Peer Social Environment Impacts Behavior and Dopamine D1 Receptor Density in Prairie Voles (Microtus ochrogaster).

Prairie voles (Microtus ochrogaster) are socially monogamous rodents that form selective, long-lasting relationships with mates and with same-sex peers. It is unknown to what extent mechanisms supporting 'peer relationships' are similar to those involved in mate relationships. The formation of pair bonds is dependent on dopamine neurotransmission, whereas the formation of peer relationships is not, providing evidence of relationship type-specificity. The current study assessed endogenous structural changes in dopamine D1 receptor density in male and female voles across different social environments, including long-term same-sex partnerships, new same-sex partnerships, social isolation, and group housing. We also related dopamine D1 receptor density and social environment to behavior in social interaction and partner preference tests. Unlike prior findings in mate pairs, voles paired with new same-sex partners did not exhibit upregulated D1 binding in the nucleus accumbens (NAcc) relative to controls paired from weaning. This is consistent with differences in relationship type: D1 upregulation in pair bonds aids in maintaining exclusive relationships through selective aggression, and we found that formation of new peer relationships did not enhance aggression. Isolation led to increases in NAcc D1 binding, and even across socially housed voles, individuals with higher D1 binding exhibited increased social avoidance. These findings suggest that elevated D1 binding may be both a cause and a consequence of reduced prosociality. These results highlight the neural and behavioral consequences of different non-reproductive social environments and contribute to growing evidence that the mechanisms underlying reproductive and non-reproductive relationship formation are distinct. Elucidation of the latter is necessary to understand mechanisms underlying social behavior beyond a mating context.

Selectivity and Sociality: Aggression and Affiliation Shape Vole Social Relationships.

The formation of selective social relationships is not a requirement of group living; sociality can be supported by motivation for social interaction in the absence of preferences for specific individuals, and by tolerance in place of social motivation. For species that form selective social relationships, these can be maintained by preference for familiar partners, as well as by avoidance of or aggression toward individuals outside of the social bond. In this review, we explore the roles that aggression, motivation, and tolerance play in the maintenance of selective affiliation. We focus on prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) as rodent species that both exhibit the unusual tendency to form selective social relationships, but differ with regard to mating system. These species provide an opportunity to investigate the mechanisms that underlie social relationships, and to compare mechanisms supporting pair bonds with mates and same-sex peer relationships. We then relate this to the role of aggression in group composition in a comparative context.

Social selectivity and social motivation in voles.

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar versus unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females versus males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

What factors drive the formation of social relationships can vary greatly in animals. While some individuals may be motivated to find social partners, others may just tolerate being around others. A desire to avoid strangers may also lead an individual to seek out acquaintances or friends. Sometimes a mix of these factors shape social behavior. Studying motivation for social relationships in the laboratory is tricky. Traditional laboratory animals like mice and rats do not bond with specific peers or mates. But small burrowing rodents called voles are a more relationship-oriented alternative to mice and rats. Prairie voles form selective and enduring preferences for both their mates and familiar same-sex peers. Meadow voles on the other hand, live alone much of the year but move in with other animals over the winter. Beery et al. show that social motivation in voles varies by relationship type, species and sex. In the experiments, voles were first trained to press a lever to get a food reward. Then, the food reward was swapped with access to familiar or unfamiliar voles. Female prairie voles strived to be with animals they knew rather than to be with strangers, while male prairie voles tried hard to access any female. In contrast, meadow voles did not overly exert themselves to access other animals. Beery et al. then measured oxytocin receptor levels in the brains of prairie voles. Prairie voles that had more receptors for oxytocin in part of their brain known as the nucleus accumbens worked harder to access their familiar partner. But individuals with more oxytocin receptors in the bed nucleus of the stria terminalis were more likely to attack an unfamiliar animal. The meadow voles' behavior suggests that they are more motivated by tolerance of familiar animals, while the female prairie voles may find it rewarding to be with animals they have bonded with. These differences may help explain why these two species of vole have evolved different social behaviors. The experiments also suggest that oxytocin ­ which is linked with maternal behavior ­ plays an important role in social motivation. Learning more about the biological mechanisms that underlie vole social behaviors may help scientists identify fundamental aspects of social behavior that may apply to other species including humans.

