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Selection for group living has occurred across taxa, despite inherent risk of disease transmission. Behavioral and immune responses to sickness affect social interactions and can be altered by social contexts. However, the majority of research on sickness behavior has focused on species that do not form selective social relationships. Prairie voles (Microtus ochrogaster) form selective social relationships with mates and peers and provide a useful study system to examine effects of sickness on social seeking in established relationships. We used peripheral injections of lipopolysaccharide (LPS) of E. coli to stimulate the innate immune system and verified effects on activity, core temperature, and corticosterone concentrations for 6 h following treatment. We demonstrated that male and female same-sex pairs of prairie voles increase social contact when sick and that this increase persists when contact is initiated by the sick vole. Finally, we assessed social motivation following immune challenge using operant choice chambers equipped with two levers and side chambers. Voles worked to gain access to chambers with social and non-social rewards. While overall effort decreased following LPS injection, only immune-challenged voles worked significantly harder for their companion than for a non-social chamber. LPS treatment also increased proportion of rewards earned for the partner versus a stranger and again led to increased huddling behavior. Prior studies in other rodent species have shown decreased social interaction when sick; the present results demonstrate an alternative outcome of sickness in the context of dyadic bonds and lay the foundation for future work in peer companions.

Oxytocin (OXT) is a peptide hormone and a neuropeptide that regulates various peripheral physiological processes and modulates behavioral responses in the central nervous system. While the humoral release occurs from the axons arriving at the median eminence, the neuropeptide is also released from oxytocinergic cell axons in various brain structures that contain its receptor, and from their dendrites in hypothalamic nuclei and potentially into the cerebrospinal fluid (CSF). Understanding oxytocins complex functions requires the knowledge on patterns of oxytocinergic projections in relationship to its receptor (OXTR). This study provides the first comprehensive examination of the oxytocinergic system in the prairie vole (Microtus ochrogaster), an animal exhibiting social behaviors that mirror human social behaviors linked to oxytocinergic functioning. Using light and electron microscopy, we characterized the neuroanatomy of the oxytocinergic system in this species. OXT+ cell bodies were found primarily in the hypothalamus, and axons were densest in subcortical regions. Examination of the OXT+ fibers and their relationship to oxytocin receptor transcripts (Oxtr) revealed that except for some subcortical structures, the presence of axons was not correlated with the amount of Oxtr across the brain. Of particular interest, the cerebral cortex that had high expression of Oxtr transcripts contained little to no fibers. Electron microscopy is used to quantify dense cored vesicles (DCV) in OXT+ axons and to identify potential axonal release sites. The ependymal cells that line the ventricles were frequently permissive of DCV-containing OXT+ dendrites reaching the third ventricle. Our results highlight a mechanism in which oxytocin is released directly into the ventricles and circulates throughout the ventricular system, may serve as the primary source for oxytocin that binds to OXTR in the cerebral cortex.

Use of a contraceptive (i.e., fertility control) is attractive for rodent management where lethal control is unwanted. Although population reduction is generally unachievable with small-scale, short-term contraceptive use, reduced juvenile recruitment is achievable. The injectable immunocontraceptive vaccine GonaCon (active ingredient: gonadotropin releasing hormone [GnRH]) was registered in 2022 by the U.S. EPA for controlling fertility of female prairie dogs (Cynomys, a type of ground squirrel) in urban/suburban settings. Here we: 1) describe past research, including a replicated field study in Colorado (GonaCon treatment vs. control sites) testing efficacy of GonaCon in prairie dogs, which gave rise to the EPA registration of this product, 2) outline future research needs for prairie dog population management with GonaCon–Prairie Dogs, 3) describe the steps required to possibly register GonaCon for additional rodent species, and 4) describe the other fertility control pesticide products that are currently registered for use against rodents in the U.S. During the replicated field study in Colorado, prairie dogs were live-trapped in a portion (avg: 18.5%, range: 7-37%) of each colony’s total area. In treatment plots, every female captured ≥ 660 g was injected with 0.4 ml of GonaCon. GonaCon was highly effective in controlling female fertility during the first year (2019), as juvenile density was reduced 3×, but not in the second year (2020) following treatment. Treating whole colonies of prairie dogs is favored, yet if small or partial colony treatment is desired then annual GonaCon treatment may be needed. An amendment to the EPA label is in progress to allow treatment of both male and female prairie dogs. Due to recent interest from land and pest managers, other fertility control products and the steps required to possibly get GonaCon registered for additional rodent species are also outlined.

Cesarean delivery is associated with diminished plasma levels of several birth-signaling hormones, such as oxytocin and vasopressin. These same hormones have been previously shown to exert organizational effects when acting in early life. For example, our previous work found a broadly gregarious phenotype in prairie voles exposed to oxytocin at birth. Meanwhile, cesarean delivery has been previously associated with changes in social behavior and metabolic processes related to oxytocin and vasopressin. In the present study, we investigated the long-term neurodevelopmental consequences of cesarean delivery in prairie voles. After cross-fostering, vole pups delivered either via cesarean or vaginal delivery were studied throughout development. Cesarean-delivered pups responded to isolation differently in terms of their vocalizations (albeit in opposite directions in the two experiments), huddled in less cohesive groups under warmed conditions, and shed less heat. As young adults, we observed no differences in anxiety-like or alloparental behavior. However, in adulthood, cesarean-delivered voles of both sexes failed to form partner preferences with opposite sex conspecifics. In a follow-up study, we replicated this deficit in partner-preference formation among cesarean-delivered voles and were able to normalize pair-bonding behavior by treating cesarean-delivered vole pups with oxytocin (0.25 mg/kg) at delivery. Finally, we detected minor differences in regional oxytocin receptor expression within the brains of cesarean-delivered voles, as well as microbial composition of the gut. Gene expression changes in the gut epithelium indicated that cesarean-delivered male voles have altered gut development. These results speak to the possibility of unintended developmental consequences of cesarean delivery, which currently accounts for 32.9 % of deliveries in the U.S. and suggest that further research should be directed at whether hormone replacement at delivery influences behavioral outcomes in later life.

