Effects of experience and avpr1a microsatellite length on parental care in male prairie voles (Microtus ochrogaster)

Pair-bonded males often make substantial contributions to the care of their offspring. Male parental behavior may be affected by a range of factors, including previous experience (parental or alloparental), genetic influences, and contributions by the female partner. Previous studies have shown that a microsatellite polymorphism in the regulatory region of the avpr1a gene influences aspects of paternal behavior in male prairie voles (Microtus ochrogaster). Specifically, males with longer avpr1a microsatellites groomed offspring more than did males with shorter avpr1a microsatellites. Previous experience with alloparental care also appears to influence subsequent paternal care in prairie voles. We investigated the influence of avpr1a microsatellite length and previous parental experience on paternal behavior in prairie voles two generations from the field and specially bred to exaggerate differences in avpr1a microsatellite length. We found that avpr1a microsatellite length alone did not affect any of the paternal behaviors that we measured. In contrast, males differed in parental behavior between first and second litters. Regardless of avpr1a microsatellite length, males licked/groomed the second litter less, and retrieved pups more quickly during the second compared to the first litter. Our results show that previous paternal experience may play a more important role than the length of the microsatellite in the regulatory region of the avpr1a gene in influencing paternal care.     

Male dominance,female choice and male copulatory behavior in two species of voles (Microtus ochrogaster and Microtus montanus)

Summary Female preferences for dominant males in prairie and montane voles were analyzed in two different test situations. In the first, prairie vole females preferentially spent time in proximity to dominant versus subordinate males which were housed behind a wire mesh screen. In a two-male tether test prairie voles females both preferentially associated and mated with dominant males. Montane voles, on the other hand, showed no preference in either test situation. The baseline copulatory behavior of naive montane vole males which became dominant differed significantly from those which became subordinate; no such differences were evident in the baseline copulatory behavior of naive praire voles. One hour following dominance testing, there was no difference evident between dominant and subordinate males of either species but there was a general facilitation of male copulatory behavior in both species, the effect being of greater magnitude in montane voles.     

Trichinella spiralis infection in voles alters female odor preference but not partner preference

Females may choose mates based on secondary sex traits that reflect disease resistance. Accordingly, females should be able to distinguish between unparasitized and parasitized males, and should prefer to mate with unparasitized individuals. Mate and odor preferences for uninfected males or males infected with the nematode, Trichinella spiralis, were examined among prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus). In a 15-min odor preference test, only female meadow voles distinguished between bedding from parasitized and unparasitized conspecific males, and preferred to spend time with bedding from unparasitized males. Although T. spiralis infection influenced odor preference in female meadow voles, there was no effect of infection status on mate preference among either species. Testosterone and corticosterone concentrations were not different between parasitized and unparasitized males. However, among prairie voles, males that spent an increased amount of time with females during the mate preference test had elevated testosterone concentrations. Taken together, these data suggest that (1) female meadow voles can discriminate between unparasitized and parasitized males, (2) the effects of infection on steroid hormone concentrations may be masked by the effects of social interactions, and (3) parasites may represent a selective constraint on partner preference in voles; however, the life cycle of parasites may influence female preference and should be considered in studies of female preference. Received: 23 April 1998 / Accepted after revision: 25 October 1998     

Natal dispersal and philopatry in prairie voles (Microtus ochrogaster) in relation to population density,season, and natal social environment

Summary We used intensive livetrapping to examine natal dispersal and philopatry in prairie voles (Microtus ochrogaster). The majority of male (70.0%) and female prairie voles (75.1 %) remained at the natal nest until death. Those males and females that did disperse left home at about the same age (45–55 days) and moved similar distances (28–33 m). Dispersal was more common (1) from small natal groups than from large natal groups, (2) following disappearance of parents, (3) during the breeding period than during the nonbreeding period, and (4) at low population densities than at high densities. Dispersal was not associated with level of competition for mates within natal groups, and dispersers did not differ from nondispersers in body weight. Our data do not support competition for mates or resources as important factors influencing natal dispersal in prairie voles. The absence of sex differences in dispersal tendency or distance, and our fording that more than half of dispersers had become reproductive before leaving the natal nest, lead us to suggest that inbreeding avoidance is not a primary function of dispersal in this species. Dispersal was, however, more common when potential mates within the natal group were relatives than when they were nonrelatives. Although not tested here, if family members avoid mating with one another through patterns of mate choice, then some animals may leave home in search of mates. The precise benefits associated with philopatry in prairie voles remain to be identified. Correspondence to: B. McGuire at her present address     