The role of dopamine signaling in prairie vole peer relationships.

Dopamine signaling mediates the formation of some types of social relationships, including reproductive pair bonds in the socially monogamous prairie vole (Microtus ochrogaster). In addition to these pair bonds with mates, prairie voles demonstrate selective preferences for familiar same-sex peers. The dependence of peer relationships on dopamine signaling has not been tested, and the mechanisms supporting these relationships may differ from those underlying pair bonds. We examined the effects of pharmacological manipulations of dopamine signaling on peer partner preference and socially conditioned place preference in female prairie voles. Haloperidol blockade of dopamine receptors at multiple doses did not alter selective preferences for familiar same-sex partners, suggesting that dopamine neurotransmission is not necessary for the formation of prairie vole peer relationships, unlike mate relationships. Dopamine receptor agonist apomorphine facilitated peer partner preferences under conditions normally insufficient for partner preference formation; however, in the absence of effects from blockade, it is difficult to distinguish between a role for dopamine in partner preference formation and the generally rewarding properties of a dopamine agonist. Prairie voles exhibited socially conditioned place preferences for new but not long-term same-sex peers, and these preferences were not blocked by haloperidol. These results suggest that prairie vole peer relationships are less dependent on dopamine signaling than pair bonds, while still being rewarding. The data support distinct roles of dopamine and motivation in prairie vole peer relationships relative to mate relationships, suggesting that reproductive bonds are mediated differently from non-reproductive ones.

Persistent mosquito fogging can be detrimental to non-target invertebrates in an urban tropical forest.

BACKGROUND: Human population growth has led to biodiversity declines in tropical cities. While habitat loss and fragmentation have been the main drivers of urban biodiversity loss, man-made interventions to reduce health risks have also emerged as an unintentional threat. For instance, insecticide fogging to control mosquito populations has become the most common method of preventing the expansion of mosquito-borne diseases such as Dengue. However, the effectiveness of fogging in killing mosquitoes has been called into question. One concern is the unintended effect of insecticide fogging on non-target invertebrates that are crucial for the maintenance of urban ecosystems. Here, we investigate the impacts of fogging on: (1) target invertebrate taxon (Diptera, including mosquitoes); (2) non-target invertebrate taxa; and (3) the foraging behavior of an invertebrate pollinator taxon (Lepidoptera) within an urban tropical forest. METHODS: We carried out fogging with Pyrethroid insecticide (Detral 2.5 EC) at 10 different sites in a forest situated in the state of Selangor, Peninsular Malaysia. Across the sites, we counted the numbers of knocked-down invertebrates and identified them based on morphology to different taxa. We constructed Bayesian hierarchical Poisson regression models to investigate the effects of fogging on: (1) a target invertebrate taxon (Diptera) 3-h post-fogging; (2) selected non-target invertebrate taxa 3-h post-fogging; and (3) an invertebrate pollinator taxon (Lepidoptera) 24-h post-fogging. RESULTS: A total of 1,874 invertebrates from 19 invertebrate orders were knocked down by the fogging treatment across the 10 sites. Furthermore, 72.7% of the invertebrates counted 3-h post-fogging was considered dead. Our regression models showed that given the data and prior information, the probability that fogging had a negative effect on invertebrate taxa 3-h post-fogging was 100%, with reductions to 11% of the pre-fogging count of live individuals for the target invertebrate taxon (Diptera), and between 5% and 58% of the pre-fogging count of live individuals for non-target invertebrate taxa. For the invertebrate pollinator, the probability that fogging had a negative effect 24-h post-fogging was also 100%, with reductions to 53% of the pre-fogging count of live individuals. DISCUSSION: Our Bayesian models unequivocally demonstrate that fogging has detrimental effects on one pollinator order and non-target invertebrate orders, especially taxa that have comparatively lower levels of chitinisation. While fogging is effective in killing the target order (Diptera), no mosquitos were found dead in our experiment. In order to maintain urban biodiversity, we recommend that health authorities and the private sector move away from persistent insecticide fogging and to explore alternative measures to control adult mosquito populations.

