Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster)

Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.     

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     

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.     

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.     

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     

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.     

Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)

In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season. Received: 2 February 1998 / Accepted after revision: 2 November 1998     

Territory ownership and familiarity status affect how much male root voles (Microtus oeconomus) invest in territory defence

Neighbour–stranger discrimination occurs when individuals respond with more aggression to strangers than to territorial neighbours—a phenomenon termed the “dear enemy phenomenon” (DEP). We investigated the DEP with male and female root voles (Microtus oeconomus Pallas 1776) using field dyadic arena tests conducted in enclosures where we could test for the effects of familiarity (familiar versus stranger), ownership (resident versus intruder status) and resource-holding potential (body mass) on territorial behaviours. The results showed that males put more effort into territorial defence than females, and males could discriminate between neighbours and strangers. In males, aggressiveness was influenced by a significant two-way interaction between treatment and ownership. Male residents were more aggressive towards stranger intruders than towards neighbour intruders, while male intruders were less aggressive towards stranger residents than towards neighbour residents. In females, neither treatment nor ownership status had a significant effect on aggressiveness. Familiar males performed more social behaviours but less non-social behaviours than stranger males. Furthermore, there was a clear dominance hierarchy between residents and intruders in stranger dyads, with the male territory holders dominating the intruder in pairwise interactions. To our knowledge, these results demonstrate for the first time DEP in a small mammal with a known pedigree and present the first evidence for “prior resident advantage” in voles. We argue that both ownership status and familiarity status affect how much an individual invests in territory defence. The benefits of neighbour–stranger discrimination for male root voles and the absence of neighbour–stranger discrimination in female root voles are discussed.     

Costs and benefits of communal rearing to female prairie voles (<Emphasis Type="Italic">Microtus ochrogaster</Emphasis>)

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.Communicated by E. Korpimäki     

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     

The costs of male parental care and its evolution in a neotropical frog

Summary Parental care is practiced exclusively by males of the Puerto Rican frog, Eleutherodactylus coqui. Males brood clutches of direct-developing eggs in non-aquatic nest sites and defend eggs against cannibalistic nest intruders. Here, I report on energetic and mating costs incurred by males that provide parental care, and suggest how these proximate costs affect male fitness and the evolution of male parental care in this species. Energetic costs are small for brooding males in comparison to non-brooding, calling males. Brooding males had a higher frequency of empty stomachs and lost small, but significant, fractions of their initial body mass during parental care. Abdominal fat bodies of brooding males during the middle third of parental care were significantly smaller than those of calling males; those of males brooding eggs in earlier or later stages were not different. The mating cost of parental care is greater. Most brooding males cease calling during parental care. However, gravid females are available (i.e., known to mate) on most nights during the principal breeding season; hence non-calling males miss potential opportunities to mate. A mating cost was estimated by calculating nightly mating probabilities for calling males in a plot where nightly calling male densities and daily oviposition schedules were known. On average, a male exhibiting normal calling behavior would be expected to obtain a new mate once every 35.7 days. Hence a brooding male that ceased calling for a 20-day parental care period would miss, on average, 0.56 additional mates. Males that were more successful than average in attracting mates could miss up to 1.63 matings. A marginal value model (Fig. 1) is used to analyze the net effect on male fitness of parental care benefits and costs in E. coqui (Fig. 3). The model indicates that males garner the highest reproductive success by providing care from oviposition through hatching. There is no stage during the pre-hatching period at which a desertion strategy would yield higher reproductive success. In fact, the model suggests that males should provide full parental care even in the face of much higher mating costs than currently obtain in the system.     

Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling

Summary A small population of meadow voles (Microtus pennsylvanicus) in a field enclosure was studied from August to February in Apalachin, New York, USA. Radiotelemetry provided direct measures of intraspecific spacing and social nesting through the fall-winter transition. Data on weather and predation were collected concurrently. A total of 32 voles were radiotracked during 6 tracking sessions, with an average of 17.3 voles (11 to 25 range) tracked per session (Figs. 1, 2a). Discrete social nesting constellations first occurred during October, primarily as a result of the formation of extended maternal families (Figs. 1, 2e). Recruitment of adult males and offspring into these early nesting groups was male biased. The average number of voles in these groupings varied from 3.2 (Jan; 3–4 range) to 7.0 (Oct; 4–10 range); but the average number of voles that slept together at any given time, the nesting cluster, remained steady at 2.4 (2–5 range) (Fig. 2e). During late December and early January under the protection of snow, many voles shifted their home areas and nesting affiliations with the result that non-lineage nesting constellations formed (Fig. 1, 3). The thermoregulatory benefits of huddling and the threat of predation appear to be important governors of movement, group formation and dispersion. The existence of an optimum group size produces and Allee Effect that may contribute importantly to population lows and multi-annual cycles.     

Polygyny and male parental care in Savannah sparrows: effects on female fitness

Summary To determine the effects of male mating status on female fitness, we compared the reproductive success, survival, and future fecundity of female Savannah sparrows (Passerculus sandwichensis) mated to monogamous vs. polygynous males in a 5-year study on Kent Island, New Brunswick, Canada. The proportion of males with more than one mate varied from 15 to 43% between years and sites. Polygynous and monogamous males fledged young of equal size in every year of the study. Females who shared paternal care with other females laid as many eggs per clutch and clutches per season as monogamously mated females. In most years polygynously mated females showed no delay in laying a second clutch, and they suffered no reduction in fecundity the following year. Recruitment of a female's offspring into the breeding population was generally independent of her mating status. Fitness costs of being mated to a polygynous male were only apparent in one year of the study, during which females mated to polygynous males had higher over-winter mortality than those mated to monogamous males. That same year, young raised by polygynous males were only one-third as likely to survive to reproductive maturity (as inferred by returns) as those raised by monogamous males. A male's mating status had no effect on his own survivorship. A male's mating status did not necessarily reflect his contributions to raising nestlings, which may partially explain why monogamously and polygynously mated females had equal fitness. At 35 nests the proportion of food deliveries brought by individual males varied from 0 to 75%; on average, males brought fewer than 30% of all food deliveries. Yet parental care by polygynous males was no less than that of monogamous males, at least at the nests of their primary females. Secondary females tended to receive less male assistance during the nestling stage, but their reproductive success was indistinguishable from that of primary females. Females feeding young without male assistance made as many food deliveries/h as did pairs in which males brought at least 30% of all food deliveries. Unassisted females did not suffer diminished fledging success or produce smaller fledglings. The benefits of polygyny for male Savannah sparrows are clear: polygynous males recruit more surviving offspring into the breeding population than monogamous males. The fitness of females, on the other hand, appears to be unaffected by whether their mate was monogamous or polygynous except in occasional years. Polygyny may be maintained in this population by the constraints of a female-biased sex ratio, the inability of females to predict a male's paternal care based on his morphology or behavior, the poor correlation between a male's mating status and his assistance at the nest, and inconsistent natural selection against mating with a polygynous male. Correspondence to: N.T. Wheelwright     

Brood guarding and the evolution of male parental care in burying beetles

Summary Parental behavior that has an impact on the increased survival of offspring, an important factor in the evolution of parental care, can include both guarding and provisioning. The effects of these two components of parental care can be separated and quantified in the burying beetle Nicrophorus orbicollis in which both male and female cooperate to rear young. Although in the absence of competition, reproductive success is reduced by the presence of the second parent in the brood chamber, two parents dramatically reduce the probability that conspecifics will usurp the resource, replace either the male or female, kill the newly hatched brood, and produce a replacement clutch. After the establishment of the burial chamber (but not before) beetles appear to assist their mates in driving off intrasexual competitors. Male assistance in burial does not account for very much of the variance in the speed in which the carcass can be concealed nor are two parents essential to guard against insect predators. There were no significant differences in the duration of parental care by males paired with virgin and non-virgin females suggesting that paternity of the brood for which the male provides care is not a factor determining the length of care. Since male and female reproductive success is limited in Nicrophorus by access to suitable carcasses, many of the typical asymmetries in the costs and benefits of parental care are lacking. However since sperm displacement is not complete, paternity of the replacement clutch, for which the male does not provide care, may be a factor encouraging male desertion before female desertion. Other factors important in the evolution of paternal care, especially the probability of additional reproductive opportunities, are discussed.     