Birth is a critical period for the developing brain, a time when surging hormone levels help prepare the fetal brain for the tremendous physiological changes it must accomplish upon entry into the extrauterine world. A number of obstetrical conditions warrant manipulations of these hormones at the time of birth, but we know little of their possible consequences on the developing brain. One of the most notable birth signaling hormones is oxytocin, which is administered to roughly 50% of laboring women in the United States prior to / during delivery. Previously, we found evidence for behavioral, epigenetic, and neuroendocrine consequences in adult prairie vole offspring following maternal oxytocin treatment immediately prior to birth. Here, we examined the neurodevelopmental consequences in adult prairie vole offspring following maternal oxytocin treatment prior to birth. Control prairie voles and those exposed to 0.25 mg/kg oxytocin were scanned as adults using anatomical and functional MRI, with neuroanatomy and brain function analyzed as voxel-based morphometry and resting state functional connectivity, respectively. Overall, anatomical differences brought on by oxytocin treatment, while widespread, were generally small, while differences in functional connectivity, particularly among oxytocin-exposed males, were larger. Analyses of functional connectivity based in graph theory revealed that oxytocin-exposed males in particular showed markedly increased connectivity throughout the brain and across several parameters, including closeness and degree. These results are interpreted in the context of the organizational effects of oxytocin exposure in early life and these findings add to a growing literature on how the perinatal brain is sensitive to hormonal manipulations at birth.

Prairie voles are among a small group of mammals that display long-term social attachment between mating partners. Many pharmacological studies show that signaling via the oxytocin receptor (Oxtr) is critical for the display of social monogamy in these animals. We used CRISPR mutagenesis to generate three different Oxtr-null mutant prairie vole lines. Oxtr mutants displayed social attachment such that males and females showed a behavioral preference for their mating partners over a stranger of the opposite sex, even when assayed using different experimental setups. Mothers lacking Oxtr delivered viable pups, and parents displayed care for their young and raised them to the weanling stage. Together, our studies unexpectedly reveal that social attachment, parturition, and parental behavior can occur in the absence of Oxtr signaling in prairie voles.

The neurohormone oxytocin regulates many aspects of physiology primarily by binding to its receptor, the oxytocin receptor. The oxytocin receptor gene (Oxtr) has been shown to have alternative transcripts in the mouse brain which may each have different biological functions or be used in specific contexts. A popular animal model for studying oxytocin-dependent social behaviors is the prairie vole, a biparental and monogamous rodent. Alternative transcriptional capacity of Oxtr in prairie voles is unknown. We used 5 rapid amplification of cDNA ends to identify alternative Oxtr transcription start sites in prairie vole brain tissue and uterine tissue. We then validated expression of specific transcripts in fetal brains and assessed the impact of exogenous oxytocin administration in utero on offspring brain development. We identified seven distinct Oxtr transcripts, all of which are present in both brain and uterine tissue. We then demonstrated that maternal oxytocin administration alters expression of a specific subset of Oxtr transcripts and that these different transcripts are under unique epigenetic regulation, such that in the perinatal period only one of the alternative transcripts is associated with DNA methylation in the Oxtr promoter. These data establish the existence of multiple Oxtr transcripts in prairie vole brain and uterine tissue and implicate oxytocin in the regulation of alternative transcript expression. These data have significant implications for our understanding of null mutant models in both mice and voles and translation in human birth and behavior.

The long-standing assumption that aboveground plant litter inputs have a substantial influence on soil organic carbon storage (SOC) and dynamics has been challenged by a new paradigm for SOC formation and persistence. We tested the importance of plant litter chemistry on SOC storage, distribution, composition, and age by comparing two highly contrasting ecosystems: an old-growth coast redwood (Sequoia sempervirens) forest, with highly aromatic litter, and an adjacent coastal prairie, with more easily decomposed litter. We hypothesized that if plant litter chemistry was the primary driver, redwood would store more and older SOC that was less microbially processed than prairie. Total soil carbon stocks to 110 cm depth were higher in prairie (35 kg C m-2) than redwood (28 kg C m-2). Radiocarbon values indicated shorter SOC residence times in redwood than prairie throughout the profile. Higher amounts of pyrogenic carbon and a higher degree of microbial processing of SOC appear to be instrumental for soil carbon storage and persistence in prairie, while differences in fine-root carbon inputs likely contribute to younger SOC in redwood. We conclude that at these sites fire residues, root inputs, and soil properties influence soil carbon dynamics to a greater degree than the properties of aboveground litter.

Abstract: Background and aims: Both drought and vegetation restoration can have dramatic effects on plant community composition, but how they influence soil microbial community diversity, structure, and co-occurrence networks remain less well known. Methods: To better understand the regulatory mechanisms of drought and vegetation restoration on soil microorganisms, we planted 12 native species in precipitation manipulation experimental plots in an invaded coastal grassland in California, USA. We measured soil bacterial and fungal community composition by amplicon sequencing, and quantified plant species richness and coverage in the third experimental year. Results: Our results showed that drought significantly altered soil bacterial diversity and composition; however, neither drought nor vegetation restoration had significant effects on fungal diversity and composition. The control plots had the most cooperative interactions (greatest number of correlations) among bacterial and/or fungal species, while drought plots yielded the most complex co-occurrence network with the highest modularity and clustering coefficient. Structural equation modeling revealed that plant species richness, net gains, and soil moisture played dominant roles in shaping bacterial community structure. Drought and bacterial community structure directly affected fungal community structure. Plant dominant species cover, common species cover, and bacterial diversity were the key drivers in regulating the microbial co-occurrence network complex. Conclusion: We conclude that soil bacterial and fungal communities differ in their responses to abiotic and biotic environmental changes, which may weaken the interspecies interactions among soil microorganisms.