Affiliation, Aggression, and Selectivity of Peer Relationships in Meadow and Prairie Voles.

Relationships between adult peers are central to the structure of social groups. In some species, selective preferences for specific peers provide a foundation for consistent group composition. These preferences may be shaped by affiliation toward familiar individuals, and/or by aversion to unfamiliar individuals. We compared peer interactions in two vole species that form selective preferences for familiar same-sex individuals but differ in mating system. Prairie voles (Microtus ochrogaster) form pair bonds with mates and may reside in family groups. Meadow voles (Microtus pennsylvanicus) are promiscuous breeders that form communal winter groups in the wild, and exhibit greater social behavior in short day (SD) lengths in the laboratory. We characterized affiliative, anxiety-like, and aggressive interactions with familiar and novel same-sex conspecifics in meadow and prairie voles housed in summer- or winter-like photoperiods. Species differences in affective behaviors were pronounced, with prairie voles exhibiting more aggressive behavior and less anxiety-like behavior relative to meadow voles. Meadow voles housed in short (vs. long) day lengths were more affiliative and more interactive with strangers; prosocial behavior was also facilitated by a history of social housing. Prairie voles exhibited partner preferences regardless of sex or day length, indicating that selective peer preferences are the norm in prairie voles. Prairie vole females formed preferences for new same-sex social partners following re-pairing; males were often aggressive upon re-pairing. These data suggest that preferences for familiar peers in prairie voles are maintained in part by aggression toward unfamiliar individuals, as in mate partnerships. In contrast, social tolerance is an important feature of meadow vole peer affiliation, demonstrated by low aggression toward unfamiliar conspecifics, and consistent with field data on winter tolerance.

Neural Circuits Underlying Rodent Sociality: A Comparative Approach.

All mammals begin life in social groups, but for some species, social relationships persist and develop throughout the course of an individual's life. Research in multiple rodent species provides evidence of relatively conserved circuitry underlying social behaviors and processes such as social recognition and memory, social reward, and social approach/avoidance. Species exhibiting different complex social behaviors and social systems (such as social monogamy or familiarity preferences) can be characterized in part by when and how they display specific social behaviors. Prairie and meadow voles are closely related species that exhibit similarly selective peer preferences but different mating systems, aiding direct comparison of the mechanisms underlying affiliative behavior. This chapter draws on research in voles as well as other rodents to explore the mechanisms involved in individual social behavior processes, as well as specific complex social patterns. Contrasts between vole species exemplify how the laboratory study of diverse species improves our understanding of the mechanisms underlying social behavior. We identify several additional rodent species whose interesting social structures and available ecological and behavioral field data make them good candidates for study. New techniques and integration across laboratory and field settings will provide exciting opportunities for future mechanistic work in non-model species.

Comparative role of reward in long-term peer and mate relationships in voles.

This is a contribution to SI: SBN/ICN meeting. In social species, relationships may form between mates, parents and their offspring, and/or social peers. Prairie voles and meadow voles both form selective relationships for familiar same-sex peers, but differ in mating system, allowing comparison of the properties of peer and mate relationships. Prairie vole mate bonds are dopamine-dependent, unlike meadow vole peer relationships, indicating potential differences in the mechanisms and motivation supporting these relationships within and/or across species. We review the role of dopamine signaling in affiliative behavior, and assess the role of behavioral reward across relationship types. We compared the reinforcing properties of mate versus peer relationships within a species (prairie voles), and peer relationships across species (meadow and prairie voles). Social reinforcement was assessed using the socially conditioned place preference test. Animals were conditioned using randomly assigned, equally preferred beddings associated with social (CS+) and solitary (CS-) housing. Prairie vole mates, but not prairie or meadow vole peers, conditioned toward the social cue. A second study in peers used counter-conditioning to enhance the capacity to detect low-level conditioning. Time spent on CS+ bedding significantly decreased in meadow voles, and showed a non-significant increase in prairie voles. These data support the conclusion that mate relationships are rewarding for prairie voles. Despite selectivity of preferences for familiar individuals in partner preference tests, peer relationships in both species appear only weakly reinforcing or non-reinforcing. This suggests important differences in the pathways underlying these relationship types, even within species.

