomers and conspecifics. As yet, we do not know the function of self-grooming and why animals do so when they encounter the odors of conspecifics. The present experiment tests the hypothesis that the amount of time that a meadow vole, Microtus pennsylvanicus, self-grooms is affected by the reproductive state of the odor donor and its own reproductive state. The findings support the hypothesis. Male voles spent more time self-grooming when they were exposed to bedding scented by female voles in postpartum estrus (PPE) compared to that of female voles in other reproductive states and female mice. PPE female voles spent more time self-grooming when they were exposed to bedding scented by testosterone-treated male voles than either to that of gonadectomized male voles and male mice. PPE female voles spent more time than OVX+E and more time than OVX females self-grooming when they were exposed to bedding scented by testosterone-treated male voles. GX+T male voles spent more time than GX male voles self-grooming when they were exposed to bedding scented by PPE female voles. The results suggest that individuals self-groom more in the presence of an odor of a highly receptive potential mate than that of a less receptive mate.

Re-feeding and the restoration of odor attractivity, odor preference, and sexual receptivity in food-deprived female meadow voles.

Food-deprived meadow voles were used to test predictions of two hypotheses associated with the recovery of sexual behaviors following re-feeding. Specifically, we tested between the body weight set point and metabolic fuels hypotheses. To do so, we determined whether the body weight of previously food-deprived female voles had to return to pre-food deprivation levels before they would recover their sexual behaviors. The body weight set point hypothesis predicts that food-deprived females that were re-fed will recover their sexual behavior after they return to their original body weight. In contrast, the metabolic fuels hypothesis predicts that food-deprived females that were re-fed will recover their sexual behavior before they return to their original body weight. That is, when the females are in positive energy balance. To distinguish between these two hypotheses, female voles were food deprived for 24 h, which is sufficient to inhibit all three components of sexual behavior. The food-deprived females were then supplied ad libitum food for 0 h, 24 h, 48 h, 72 h, or 96 h and weighed. Females were then tested for their sexual behaviors (odor attractivity, odor preference or proceptivity, sexual receptivity). Re-feeding for 48 h was sufficient to restore odor attractivity, 72 h was sufficient to restore odor preferences for opposite sex conspecific odors, and 96 h was sufficient to restore sexual receptivity to those similar to that of females that were not food deprived. The time-points that the behaviors were recovered were prior to voles recovering their initial body weight. Thus, the data support the metabolic fuels hypothesis.

A battery of olfactory-based screens for phenotyping the social and sexual behaviors of mice.

We provide a battery of screens that reflect the social and sexual behavior displayed by both captive and feral mice. Some screens focus on measuring aspects of chemical communication, providing information about whether or not mice will interact and if they do so, predict the nature of the interaction. Other screens measure direct interactions between target mice and same- and opposite-sex conspecifics, providing an indication of the social status and sexual responsiveness, respectively, of target mice. The battery of screens yields a high-throughput bioassay of a mouse's relative social status, competitive ability, social discrimination, and sexuality. These traits are essential elements of the socio-sexual behavior of mice as well as humans. Thus, by identifying phenotypic deviants for complex behaviors we will allow geneticists to map behavioral abnormalities onto specific chromosomes and increase the efficacy of genetically altered mice as models for human behavioral disorders.

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.

Female meadow voles, Microtus pennsylvanicus, do not alter their over-marking in response to female conspecifics that were food deprived.

Many terrestrial mammals will deposit scent marks and over-marks, the latter being the overlapping scent marks of two conspecifics. Studies have shown that male rodents that are exposed to the overlapping scent marks of two female conspecifics later spend more time investigating the mark of the top-scent female than that of the bottom-scent female. This suggests over-marking is a form of competition and that the top-scent female is more likely than the bottom-scent female to be chosen as a potential mate. Thus, females should over-mark the scents of neighboring females at a rate that will maximize their chances of attracting males. However, meadow voles live in areas that may contain patchy food availability, and residents may differ in their nutritional status. Females in a better nutritional state may be more likely than those in poorer nutritional states to indicate their presence in an area, signal possession of a territory, and to attract mates. Thus, we tested the prediction that female meadow voles, Microtus pennsylvanicus, that were not food deprived would deposit more over-marks than female voles that were food deprived for six hours. Food-deprived female voles and female voles that had continuous access to food deposited a similar number of scent marks and used a similar proportion of those marks as over-marks when they encountered the scent marks of female conspecifics. These findings suggest that the nutritional status of female voles does not affect their ability to signal their presence in an area marked by a female conspecific.

Maternal Food Restriction During Lactation Affects Body Weightand Sexual Behavior of Male Offspring in Meadow Voles (Microtus pennsylvanicus).

Little is known about the occurrence of individual variation in sexual behavior and how maternal nutrition can affect this variation. We tested the hypothesis that male offspring of female meadow voles, Microtus pennsylvanicus, that were 30% food restricted (FR) during days 1-7 of lactation (FR 1-7), days 8-14 of lactation (FR 8-14), or late days 15-21 of lactation (FR 15-21) lactation show persistent, negative effects on their sexual behavior as adults relative to male offspring of females that were not food restricted. We measured three components of sexual behavior, attractivity, proceptivity and receptivity, beginning when the males were 98 days of age. Food restriction during middle lactation (FR 8-14) but not during early (FR 1-7) and late lactation (FR 15-21) was sufficient to induce adult male voles to produce anogenital marks that were not as attractive as those produced by control males. Food restriction during lactation did not affect the proceptive behavior of male voles but did affect their receptivity. Only 4 of 12 FR 8-14 male voles mated compared to 9 of 12 FR 1-7 males, 8 of 12 FR 15-21 males, and 8 of 11 control males. However, no differences existed in their copulatory behavior among the males that did mate. The body weight of FR 1-7 and FR 8-14 males was lower than that of FR 15-21 and control males when they were between 22 days of age (weaning) and 48 days of age (puberty) but was similar when the males were 98 days of age. Food intake was similar for the FR and control males between day 22 and day 98. It remains unclear, however, if this type of maternal effect represents strategic programming of offspring behavior in response to the environment experienced by mothers or is a product of developmental processes of food restriction prior to weaning (Forstmeier et al. 2004).

Food deprivation and restriction during late gestation affects the sexual behavior of postpartum female meadow voles, Microtus pennsylvanicus.

In many species of small mammals, including meadow voles, Microtus pennsylvanicus, females come into postpartum estrus (PPE) within 12-24 h of giving birth, allowing them to mate and become pregnant while raising the current litter. PPE females show increases in attractivity, proceptivity, and receptivity, the three components of sexual behavior, relative to females not in PPE. Several studies have shown that food deprivation and restriction reduce attractivity, proceptivity, and receptivity of females not in PPE. We tested the hypothesis that food deprivation and restriction during late gestation causes deficits and decreases the attractivity, proceptivity, and receptivity of females when they enter PPE. Our data support the hypothesis. On day 1 of lactation, females that were food deprived and food restricted produced scent marks that were significantly less attractive as those produced by control PPE females. Food deprivation but not food restriction caused females to no longer display significant preferences for the scent marks of males over those of females (proceptivity). Food deprivation and food restriction were sufficient to induce females to become significantly less sexually receptive than control females. Eleven of 12 control PPE females mated, 4 of 12 food-restricted females mated, and 3 of 12 food-deprived females mated. Dams facing food deprivation or restriction during late gestation may have to balance the benefits of mating during PPE with the increased costs associated with getting pregnant while they are lactating.