Social isolation influences depression- and anxiety-related disorders and cardiac function. Oxytocin may mediate these conditions through interactions with social behavior, emotion, and cardiovascular function, via central and/or peripheral mechanisms. The present study investigated the influence of oxytocin antagonism using L-368,899, a selective oxytocin receptor antagonist that crosses the blood-brain barrier, on depression- and anxiety-related behaviors and heart rate in prairie voles. This rodent species has translational value for investigating interactions of social stress, behavior, cardiac responses, and oxytocin function. Adult female prairie voles were socially isolated or co-housed with a sibling for 4 weeks. A subset of animals in each housing condition was subjected to 4 sessions of acute L-368,899 (20 mg/kg, ip) or saline administration followed by a depression- or anxiety-related behavioral assessment. A subset of co-housed animals was evaluated for cardiac function following acute administration of L-368,899 (20 mg/kg, ip) and during behavioral assessments. Social isolation (vs. co-housing) increased depression- and anxiety-related behaviors. In isolated animals, L-368,899 (vs. vehicle) did not influence anxiety-related behaviors but exacerbated depression-related behaviors. In co-housed animals, L-368,899 exacerbated depression-related behaviors and increased heart rate at baseline and during behavioral tests. Social isolation produces emotion-related behaviors in prairie voles; central and/or peripheral oxytocin antagonism exacerbates these behavioral signs. Oxytocin antagonism induces depression-relevant behaviors and increases basal and stressor-reactive heart rate in co-housed prairie voles, similar to the consequences of social isolation demonstrated in this model. These results provide translational value for humans who experience behavioral and cardiac consequences of loneliness or social stress.

Prairie dogs are an accessible and enjoyed wildlife species in Colorado that require occasional surveys because populations can change abruptly due to plague outbreaks or human-induced control. We evaluated the use of small copter drones at four prairie dog colonies on Open Space and Mountain Parks lands, City of Boulder, to determine if this methodology improves efficiency over ground-based survey methods. We counted prairie dogs and burrows using two types of drones (DJI Matric 210 and Autel Evo II) at altitudes 100', 150', and 400' (burrows only). We recorded video and merged still images into orthomosaics prior to having USDA staff analyze this imagery. We then compared the drone imagery counts to those of our simultaneous ground-based counts of prairie dogs. We determined that 100' altitude mosaics produced using DJI Matric 210 drone were most accurate (closest to true, ground-based counts) for burrow abundance. We were not able to identify the best drone and altitude combination for drone-based prairie dog abundance. Overall video and mosaics both had similar accuracy in most prairie dog counts, however 150' video was more accurate than 100' video. One staff member counted burrows more closely to true than did the other. Both staff members required about the same amount of time to count and analyze imagery; videos could be evaluated slightly faster than mosaics (average of 3.8 hours vs. 5.5 hours per imagery) when counting prairie dogs, and burrow counts (of mosaics) generally took 2-3 times longer to analyze (averaging 8.1 hours per imagery; range: 3-13 hours) than did prairie dog counts. The labor requirement of using drones for burrow and prairie dog counts is far more time consuming (3-4 times longer per hectare) than having field staff conduct the traditional on-the-ground counts that include repeated prairie dog counts in a day. Until drone technology improves to allow targeting larger colonies (>2 km2) and automated detection and counting of wildlife become more commonplace, drone surveys are unlikely to be a more efficient technique than ground-based surveys for evaluating prairie dog abundances.

The rewarding properties of social interactions facilitate relationship formation and maintenance. Prairie voles are one of the few laboratory species that form selective relationships, manifested as "partner preferences" for familiar partners versus strangers. While both sexes exhibit strong partner preferences, this similarity in outward behavior likely results from sex-specific neurobiological mechanisms. We recently demonstrated that in operant trials, females worked hardest for access to familiar conspecifics of either sex, while males worked equally hard for access to any female, indicating a sex difference in social motivation. As tests were performed with one social target at a time, males might have experienced a ceiling effect, and familiar females might be more relatively rewarding in a choice scenario. Here we performed an operant social choice task in which voles lever-pressed to gain temporary access to either the chamber containing their mate or one containing a novel opposite-sex vole. Females worked hardest to access their mate, while males pressed at similar rates for either female. Individual male behavior was heterogeneous, congruent with multiple mating strategies in the wild. Voles exhibited preferences for favorable over unfavorable environments in a non-social operant task, indicating that lack of social preference does not reflect lack of discrimination. Natural variation in oxytocin receptor genotype at the intronic single nucleotide polymorphism NT213739 was associated with oxytocin receptor density, and predicted individual variation in stranger-directed aggressive behavior. These findings suggest that convergent preference behavior in male and female voles results from sex-divergent pathways, particularly in the realm of social motivation.

In pair bonding animals, coordinated behavior between partners is required for the pair to accomplish shared goals such as raising young. Despite this, experimental designs rarely assess the behavior of both partners within a bonded pair. Thus, we lack an understanding of the interdependent behavioral dynamics between partners that likely facilitate relationship success. To identify intra-pair behavioral correlates of pair bonding, we used socially monogamous prairie voles (Microtus ochrogaster) and tested both partners using social choice and non-choice tests at short- and long-term pairing timepoints. Females developed a preference for their partner more rapidly than males, with preference driven by different behaviors in each sex. Further, as bonds matured, intra-pair behavioral sex differences and organized behavior emerged-females consistently huddled more with their partner than males did regardless of overall intra-pair affiliation levels. When animals were allowed to freely interact with a partner or a novel vole in sequential free interaction tests, pairs spent more time interacting together than either animal did with a novel vole, consistent with partner preference in the more commonly employed choice test. Total pair interaction in freely moving voles was correlated with female, but not male, behavior. Via a social operant paradigm, we found that pair-bonded females, but not males, are more motivated to access and huddle with their partner than a novel vole. Together, our data indicate that as pair bonds mature, sex differences and organized behavior emerge within pairs, and that these intra-pair behavioral changes are likely organized and driven by the female animal.