Water vapor absorption allows for volume expansion during molting in Armadillidiumvulgare and Porcelliodilatatus (Crustacea, Isopoda, Oniscidea).

Arthropods require periodic molting in order to grow which presents a number of challenges to terrestrial taxa. Following ecdysis, the pliant new cuticle is susceptible to buckling under gravity and requires elevated hydrostatic pressure for support. Terrestrial species also require a mechanism of volume expansion and stretching of the integument prior to sclerotization, a need that is readily met in aquatic arthropods by drinking. Options for land arthropods include drinking of dew, swallowing of air, or using muscular contractions to inflate air sacs in tracheate taxa. In this study we tested the hypothesis that crinochete terrestrial isopods (Isopoda: Oniscidea: Crinocheta) exploit their capacity for active water vapor absorption (WVA) to increase volume during molting. Two crinochete species, Armadillidiumvulgare and Porcelliodilatatus, were studied and compared with the non-absorbing species Ligidiumlapetum (Oniscidea: Ligiamorpha). Pre-molting animals were identified by sternal CaCO3 deposits and exposed to 100% or 97% relative humidity (RH). Mass-changes were monitored by daily weighing and the timing of the posterior and anterior ecdyses was used to categorize time (days premolt and days post-molt) over the molt cycle. In each treatment RH, A.vulgare and P.dilatatus showed a progressive mass increase from 5 days premolt until the posterior or anterior ecdysis, followed abruptly by period of mass-loss lasting 3-4 days post-molt. The fact that the initial mass-gain is seen in 97 % RH, a humidity below the water activity of the hemolymph, confirms the role of WVA. Similarly, since the post-molt mass-loss is seen in 100 % RH, this must be due to active expulsion of water, possibly via maxillary urine. Concurrent changes in hemolymph osmolality were monitored in a separate batch of A.vulgare and show sustained osmolality during premolt and an abrupt decrease between the anterior and posterior ecdysis. These patterns indicate a mobilization of sequestered electrolytes during premolt, and a loss of electrolytes during the post-molt mass-loss, amounting to approximately 8.6 % of total hemolymph solutes. WVA, in conjunction with pulses of elevated hemolymph pressure, provides an efficient mechanism of pre-molt volume expansion prior to and during the biphasic molt in these species. Premolt Ligidiumlapetum exposed to same treatments failed to molt successfully and no premolt animals survived to day 3 (72 h) even in 100 % RH. The apparent dependence of this species on liquid water for successful molting could explain its obligatory association with riparian fringe habitats.

Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation.

Social behavior is often described as a unified concept, but highly social (group-living) species exhibit distinct social structures and may make different social decisions. Prairie voles (Microtus ochrogaster) are socially monogamous rodents that often reside in extended family groups, and exhibit robust preferences for familiar social partners (same- and opposite-sex) during extended choice tests, although short-term preferences are not known. Mice (Mus musculus) are gregarious and colonial, but in brief laboratory tests of social preference they typically prefer social novelty. This preference for novel vs. familiar peers may represent a species-specific difference in social decision-making between mice and prairie voles. However, the tests used to measure preferences in each species differ markedly in duration and degree of contact, such that the behaviors cannot be directly compared. We assessed whether social preferences for novelty or familiarity differed between mice and prairie voles of both sexes when assessed with matching protocols: the sociability/social preference test (SPT) typically used in mice (short, no direct contact), and the partner preference test (PPT) used in voles (long, direct contact). A subset of voles also underwent a PPT using barriers (long, no direct contact). In the short SPT, behavior did not differ between species. In the longer test, pronounced partner preferences emerged in prairie voles, but mice exhibited no social preferences and rarely huddled. No sex differences were evident in either test. Direct physical contact was required for partner preferences in huddling time in voles, but preference for the partner chamber was evident with or without contact. Both prairie voles and mice are social, but they exhibit important differences in the specificity and extent of their social behavior. While mice are often used to study social approach and other behaviors, voles are a more suitable species for the study of selective social relationships. Consideration of these differences will be important for studies examining the neural mechanisms supporting different kinds of peer social behavior.