The nature and frequency of social interactions among free-living prairie voles (Microtus ochrogaster)

Hypotheses relating the behavior of voles to their population cycles often assume that the rate of social interaction increases with population density. To test this assumption, we examined the frequency of social interactions in a population of prairie voles (Microtus ochrogaster) over a 7-year period. In addition, we characterized space use by resident animals, patterns of visitation by nonresidents to nests, and participants in social interactions. Social groups within the population typically displayed little overlap in their use of space, even at high population densities. Nevertheless, nonresidents, particularly wandering males, were captured as visitors at nests. The number of visits per social group did not increase in a simple linear manner with population density and was particularly variable when there were fewer than 100 animals/ha. At such times, more single females and fewer pairs received visits from males than expected based on the frequency of occurrence of these groups in the population; a similar pattern was noted during periods of high population density (≥100 animals/ha) but the comparisons failed to reach statistical significance. Furthermore, at high population density, more communal groups received visits from females than expected. Patterns of visitation to communal groups were influenced by the number of adult male residents (winter only), but not by the number of adult female residents or presence of philopatric female offspring. These data indicate that the frequency of social contact in prairie voles does not increase linearly with population density and is influenced by the spacing and possible mate-guarding behavior of resident animals. Received: 7 January 1998 / Accepted after revision: 16 May 1998     

A field test of the Bruce effect in the monogamous prairie vole (Microtus ochrogaster)

The Bruce effect is a widely studied reproductive phenomenon in rodents in which exposure of pregnant females to unknown males causes termination of the current pregnancy. The Bruce effect has been reported from numerous studies in the laboratory, and one field study with the promiscuous gray-tailed vole, Microtus canicaudus, failed to support it. We conducted a field study with the monogamous prairie vole, M. ochrogaster, to determine if complete replacement of the male population every 10-14 days affected pregnancy and juvenile recruitment. The mean days to first parturition for control and treatment females were 36.8 and 44.4 days. Fifty-five percent of control females and 33% of treatment females conceived within the first 14 days of the study. All control females and 79% of treatment females successfully delivered at least one litter. These differences between treatment and control populations provide minimal support for the Bruce effect when compared with results from laboratory studies. Nulliparous females may have experienced some pregnancy disruption, but not parous females. Removal of mates, rather than exposure to strange males, may have contributed more to the lower reproductive success of treatment females than exposure to strange males. Treatment females, however, had lower juvenile recruitment than controls, which may have been due to infanticide from strange males. Our results are more similar to those of the field study of the gray-tailed vole than predicted, based on laboratory studies of prairie voles.     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

High male reproductive success in a low-density Antarctic fur seal (Arctocephalus gazella) breeding colony

Understanding how population density influences mating systems may lead to important insights into the plasticity of breeding behavior, but few natural systems allow for such studies. Antarctic fur seals (Arctocephalus gazella) provide an interesting model system because they breed in colonies of varying densities. Previous studies have largely focused on a high-density site at Bird Island, South Georgia. Here, 13 highly polymorphic microsatellite loci were used to conduct a genetic analysis of a low-density breeding colony of this species at Livingston Island, approximately 1,600 km south of South Georgia. The majority of adults seen ashore (n?=?54) were sampled together with every pup born (n?=?97) over four consecutive years. Paternities were confidently assigned for 34 out of the 97 pups. Two out of 23 sampled males accounted for the paternity of 28 % of all pups sampled during the study and 82 % of the pups with an assigned father. Moreover, a full likelihood pedigree inference method assigned a further eight paternities to a single unsampled male seal that is inferred to have held a territory during the season before the study began. The most successful males in our study easily surpassed the previous record for the total number of pups sired per male seal for the species. Furthermore, we identified two triads of full siblings implying that their parents remated in three consecutive years. These findings suggest that territorial male fur seals may achieve greater success in monopolizing access to breeding females when population density is relatively low.     