In recent years, there has been increasing interest in the use of carbon monoxide-generating devices to control burrowing rodents. A pilot study was performed to determine how long a black-tailed prairie dog burrow needed to be fumigated with a BurrowRx® machine to obtain control. This pilot study obtained 92% efficacy with a four-minute injection, 86.7% with a 3:45-minute injection and 90% efficacy with a three-minute injection. Out of 59 burrows, 85% had only a single entrance. Of the nine that had two or more openings, six had only two, one had three openings, and two had five openings. Surface measurements from the treated opening to the furthest connected opening ranged from 10 feet to 43 feet with the average being 23.33 feet. The paper also discusses suggestions for further research and suggestions for practical use of the device.

In mammals, sleep duration is highest in the early postnatal period of life and is critical for shaping neural circuits that control the development of complex behaviors. The prairie vole is a wild, highly social rodent that serves as a unique model for the study of complex, species-typical social behaviors. Previous work in our laboratory has found that early life sleep disruption (ELSD) in prairie voles during a sensitive window of postnatal development leads to long lasting changes in social and cognitive behaviors as well as structural changes in excitatory and inhibitory neural circuits in the brain. However, it is currently unknown how later sleep is impacted by ELSD, both shortly after ELSD and over the long term. Therefore, the aim of this study was to describe the effects of ELSD on later life sleep, compared to sleep in normally developing prairie voles. First, we conducted tethered electroencephalogram/electromyogram (EEG/EMG) recordings in juvenile prairie voles undergoing ELSD, compared to Control conditions. Second, we conducted 24 h of home cage tethered EEG/EMG recordings in either adolescent or adult male and female prairie voles that had previously undergone ELSD or Control conditions as juveniles. We found that, as adults, male ELSD prairie voles showed persistently lower REM sleep duration and female ELSD prairie voles showed persistently higher NREM sleep duration compared to Controls, but no other sleep parameters differed. We concluded that 1) persistent effects of ELSD on sleep into adulthood may contribute to the social and cognitive deficits observed in adult voles, and 2) sleep disruption early in life can influence later sleep patterns in adulthood.

RationaleAnandamide is an endocannabinoid that contributes to certain aspects of social behavior, like play and reward, by binding to cannabinoid receptor type 1 (CB1). Most interesting is the recent discovery that anandamide may be mobilized by oxytocin receptor activation under certain contexts, particularly in the nucleus accumbens.ObjectivesGiven the established role of oxytocin and the nucleus accumbens in the neurobiology of pair-bonding, we investigated whether systemic administration of brain-permeable modulators of the endocannabinoid system could alter preferential partner contact in both male and female prairie voles.MethodsSpecifically, we tested whether intraperitoneal administration of the neutral CB1 antagonist AM4113 (4.0-16.0 mg/kg) or the anandamide hydrolysis inhibitor URB597 (5.0-20.0 mg/kg) could prevent or facilitate partner preference formation, respectively. To further investigate the specificity of effects on partner preference, we repeated our URB597 dosing regimen on an additional group of females and tested their anxiety-related behavior in both an elevated-plus maze and a light/dark test.ResultsAM4113 administration had no effect on partner preference. But while URB597 also had no effect on partner preference, low-dose females did increase absolute preferential contact with either the partner or the stranger; individual females spent significant contact time with either the partner or the stranger. None of our outcome measures in either anxiety test showed significant effects of treatment.ConclusionsOur results reveal that experimentally increasing anandamide levels in female prairie voles can increase social contact with both a familiar and novel male via unknown mechanisms that are likely separate from anxiety reduction.

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.

Prairie cordgrass (Spartina pectinata Link) is a native perennial warm-season (C4) grass common in North American prairies. With its high biomass yield and abiotic stress tolerance, there is a high potential of developing prairie cordgrass for conservation practices and as a dedicated bioenergy crop for sustainable cellulosic biofuel production. However, as with many other undomesticated grass species, little information is known about the genetic diversity or population structure of prairie cordgrass natural populations as compared to their ecotypic and geographic adaptation in North America. In this study, we sampled and characterized a total of 96 prairie cordgrass natural populations with 9315 high quality SNPs from a genotyping-by-sequencing (GBS) approach. The natural populations were collected from putative remnant prairie sites throughout the Midwest and Eastern USA, which are the major habitats for prairie cordgrass. Partitioning of genetic variance using SNP marker data revealed significant variance among and within populations. Two potential gene pools were identified as being associated with ploidy levels, geographical separation, and climatic separation. Geographical factors such as longitude and altitude, and environmental factors such as annual temperature, annual precipitation, temperature of the warmest month, precipitation of the wettest month, precipitation of Spring, and precipitation of the wettest month are important in affecting the intraspecific distribution of prairie cordgrass. The divergence of prairie cordgrass natural populations also provides opportunities to increase breeding value of prairie cordgrass as a bioenergy and conservation crop.

RationaleAnandamide is an endocannabinoid that contributes to certain aspects of social behavior, like play and reward, by binding to cannabinoid receptor type 1 (CB1). Most interesting is the recent discovery that anandamide may be mobilized by oxytocin receptor activation under certain contexts, particularly in the nucleus accumbens.ObjectivesGiven the established role of oxytocin and the nucleus accumbens in the neurobiology of pair-bonding, we investigated whether systemic administration of brain-permeable modulators of the endocannabinoid system could alter preferential partner contact in both male and female prairie voles.MethodsSpecifically, we tested whether intraperitoneal administration of the neutral CB1 antagonist AM4113 (4.0-16.0 mg/kg) or the anandamide hydrolysis inhibitor URB597 (5.0-20.0 mg/kg) could prevent or facilitate partner preference formation, respectively. To further investigate the specificity of effects on partner preference, we repeated our URB597 dosing regimen on an additional group of females and tested their anxiety-related behavior in both an elevated-plus maze and a light/dark test.ResultsAM4113 administration had no effect on partner preference. But while URB597 also had no effect on partner preference, low-dose females did increase absolute preferential contact with either the partner or the stranger; individual females spent significant contact time with either the partner or the stranger. None of our outcome measures in either anxiety test showed significant effects of treatment.ConclusionsOur results reveal that experimentally increasing anandamide levels in female prairie voles can increase social contact with both a familiar and novel male via unknown mechanisms that are likely separate from anxiety reduction.

