Total huddling time of trio-housed SD females was indistinguishable from that of SD females housed in same-sex pairs from weaning i. Females housed in winter day lengths have smaller uteri than females housed in summer-like long days LDs [ 16 ].
The right panel displays the same 14 tests divided into groups based on whether the test was the one in which a given focal vole huddled with its partner more Trio pref. Total time spent huddling with the partner versus stranger was compared within each treatment group using t -tests assuming unequal variances; groups that huddled ificantly more with the partner than the stranger were considered to exhibit a partner preference.
Descriptions of interactions were recorded as annotations at the end of each file. Unlike females Fig. SD in total or partner-specific huddling time, or time spent in vole-occupied chambers Fig. In both day lengths, males spent little time huddling with strangers. Males also formed same-sex social attachments, but unlike female affiliative behavior, male partner preferences were not ificantly affected by day length.
Comparison of behavior of trio-housed voles from either a single litter SD trio or three distinct litters SD mixed trio to pair-housed voles. Experiment 2 tested whether females can form social bonds Extreme 93561 female sex more than one individual concurrently. Specific male-male social preferences have rarely been documented in rodents [ 22 ]. Breeders were housed in opaque cages containing a plastic nest box. Male home ranges in spring and summer are larger than those of females, and substantially overlap those of other males, as well as multiple Extreme 93561 female sex [ 489 ].
The present experiments characterize several aspects of same-sex social bond formation, including the role of gender and day length, the capacity to form concurrent attachments to multiple partners, the influence of kinship between partners, and the effects of duration of cohabitation. Data for females shown for comparison have been ly published [ 16 ]. Briefly, the apparatus consisted of three plastic cages: a rear chamber connected by separate tubes to two front chambers. In their study, exposure to the first and second partner occurred consecutively in adulthood.
As there was no basis for an expectation that LD males would be as antisocial as LD females, we tested the hypothesis that males more readily form partner preferences with each other than do females during summer-like LDs. The typical winter social group of up to 10 meadow voles [ 12 ] provides an opportunity for the formation of multiple social attachments. The present study demonstrates that same-sex social attachments in short day lengths are not exclusive; females formed concurrent attachments with more than one individual, and with non-kin as well as siblings.
Focal voles from both same-litter and mixed-litter trios displayed ificant partner preferences for a randomly selected cage-mate. These mixed-sex groups consist of 3—10 voles that sleep in clusters of 2—3 [ 12 ].
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Video files were scored at 4x speed by an experimenter using a custom program to record counts and durations of presence in each chamber and of huddling, defined as side-by-side contact of the focal and tethered voles. Tethers were affixed to the chamber lids and permitted movement of the tethered vole throughout half the chamber. In winter months, male meadow voles caught in the field are typically nonscrotal [ 13 ].
One member of each test-pair was deated the focal untethered vole. These SD females can form selective partner preferences for either a male or female cage mate [ 16 — 18 ], whereas LD females exhibit markedly reduced same-sex social behavior in laboratory partner preference tests [ 16 ] and in the field [ 419 ].
Partner preferences between females were established within one day of cohousing and did not intensify with greater durations of cohabitation. We determined whether more than one bond can form between littermates, as well as whether multiple bonds could form between non-kin. Fifty-four female meadow voles were weaned into groups of three individuals 18 trios. Male right panels and female left panels same-sex behavior huddling.
Tests were conducted as described in Beery et al. In contrast, meadow voles Microtus pennsylvanicusin common with the vast majority of rodents, are polygamous and display multiple paternity within litters [ 4 — 6 ].
Apparatuses were washed thoroughly after each contact with voles. One contributing factor may be ificant differences in oxytocin receptor distributions in the brains of females in LDs versus SDs [ 17 ]; oxytocin mediates opposite sex partner preference formation in prairie voles [ 20 ] and may affect nonsexual social behavior [ 21 ]. The positions of the partner and stranger left versus right chamber were alternated between tests of each type.
Neither total time huddling nor huddling time with the partner differed between tests 1 and 2 Fig. The possibility remains that each focal vole formed a preference for only a single cage-mate, and the first and second tests did not differ because an equal proportion of the group preferred the first partner as preferred the second partner.
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In the repeat test the original focal vole was offered a choice between its other cage-mate and a novel stranger. B Mean time focal voles spent in the same chamber as the partner or the stranger during a 3 h test. Louis MO and tap water were available ad libitum. Finally, we examined the effects of different cohousing intervals on partner preference formation, in order to determine minimum exposure intervals that preferentially promote the formation of same-sex bonds and whether duration of exposure affects the strength of the partner preference.
Partner preference in individual trials was inferred when the focal vole spent at least twice as much time in side-by-side contact with the familiar as with the unfamiliar vole as in prior studies [ 1618 ]. Adult meadow voles Microtus pennsylvanicus are solitary in the spring—summer reproductive season, but during Extreme 93561 female sex months, females and males are socially tolerant and aggregate in groups.
Asterisks above the brackets denote ificant differences in total huddling or chamber time between bracketed groups. Scoring was conducted without knowledge of treatment groups. Experiment 1 assessed the degree of same-sex partner preference formation in male meadow voles housed in LDs and SDs.