Genital morphology linked to social status in the bank vole (<Emphasis Type="Italic">Myodes glareolus</Emphasis>)

Since genital morphology can influence the outcome of post-copulatory sexual selection, differences in the genitalia of dominant and subordinate males could be a factor contributing to the fertilisation advantage of dominant males under sperm competition. Here we investigate for the first time if penile morphology differs according to male social status in a promiscuous mammal, the bank vole (Myodes glareolus). In this species, dominant males typically achieve higher reproductive success than subordinates in post-copulatory sexual selection, and male genital morphology is complex, including both a baculum (os penis) and penile spines. Our results show that despite no difference in body size associated with male social status, baculum width is significantly larger in dominant male bank voles than in subordinates. We also found evidence of positive allometry and a relatively high coefficient of phenotypic variation in the baculum width of male bank voles, consistent with an influence of sexual selection. By contrast, baculum length and three measures of penile spinosity did not differ according to male social status or show evidence of positive allometry. We conclude that dominant male bank voles may benefit from an enlarged baculum under sperm competition and/or cryptic female choice and that differences in penile morphology according to male social status might be important but as yet largely unexplored source of variation in male reproductive success.     

The anxious vole: the impact of group and gender on collective behavior under life-threat

Social animals behave collectively in order to maintain a cohesive group. This collective behavior is often led by a few individuals of specific gender, social rank, or spatial physical location in the group (i.e., perimeter or front). We examined how individual social voles (Microtus socialis) in same-gender compared with mixed-gender groups respond to an owl attack. We found that anxiety level, as measured by the time that each individual spent in less-sheltered sectors (open arms of elevated plus-maze and center of open arena), was affected by both the social context and the gender of the tested individuals. While both female and male voles generally reduced their activity in the open following owl attack, males in mixed-gender groups were exceptional in dichotomizing into those that spent a short period and those that spent a long period in the open arms of the plus-maze. Based on the similar responses of the same-gender groups, we suggest that anxiety is contagious, and based on the lower anxiety level of the mixed-gender groups, we suggest that natural groups that comprise both males and females are better able to cope with life-threat compared with same-gender groups. Finally, we suggest that the differential responses of males in the mixed-gender groups were due to a few males that displayed a low level of anxiety. These males were probably individuals of high social rank, and their response reflects their natural protective role, as previously described in social voles.     

Reproductive success of parasitized males in a marine reef fish

Parasitism is hypothesized to reduce reproductive success in heavily parasitized males because females may preferentially mate with less parasitized males (parasite-mediated sexual selection) or parasites may compromise male competitiveness. In marine systems, this hypothesis is largely unexplored. This paper provides the first confirmed record of a copepod ectoparasite (Caligus buechlerae Hewitt 1964) on the common triplefin (Forsterygion lapillum) and evaluates the hypothesis that males parasitized with C. buechlerae experience lower reproductive success than unparasitized males (as determined by the presence and area of eggs within male nests). We found that 38 % of males we surveyed were infected with at least one C. buechlerae, with a median of two individuals per infected male. About 32 % of males were defending eggs, with 62.5 % of those males infected with at least one parasite. Males of greater total length (TL) were both more likely to be infected and more likely to be defending eggs. However, when statistically accounting for the effects of TL, parasite infection had no effect on the probability of defending eggs, or the average surface area of eggs when present. Positive covariation in fish length, the presence of eggs and parasite infection observed here potentially suggest that the importance of parasitic infection on reproductive success may depend upon the strength of selection for larger male body size. Our study is one of the few studies to investigate the effects of ectoparasites on reproductive success in reef fish and also provides a quantitative measure of infection for a widespread species within New Zealand.     

Multiple paternity in meadow voles (Microtus pennsylvanicus): investigating the role of the female

Multiple paternity in single litters conceived in the wild was recently demonstrated in meadow voles (Microtuspennsylvanicus). In this study, we used an experimental approach (males tethered and females allowed to mate freely with one or several males) to investigate the role of female meadow voles in multiple paternity. We found that among 29 (of 39) females that copulated during our experiment, 79.3% chose to mate with more than one male. Female behavior in meadow voles thus clearly promotes multiple paternity and their role is an active one. Some of the hypotheses explaining promiscuity in meadow voles should be reconsidered in light of this result. We do not know the primary determinant of female mate choice, but male body mass played a secondary role in driving female preferences. The partial dependence between male body mass and female choice, coupled with the active role played by females, indicates that intersexual selection has the potential for reinforcing the effects of intrasexual selection (male-male dominance relationships) in this species. Finally, we demonstrate that the time period over which tests are conducted is an important part of the design of experiments aimed at understanding the role of females in multiple paternity. Received: 14 April 1998 / Accepted after revision: 12 September 1998     