The prairie vole has proven a valuable animal model for the neurobiological study of social monogamy and pair bonding. Previous research has focused almost exclusively on virgin prairie voles forming pair-bonds for the first time - a paradigm with limited relevance to human social behavior. In the present study, we used stud males to assess the impact of repeated pair-bond formation and dissolution on the behaviors and neurobiology relevant to subsequent pair-bond formation. Stud males were tested for behavioral and neurobiological effects of repeated pair-bonding after the 1st, 5th, and 10th pairing. Aged breeder males that experienced minimal pair-bond dissolution were included to control for the effects of aging. Results showed that male prairie voles readily form new pair-bonds after repeated pair-bond dissolution. In terms of social monogamy, old age was associated with males spending less time in close social contact with unfamiliar females. There were no effects of age nor number of lifetime pairings on depressive-like behavior or paternal behavior toward pups. Within the brain, the patterns of oxytocin (OTR) and vasopressin type 1a (V1aR) receptors were largely unaffected, with the following exceptions: 1) males with only a single pairing had higher OTR densities in the paraventricular thalamus and bed nucleus of the stria terminalis; 2) there was an age-related increase in the density of OTR in the caudate putamen and an age-related decline in the density of V1aR in the cortical amygdala. The present findings have translational relevance to human social behavior in the context of aging and social experience.

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.

Black-tailed prairie dogs’ feeding and burrowing behavior is a significant economic nuisance to agricultural producers. We tested the Rodenator™ on two portions of an isolated prairie dog town in Lewis and Clark County, Montana to determine how effective it was in reducing prairie dog numbers. Though other studies have been done using propane-oxygen devices, our study employed updated application techniques and an aggressive hole closing procedure to reduce the likelihood of false failures. In the southern area, we treated 53 burrows for 30 seconds with oxygen set at 40 psi and propane at 45 psi. In the northern area, we treated 120 burrows with an injection time of 45 seconds using the same oxygen and propane psi rates. Using the open burrow method for determining efficacy, our results were 58.7% for the southern area and 65% for the northern. Our study revealed that future studies should incorporate population surveys and appropriate control plots to determine the true efficacy of the Rodenator™, and we provide suggestions to improve overall method efficiency.

Oxytocin (OT) elicits weight loss in diet-induced obese (DIO) rodents, nonhuman primates and humans by reducing food intake and increasing energy expenditure. In addition to being important in the regulation of energy balance, OT is involved in social behaviors including parent-infant bonds, friendships, and pair bonds. However, the impact of social context on susceptibility to diet-induced obesity (DIO) and feeding behavior (including food sharing) has not been investigated in a rodent model that forms strong social bonds (i.e. prairie vole). Our goals were to determine in Prairie voles (Microtus ochrogaster) whether i) social context impacts susceptibility to DIO and ii) chronic intranasal OT reverses DIO. Voles were housed in divided cages with holes in the divider and paired with a same-sex animal with either the same food [high fat diet (HFD)/HFD, [low fat diet (LFD; chow)/chow], or the opposite food (HFD/chow or chow/HFD) for 19 weeks. HFD-fed voles pair-housed with voles maintained on the HFD demonstrated increased weight relative to pair-housed voles that were both maintained on chow. The study was repeated to determine the impact of social context on DIO susceptibility and body composition when animals are maintained on purified sugar-sweetened HFD and LFD to enhance palatability. As before, we found that voles demonstrated higher weight gain on the HFD/HFD housing paradigm, in part, through increased energy intake and the weight gain was a consequence of an increase in fat mass. However, HFD-fed animals housed with LFD-fed animals (and vice versa) showed intermediate patterns of weight gain and evidence of food sharing. Of translational importance is the finding that chronic intranasal OT appeared to reduce weight gain in DIO voles through a decrease in fat mass with no reduction in lean body mass. These effects were associated with transient reductions in food intake and increased food sharing. These findings identify a role of social context in the pathogenesis of DIO and indicate that chronic intranasal OT treatment reduces weight gain and body fat mass in DIO prairie voles, in part, by reducing food intake.

Oxytocin (OT) elicits weight loss in diet-induced obese (DIO) rodents, nonhuman primates and humans by reducing food intake and increasing energy expenditure. In addition to being important in the regulation of energy balance, OT is involved in social behaviors including parent-infant bonds, friendships, and pair bonds. However, the impact of social context on susceptibility to diet-induced obesity (DIO) and feeding behavior (including food sharing) has not been investigated in a rodent model that forms strong social bonds (i.e. prairie vole). Our goals were to determine in Prairie voles (Microtus ochrogaster) whether i) social context impacts susceptibility to DIO and ii) chronic intranasal OT reverses DIO. Voles were housed in divided cages with holes in the divider and paired with a same-sex animal with either the same food [high fat diet (HFD)/HFD, [low fat diet (LFD; chow)/chow], or the opposite food (HFD/chow or chow/HFD) for 19 weeks. HFD-fed voles pair-housed with voles maintained on the HFD demonstrated increased weight relative to pair-housed voles that were both maintained on chow. The study was repeated to determine the impact of social context on DIO susceptibility and body composition when animals are maintained on purified sugar-sweetened HFD and LFD to enhance palatability. As before, we found that voles demonstrated higher weight gain on the HFD/HFD housing paradigm, in part, through increased energy intake and the weight gain was a consequence of an increase in fat mass. However, HFD-fed animals housed with LFD-fed animals (and vice versa) showed intermediate patterns of weight gain and evidence of food sharing. Of translational importance is the finding that chronic intranasal OT appeared to reduce weight gain in DIO voles through a decrease in fat mass with no reduction in lean body mass. These effects were associated with transient reductions in food intake and increased food sharing. These findings identify a role of social context in the pathogenesis of DIO and indicate that chronic intranasal OT treatment reduces weight gain and body fat mass in DIO prairie voles, in part, by reducing food intake.