Partner preference tests were conducted between 80— days on a focal vole provided access to its cage-mate the partner and an unfamiliar male the stranger of similar age that also had been cohoused in a same-sex pair.
Breeding pairs were continuously cohoused in LDs light:dark cycle. This leaves open the possibility that multiple attachments in meadow voles can occur under other circumstances, such as when the potential partners are available concurrently. A control group consisted of unpaired females of the same age tested with two strangers. Data from a study [ 16 ] involving LD and SD female pairs, cohoused as littermates from weaning and tested in the same apparatus as in the present study, are shown for comparison in multiple figures.
This behavioral difference is triggered by day length: female meadow voles housed in short, winter-like day lengths form same-sex partner preferences, whereas those housed in long, summer-like day lengths are less social. Male meadow voles are considered less territorial than females [ 15 ] but do engage in agonistic encounters with neighbors in summer months [ 1419 ]; seasonal agonism is particularly directed towards unfamiliar individuals [ 15 ], but is less pronounced in males than females [ 1924 ].
Food mouse chow no. These data are discussed in the context of field behavior and the physiological mechanisms supporting social behavior in voles.
Asterisks above the grey bars denote ificant within-group differences in time spent with partners versus strangers. Same-sex social preferences have ly been demonstrated only between meadow vole littermate pairs. In winter, meadow vole home ranges contract and those of multiple individuals overlap substantially. Ovariectomy does not increase social behavior in LD female meadow voles, however, suggesting that seasonal differences beyond altered ovarian hormone secretion affect variation in behavior.
Same-sex social behavior in meadow voles: multiple and rapid formation of attachments
B Mean time focal females spent in the same chamber as the partner or the stranger during a 3 h test. Offspring were weaned as singletons, pairs, or trios, as described below, and transferred to SDs light:dark cycle or maintained in LDs. Dark onset was PST in both photoperiods.
Effects of day length LD or SD were also analyzed using t -tests assuming unequal variance. Investigations of meadow vole social behavior may yield insights into the mechanisms that support sociality outside of reproductive contexts.
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Time spent in occupied chambers by voles of both trio types was indistinguishable from the behavior of SD pairs, and ificantly different from LD pairs. Even after sorting of paired tests, no ificant difference in preference for the two partners was detectable. The letters N. S above a bracket indicate no ificant differences in total huddling times between groups. The period of data collection overlapped for these studies. Statistical analyses were performed using JMP 7.
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Experiment 3 assessed the time course of same-sex social bond formation. Seasonal changes in meadow vole behavior are concomitant with seasonal changes in reproductive physiology in both sexes, and social behavior appears to be at least partly dependent on the reduced secretion of gonadal steroids. Intermale aggression towards unfamiliar individuals increases in spring months as the gon undergo recrudescence [ 1415 ], and castration of field-caught males reduces intermale aggression [ 13 ].
Pairings between non-sibling females of the same age were in effect for 1.
Neurobiological analysis of social behavior of the genus Microtus has focused primarily on prairie voles, a socially monogamous species that forms long-lasting attachments with an opposite Extreme 93561 female sex partner [ 23 ]. Experimenters were absent from the test room during recording of social behavior. The left panel displays huddling data from these voles in tests 1 and 2. Social groups formed at the end of the breeding season typically are initially comprised of a female and her most recent offspring, with immigrant males ing the group throughout the fall [ 10 ].
Focal females were tested for partner preference between 80— days of age with a randomly selected member of the trio and a stranger. Asterisks denote ificant differences within groups between partners and strangers. The social and reproductive systems of arvicoline formerly microtine rodents are diverse, including social monogamy, polygamy, and territoriality among females, males, or both sexes [ 1 ]. Because male meadow voles aggregate with other males in winter [ 12 ], and SD-housed males display equal preferences for the odors of SD males and females [ 23 ], we speculated that SD males might form specific social attachments with other males.
Among field populations of meadow voles in several habitats, the reproductive season is characterized by female maintenance of exclusive territories that rarely overlap those of other females [ 48 ]. During winter months in the field, or when housed in short day lengths SDs in the laboratory, meadow voles become non-reproductive and shift their behavior to a social phenotype.
Summer contact between males and females is limited to reproductive activity, as suggested by the absence of captures of opposite sexed adult meadow voles in a single trap [ 8 ], an event that occurs regularly in socially monogamous prairie voles [ 2 ]. Little additional information is available about long-term same-sex attachments in meadow voles. C Focal voles from 7 trios were tested one week after the initial test test 1 but with the second cage mate test 2.
Tethered voles were acclimated to the chamber for 5 min before the focal animal was placed in the rear chamber Extreme 93561 female sex allowed to move freely for the duration of the 3 hour test. On the day of the behavioral test, the other member of the co-housed test-pair the partner and an unfamiliar vole from the same treatment condition the stranger were tethered in separate front chambers. Seven trios were re-tested one week after the initial partner preference test.
Females also migrate during this period [ 11 ], and by late December to early January, social constellations no longer represent family lineages [ 10 ].
Exposure to endogenous or exogenous estradiol reduces same-sex huddling behavior in females [ 16 ]. Non-sexual social behavior forms the basis for group living in many species [ 7 ] and is an important component of complex societies.