Pre-copulatory sexual selection in the cigarette beetle Lasioderma serricorne

Traditional concepts of sexual selection and sexual conflict make different predictions about the costs and benefits to females of exposure to males with higher mating success. The traditional concepts of sexual selection assume that females benefit from their mate choices, whereas sexual conflict assumes that the females suffer greater costs by mating with males who have greater mating success and thus reduce their fitness. In order to understand how mate choice evolves, it is necessary to estimate the overall effect of mate choice on female fitness. However, relatively few studies have conducted that investigation. In this study, we investigated the direct and indirect effects of mating with attractive males on the fitness of females in the cigarette beetle Lasioderma serricorne. Mating with attractive males increased the number of female offspring but did not affect female longevity. Additionally, we found evidence that attractive males sire highly attractive sons. Thus, mating with an attractive male provides direct and indirect benefits but no fitness cost to female L. serricorne.     

D-Pulegone: A feeding deterrent to deer mice (Peromyscus maniculatus) and prairie voles (Microtus ochrogaster)

Summary D-Pulegone, a monoterpene present in pennyroyålMentha sp. is repellent to a number of vertebrates, decreasing consumption of feed and granular particles. In the present study, several tests were used to determine the reliability of this substance as a feeding deterrent. D-Pulegone (10mM—1M) applied as a coating to apple pieces significantly (P < 0.001) decreased ingestion by deer mice,Peromyscus maniculatus, and prairie voles,Microtus ochrogaster. The deterrent effect of d-pulegone was not diminished following multiple exposures suggesting that this compound may be a promising candidate for use a a general vertebrate repellent. The inhibitory effect of 1M d-pulegone on apple ingestion in voles was abolished when contact was prevented by encasing the stimulus solution in plastic mesh capsules. We conclude that while d-pulegone has repellent properties following direct contact, volatile exposure alone may not be sufficient to elicit avoidance behavior.     

Scent mediation of intraspecific,interspecific, and intergeneric agonistic behavior among sympatric species of voles (Microtinae)

Summary The hypothesis that the posterolateral scent glands of male microtine rodents (Muridae) direct the attacks of other males was tested.Montane voles (Microtus montanus) and sagebrush voles (Lagurus curtatus) were established as residents in terraria, and conspecific and heterospecific males, from which posterolateral scent glands had been unilaterally removed, were introduced. More attacks by residents were aimed at the glandular sides than at the glandless sides. Male M. montanus also attacked the unilateral hip gland of longtail voles (M. longicaudus), the growth of which had been induced by exogenous hormone inasmuch as this species does not normally possess these glands. Resident male M. longicaudus did not similarly attack the induced glands of conspecific males.The findings are related to demographic patterns, mterspecific relationships, and the evolutionary development of posterolateral scent glands among microtine rodents.     

Determinants of male spacing behavior in microtines: an experimental manipulation of female spatial distribution and density

Theory on microtine mating systems predicts that male spacing behavior will be related to female spatial and temporal distribution. However, data from a natural population of field voles, Microtus agrestis, indicated a potential influence of female density on the spacing behavior of males. Therefore, I experimentally investigated the relative importance of female density and female spatial distribution for the spacing behavior of males in M. agrestis. Males were radio-tracked in enclosed natural habitats in which females at different densities were placed in two different spatial arrangements: clumped versus even distribution. Female density was the main factor determining male spacing behavior. At the high female density males had smaller home ranges and moved shorter distances between radio-tracking recordings. Also, home ranges were more exclusive at high female density. However, since there was a significant positive correlation between home range size and range overlap, range exclusiveness seemed to be influenced by female density indirectly through the effect of range size. Female spatial distribution, on the other hand, had no influence on male home range exclusiveness.     