For altricial mammalian species, early life social bonds are constructed principally between offspring and their mothers, and the mother-offspring relationship sets the trajectory for offspring bio-behavioral development. In the rare subset of monogamous and biparental species, offspring experience an expanded social network which includes a father. Accordingly, in biparental species fathers also have the potential to influence trajectories of offspring development. Previous semi-natural and laboratory study of one monogamous and biparental species, the prairie vole (Microtus ochrogaster), has given insight into the role that mothers and fathers play in shaping behavioral phenotypes of offspring. Of particular interest is the influence of biparental care in the development of monogamous behavior in offspring. Here, we first briefly review that influence. We then present novel research which describes how parental investment in prairie voles changes across sequential litters of pups, and the extent to which it is coordinated between mothers and fathers. We use approximately 6 years of archival data on prairie vole parenting to investigate trajectories and inter-parent dynamics in prairie vole parenting. We use a series of latent growth models to assess the stability of parental investment across the first 4 l. Our findings suggest that prairie voles display sexually dimorphic patterns of change in parental behavior: mothers' investment declines linearly whereas fathers' pattern of change is characterized by initial decline between litters 1 and 2 with subsequent increase from litters 2 to 4. Our findings also support a conclusion that prairie vole paternal care may be better characterized as compensatory-that is, fathers may compensate for decline in maternal investment. Opposing trends in investment between mothers and fathers ultimately imply stability in offspring investment across sequential litters. These findings, combined with previous studies, generate a hypothesis that paternal compensation could play an important role in maintaining the development of monogamous behavioral phenotypes in individual offspring and across cohorts of those offspring. Understanding longitudinal and inter-individual dynamics of complex social behaviors is critical for the informed investigation of both proximate and ultimate mechanisms that may subserve these behaviors.

For altricial mammalian species, early life social bonds are constructed principally between offspring and their mothers, and the mother-offspring relationship sets the trajectory for offspring bio-behavioral development. In the rare subset of monogamous and biparental species, offspring experience an expanded social network which includes a father. Accordingly, in biparental species fathers also have the potential to influence trajectories of offspring development. Previous semi-natural and laboratory study of one monogamous and biparental species, the prairie vole (Microtus ochrogaster), has given insight into the role that mothers and fathers play in shaping behavioral phenotypes of offspring. Of particular interest is the influence of biparental care in the development of monogamous behavior in offspring. Here, we first briefly review that influence. We then present novel research which describes how parental investment in prairie voles changes across sequential litters of pups, and the extent to which it is coordinated between mothers and fathers. We use approximately 6 years of archival data on prairie vole parenting to investigate trajectories and inter-parent dynamics in prairie vole parenting. We use a series of latent growth models to assess the stability of parental investment across the first 4 l. Our findings suggest that prairie voles display sexually dimorphic patterns of change in parental behavior: mothers' investment declines linearly whereas fathers' pattern of change is characterized by initial decline between litters 1 and 2 with subsequent increase from litters 2 to 4. Our findings also support a conclusion that prairie vole paternal care may be better characterized as compensatory-that is, fathers may compensate for decline in maternal investment. Opposing trends in investment between mothers and fathers ultimately imply stability in offspring investment across sequential litters. These findings, combined with previous studies, generate a hypothesis that paternal compensation could play an important role in maintaining the development of monogamous behavioral phenotypes in individual offspring and across cohorts of those offspring. Understanding longitudinal and inter-individual dynamics of complex social behaviors is critical for the informed investigation of both proximate and ultimate mechanisms that may subserve these behaviors.

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.

The North American prairie covered about 3.6 million-km2 of the continent prior to European contact. Only 1-2% of the original prairie remains, but the soils that developed under these prairies are some of the most productive and fertile in the world, containing over 35% of the soil carbon in the continental United States. Cultivation may alter microbial diversity and composition, influencing the metabolism of carbon, nitrogen, and other elements. Here, we explored the structure and functional potential of the soil microbiome in paired cultivated-corn (at the time of sampling) and never-cultivated native prairie soils across a three-states transect (Wisconsin, Iowa, and Kansas) using metagenomic and 16S rRNA gene sequencing and lipid analysis. At the Wisconsin site, we also sampled adjacent restored prairie and switchgrass plots. We found that agricultural practices drove differences in community composition and diversity across the transect. Microbial biomass in prairie samples was twice that of cultivated soils, but alpha diversity was higher with cultivation. Metagenome analyses revealed denitrification and starch degradation genes were abundant across all soils, as were core genes involved in response to osmotic stress, resource transport, and environmental sensing. Together, these data indicate that cultivation shifted the microbiome in consistent ways across different regions of the prairie, but also suggest that many functions are resilient to changes caused by land management practices - perhaps reflecting adaptations to conditions common to tallgrass prairie soils in the region (e.g., soil type, parent material, development under grasses, temperature and rainfall patterns, and annual freeze-thaw cycles). These findings are important for understanding the long-term consequences of land management practices to prairie soil microbial communities and their genetic potential to carry out key functions.

The North American prairie covered about 3.6 million-km2 of the continent prior to European contact. Only 1-2% of the original prairie remains, but the soils that developed under these prairies are some of the most productive and fertile in the world, containing over 35% of the soil carbon in the continental United States. Cultivation may alter microbial diversity and composition, influencing the metabolism of carbon, nitrogen, and other elements. Here, we explored the structure and functional potential of the soil microbiome in paired cultivated-corn (at the time of sampling) and never-cultivated native prairie soils across a three-states transect (Wisconsin, Iowa, and Kansas) using metagenomic and 16S rRNA gene sequencing and lipid analysis. At the Wisconsin site, we also sampled adjacent restored prairie and switchgrass plots. We found that agricultural practices drove differences in community composition and diversity across the transect. Microbial biomass in prairie samples was twice that of cultivated soils, but alpha diversity was higher with cultivation. Metagenome analyses revealed denitrification and starch degradation genes were abundant across all soils, as were core genes involved in response to osmotic stress, resource transport, and environmental sensing. Together, these data indicate that cultivation shifted the microbiome in consistent ways across different regions of the prairie, but also suggest that many functions are resilient to changes caused by land management practices - perhaps reflecting adaptations to conditions common to tallgrass prairie soils in the region (e.g., soil type, parent material, development under grasses, temperature and rainfall patterns, and annual freeze-thaw cycles). These findings are important for understanding the long-term consequences of land management practices to prairie soil microbial communities and their genetic potential to carry out key functions.