Food abundance and parental care in yellow warblers (Dendroica petechia)

Emlen and Oring (1977) suggested that monogamy in birds is maintained because of the need for strict biparental care. A corollary of their suggestion is that paternal care should decrease under conditions of high food abundance. An alternative is that paternal care would increase if males take advantage of the higher food abundance by trying to reduce the length of the nestling feeding period. We tested these two ideas using yellow warblers (Dendroica petechia) by providing some pairs with supplemental food, thereby reducing the importance of biparental care. However, the extra food did not decrease paternal effort, nor did it increase it (Fig. 2). Early in the nestling period experimental females brooded more but visited their nestlings less than did control females, but later, when brooding times decreased, experimental females fed their nestlings more than did control females (Fig. 3). There were no significant differences in nestling survival (Fig. 5), but nestlings in the control treatment were larger and heavier up to 6 days old (Fig. 6). The main effect of supplemental food was on maternal, not paternal behaviour. Models of biparental care assume interdependence between the parental effort of both parents. In this species, however, males and females provide for their brood independently from each other.     

Digit length ratio (2D/4D): comparing measurements from X-rays and photographs in field voles (<Emphasis Type="Italic">Microtus agrestis</Emphasis>)

The ratio of second-to-fourth digit length (2D/4D) has been suggested to be a useful adult age marker of intrauterine exposure to steroids because it should be sexually dimorphic and fixed already in utero. Numerous studies mainly on humans have supported this conclusion, but it is yet unclear how well this applies to other vertebrates. This information would be especially valuable to field biologists to whom measuring steroids in utero is often impossible. The non-human studies conducted so far have yielded inconsistent results, perhaps due to the variety of different methods employed in measuring 2D/4D. We examined the age and sex dependency and lateral asymmetry of 2D/4D in field voles (Microtus agrestis) and compared whether these effects differed between 2D/4D measurements taken from photographs and X-rays. Our results show that 2D/4D measurements from photos had a higher measurement error and gave consistently higher 2D/4D than those from X-rays. According to both measurement methods, the right paw showed higher 2D/4D values than the left paw (lateral asymmetry). Adult voles had a lower 2D/4D than juveniles when measured from X-rays, but not when measured from photographs. We found no evidence for a sex difference in 2D/4D using either of the measurement methods. Our findings thus suggest that X-rays, due to their greater accuracy, should be preferred over photographs for measuring digit ratios in rodents. Our results also indicate that in this species, 2D/4D is laterally asymmetric, but it may not be either fixed in utero or sexually dimorphic. In conclusion, 2D/4D appears to be a rather species- and method-specific measure and researchers should be careful when generalising its applicability to study early hormonal effects in vertebrates.     

Patterns of parental provisioning covary with male morphology in a horned beetle (Onthophagus taurus) (Coleoptera: Scarabaeidae)

Male dung beetles, Onthophagus taurus, are dimorphic for a secondary sexual trait, head horns. Horned males participate in the production of brood masses while hornless male do not. Here we examine the reproductive performance of females mated with males exhibiting alternative horn morphologies. We found that exposure to males may be costly for females in that it reduced the total number of brood masses produced. However, females paired with horned males produced significantly larger brood masses than females paired with hornless males or females producing broods alone. We discuss the possible selection pressures that may underly horn evolution in this genus. Received: 22 August 1997 / Accepted after revision: 19 January 1998     

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.