Genetic relationship between offspring and guardian adults of a rhacophorid frog and its care effort in response to paternal share

The rhacophorid frog, Kurixalus eiffingeri, is one of only a few frog species that exhibits polyandry and paternal care of eggs. Previous studies predicted that multiple paternity within an egg clutch could influence the degree of paternal care and reproductive strategies. We used microsatellite DNA markers to assess the prevalence of multiple paternity within egg clutches and the relationship between male paternal care and the percent of male’s genetic contribution to the clutch, i.e., paternal share. We conducted field observations of paternal care and collected tissues from both male frogs and tadpoles for parentage analyses. Our results showed that at least five out of 31 egg clutches had multiple paternity. Attending males were always the genetic fathers of some, if not all of the eggs in the clutch they guarded. All egg clutches except one were attended by one male frog but the attending male did not necessarily sire the majority of offspring. Multiple paternity in all cases consisted of two fathers and one mother and most likely resulted from synchronous polyandry. Paternal care effort correlated significantly with the male’s genetic contribution to the clutch, suggesting that male frogs adjust the effort expended in care in response to paternal share. In addition, our results suggest that externally fertilizing species with parental care and multiple paternity may develop novel reproductive and behavioral strategies to safeguard their parental investment and overcome sperm competition.     

Female tactile cues maximize paternal behavior in prairie voles

Most monogamous male mammals display parental care, but the mechanism by which they become motivated to care for infants remains unknown. We used prairie voles (Microtus ochrogaster) as a model of biparental species to test the hypothesis that physical contact with a female enhances male parental responsiveness before the birth of offspring. We tested four groups of males: mated with physical contact with their mate, mated with only distal cues from their mate, mated with no cues, and unmated with distal cues from a female. The subjects were placed in an oversized cage divided into two compartments by a perforated barrier. At mid-gestation, the bedding and females were removed, and the males’ responses toward two infants were videotaped. Although most males behaved parentally, mated males exposed to their mate’s tactile or distal cues approached the young faster and were more likely to care for both infants than unmated males which received female distal cues. Males who had physical contact with their mate showed “kyphosis” (a crouching position over infants) and contacted infants more frequently than mated males which received no cues from their mate or unmated males which received female distal cues. Furthermore, the frequency of non-social behaviors was lowest in mated males that had physical contact with their mate. The data suggest that exposure to female distal cues after mating is sufficient to increase male parental attentiveness, but female somatosensory cues affect the male's tendency to remain in physical contact with infants.     

Experience affects mating behavior, but does not impact parental reproductive allocation in a lizard

Investment into reproduction is influenced by multiple factors and varies substantially between males and females. Theory predicts that males should adjust their ejaculate size or quality in response to variation in female experience or phenotypic quality. In addition, sperm investment by males may also be influenced by their own status and experience. Although such adjustments of male ejaculate size can impact reproductive success (via fertilization success), fitness returns from male sperm investment may be influenced (either limited or facilitated) by the level of maternal investment. To test this hypothesis, we conducted an experiment that simultaneously evaluated the effect of paternal and maternal experience (which incorporates mating status, age, body size, and other related variables) on paternal sperm investment and maternal reproductive allocation in the lizard Anolis sagrei. During staged mating trials, experienced males were more likely to copulate with females, but these individuals were less likely to transfer sperm during mating than were naïve individuals. Maternal experience had no impact on these mating behaviors. In contrast to expectations, experience and phenotypic quality (of both sexes) had no impact on male ejaculate size or quality (proportion of live sperm) or on maternal reproductive investment (in terms of egg size and yolk steroids). These findings were intriguing given the mating system and past evidence for differential maternal investment in relation to sire quality in A. sagrei. The results found in this study highlight the complexity of reproductive investment patterns, and we urge caution when applying general conclusions across populations or taxa.     

Polyandry and paternity in a wild population of the swordtail Xiphophorus nigrensis

Genetic analyses of parentage provide crucial information about the prevalence of polyandry and the potential for sexual selection to operate in wild populations. In the swordtail Xiphophorus nigrensis, large males are thought to have a competitive advantage due to their superiority in male–male contests and attractiveness to females, who are presumed to mate multiply. I examined the distribution of paternity within broods, the relationship between male body size and paternity and the effect of sire number on fecundity from females collected in the field. Sixty-one percent of females produced offspring from two to four males, with 70% of the offspring typically sired by one of the males represented in the brood. Male body size did not affect paternity share or whether females were multiply mated, as predicted if precopulatory sexual selection has a strong effect on the outcome of postcopulatory sexual selection. Female fecundity increased with the number of sires; however, this relationship was not observed when the smallest broods, where multiple mating is more difficult to detect, were excluded from the analysis. The high levels of multiple paternity and reproductive skew suggest that postcopulatory sexual selection has important evolutionary consequences in X. nigrensis. Traits important in precopulatory sexual selection, such as male body size, however, are more likely to affect sexual selection by increasing the number of mates obtained rather than paternity share within broods.