Paternal absence can significantly alter bio-behavioural development in many biparental species. This effect has generally been demonstrated by comparing the development of offspring reared under biparental care with those reared by a single mother. However, studies employing this design conflate two significant modifications to early-life experience: removal of father-specific qualities and the general reduction of offspring-directed care. In the socially monogamous prairie vole (Microtus ochrogaster), the experience of paternal absence without substitution during development inhibits partner preference formation in adulthood, a hallmark of social monogamy, in females and males. Employing alloparents as substitutes for fathers, our previous work demonstrated that paternal absence affects pair-bond formation in female offspring via reduced quantity of care, although it affects pair-bond formation in male offspring by means of a missing paternal quality (or qualities). Here, we present evidence that paternal absence (with and without alloparental substitution) may alter the ontogeny of neural oxytocin receptor (OXTR) and/or vasopressin 1a receptor (AVPR1a) distribution in male and female prairie voles. Compared to biparentally reared controls (BPC), male offspring reared in mother only (MON) and maternal-plus-alloparental (MPA) conditions show lower densities of OXTR in the central amygdala; and MPA males show lower densities of OXTR in the caudate putamen and nucleus accumbens. Early-life experience was not associated with differences in AVPR1a density in males. However, MON and MPA females show greater densities of AVPR1a in the medial amygdala than BPC; and MPA females show greater densities of AVPR1a in the ventromedial nucleus of the hypothalamus. We also demonstrate with corticosterone concentrations that MON and MPA offspring are not differentially susceptible to a stressor (ie, social isolation) than BPC offspring. These findings suggest that paternal absence, although likely not a salient early-life stressor, has neuroendocrine consequences for offspring, some of which may affect partner preference formation.

During the last several decades, viruses have been increasingly recognized for their abundance, ubiquity, and important roles in different ecosystems. Despite known contributions to aquatic systems, few studies examine viral abundance and community structure over time in terrestrial ecosystems. The effects of land conversion and land management on soil microbes have been previously investigated, but their effects on virus population are not well studied. This study examined annual dynamics of viral abundance in soils from a native tallgrass prairie and two croplands, conventional till winter wheat and no-till canola, in Oklahoma. Virus-like particle (VLP) abundance varied across sites, and showed clear seasonal shifts. VLP abundance significantly correlated with environmental variables that were generally reflective of land use, including air temperature, soil nitrogen, and plant canopy coverage. Structural equation modeling supported the effects of land use on soil communities by emphasizing interactions between management, environmental factors, and viral and bacterial abundance. Between the viral metagenomes from the prairie and tilled wheat field, 1,231 unique viral operational taxonomic units (vOTUs) were identified, and only five were shared that were rare in the contrasting field. Only 13% of the vOTUs had similarity to previously identified viruses in the RefSeq database, with only 7% having known taxonomic classification. Together, our findings indicated land use and tillage practices influence virus abundance and community structure. Analyses of viromes over time and space are vital to viral ecology in providing insight on viral communities and key information on interactions between viruses, their microbial hosts, and the environment. IMPORTANCE Conversion of land alters the physiochemical and biological environments by not only changing the aboveground community, but also modifying the soil environment for viruses and microbes. Soil microbial communities are critical to nutrient cycling, carbon mineralization, and soil quality; and viruses are known for influencing microbial abundance, community structure, and evolution. Therefore, viruses are considered an important part of soil functions in terrestrial ecosystems. In aquatic environments, virus abundance generally exceeds bacterial counts by an order of magnitude, and they are thought to be one of the greatest genetic reservoirs on the planet. However, data are extremely limited on viruses in soils, and even less is known about their responses to the disturbances associated with land use and management. The study provides important insights into the temporal dynamics of viral abundance and the structure of viral communities in response to the common practice of turning native habitats into arable soils.

During the last several decades, viruses have been increasingly recognized for their abundance, ubiquity, and important roles in different ecosystems. Despite known contributions to aquatic systems, few studies examine viral abundance and community structure over time in terrestrial ecosystems. The effects of land conversion and land management on soil microbes have been previously investigated, but their effects on virus population are not well studied. This study examined annual dynamics of viral abundance in soils from a native tallgrass prairie and two croplands, conventional till winter wheat and no-till canola, in Oklahoma. Virus-like particle (VLP) abundance varied across sites, and showed clear seasonal shifts. VLP abundance significantly correlated with environmental variables that were generally reflective of land use, including air temperature, soil nitrogen, and plant canopy coverage. Structural equation modeling supported the effects of land use on soil communities by emphasizing interactions between management, environmental factors, and viral and bacterial abundance. Between the viral metagenomes from the prairie and tilled wheat field, 1,231 unique viral operational taxonomic units (vOTUs) were identified, and only five were shared that were rare in the contrasting field. Only 13% of the vOTUs had similarity to previously identified viruses in the RefSeq database, with only 7% having known taxonomic classification. Together, our findings indicated land use and tillage practices influence virus abundance and community structure. Analyses of viromes over time and space are vital to viral ecology in providing insight on viral communities and key information on interactions between viruses, their microbial hosts, and the environment. IMPORTANCE Conversion of land alters the physiochemical and biological environments by not only changing the aboveground community, but also modifying the soil environment for viruses and microbes. Soil microbial communities are critical to nutrient cycling, carbon mineralization, and soil quality; and viruses are known for influencing microbial abundance, community structure, and evolution. Therefore, viruses are considered an important part of soil functions in terrestrial ecosystems. In aquatic environments, virus abundance generally exceeds bacterial counts by an order of magnitude, and they are thought to be one of the greatest genetic reservoirs on the planet. However, data are extremely limited on viruses in soils, and even less is known about their responses to the disturbances associated with land use and management. The study provides important insights into the temporal dynamics of viral abundance and the structure of viral communities in response to the common practice of turning native habitats into arable soils.

Tallgrass Prairie National Preserve (TAPR) is a rural protected natural area in Kansas, United States. This parcel of public land provides visitors from varying areas with opportunities to experience a remaining collective of the tallgrass prairie ecosystem that once spanned large areas of North America. TAPR also provides visitors with opportunities to engage in nature-based experiences while also executing active pursuits. The researchers examined the effects of visiting TAPR on individuals’ stress and activity levels during fall 2016. Electronic surveys and accelerometers were used to quantify individual stress levels and exercise. Participants (n = 239) traveled an average of 138 km to visit TAPR and spent an average of 143.7 minutes at the park, with an average of 68.1 minutes in moderate to vigorous exercise. A large majority of visitors (88.3%) also reported feeling less stressed than usual while at the park. The results suggest visiting natural areas have the potential to reduce stress and promote exercise, both well-known factors contributing to individual well-being. The results of this case study also convey the significance that accessible natural areas can have regarding opportunities of people to spend time in public lands and their reception of the benefits (e.g., mental, emotional, and physical) gained from the natural experience(s).

Tallgrass Prairie National Preserve (TAPR) is a rural protected natural area in Kansas, United States. This parcel of public land provides visitors from varying areas with opportunities to experience a remaining collective of the tallgrass prairie ecosystem that once spanned large areas of North America. TAPR also provides visitors with opportunities to engage in nature-based experiences while also executing active pursuits. The researchers examined the effects of visiting TAPR on individuals’ stress and activity levels during fall 2016. Electronic surveys and accelerometers were used to quantify individual stress levels and exercise. Participants (n = 239) traveled an average of 138 km to visit TAPR and spent an average of 143.7 minutes at the park, with an average of 68.1 minutes in moderate to vigorous exercise. A large majority of visitors (88.3%) also reported feeling less stressed than usual while at the park. The results suggest visiting natural areas have the potential to reduce stress and promote exercise, both well-known factors contributing to individual well-being. The results of this case study also convey the significance that accessible natural areas can have regarding opportunities of people to spend time in public lands and their reception of the benefits (e.g., mental, emotional, and physical) gained from the natural experience(s).

Rationale: Anandamide is an endocannabinoid that contributes to certain aspects of social behavior, like play and reward, by binding to cannabinoid receptor type 1 (CB1). Most interesting is the recent discovery that anandamide may be mobilized by oxytocin receptor activation under certain contexts, particularly in the nucleus accumbens. Objectives: Given the established role of oxytocin and the nucleus accumbens in the neurobiology of pair-bonding, we investigated whether systemic administration of brain-permeable modulators of the endocannabinoid system could alter preferential partner contact in both male and female prairie voles. Methods: Specifically, we tested whether intraperitoneal administration of the neutral CB1 antagonist AM4113 (4.0–16.0 mg/kg) or the anandamide hydrolysis inhibitor URB597 (5.0–20.0 mg/kg) could prevent or facilitate partner preference formation, respectively. To further investigate the specificity of effects on partner preference, we repeated our URB597 dosing regimen on an additional group of females and tested their anxiety-related behavior in both an elevated-plus maze and a light/dark test. Results: AM4113 administration had no effect on partner preference. But while URB597 also had no effect on partner preference, low-dose females did increase absolute preferential contact with either the partner or the stranger; individual females spent significant contact time with either the partner or the stranger. None of our outcome measures in either anxiety test showed significant effects of treatment. Conclusions: Our results reveal that experimentally increasing anandamide levels in female prairie voles can increase social contact with both a familiar and novel male via unknown mechanisms that are likely separate from anxiety reduction.

Early experience and social context interact to alter the phenotype of complex social behaviors. These early experiences can also result in alterations to cortical organization and connections. Given the ability of the neuropeptide oxytocin (OT) to modulate social and reproductive behavior, OT is likely involved in these cortical processes. However, little is known about the distribution of OT and OT receptors (OTR) within the neocortex. Using autoradiographic and neuroanatomical techniques, we characterized the cortical distribution of OT receptors (OTR) in prairie voles, a socially monogamous rodent species. We found that OTR density was low in the primary sensory areas (including primary somatosensory and auditory regions) but was quite high in association regions (including temporal and parietal association areas, and prelimbic regions). In the primary motor area as well as the temporal and parietal association areas, we observed differences in OTR density across cortical layers. Specifically, cortical layers 2/3 and 5 exhibited greater OTR density than layer 4. Our results point to a role for OT in integrating sensory and motor in the prairie vole brain, providing a complementary mechanism for the modulation of social interactions. Given the ability of early social experience and developmental manipulations of OT to affect the brain and behavior, these results suggest a novel mechanism for how OT may influence cortical organization.

Early experience and social context interact to alter the phenotype of complex social behaviors. These early experiences can also result in alterations to cortical organization and connections. Given the ability of the neuropeptide oxytocin (OT) to modulate social and reproductive behavior, OT is likely involved in these cortical processes. However, little is known about the distribution of OT and OT receptors (OTR) within the neocortex. Using autoradiographic and neuroanatomical techniques, we characterized the cortical distribution of OT receptors (OTR) in prairie voles, a socially monogamous rodent species. We found that OTR density was low in the primary sensory areas (including primary somatosensory and auditory regions) but was quite high in association regions (including temporal and parietal association areas, and prelimbic regions). In the primary motor area as well as the temporal and parietal association areas, we observed differences in OTR density across cortical layers. Specifically, cortical layers 2/3 and 5 exhibited greater OTR density than layer 4. Our results point to a role for OT in integrating sensory and motor in the prairie vole brain, providing a complementary mechanism for the modulation of social interactions. Given the ability of early social experience and developmental manipulations of OT to affect the brain and behavior, these results suggest a novel mechanism for how OT may influence cortical organization.

Early experience and social context interact to alter the phenotype of complex social behaviors. These early experiences can also result in alterations to cortical organization and connections. Given the ability of the neuropeptide oxytocin (OT) to modulate social and reproductive behavior, OT is likely involved in these cortical processes. However, little is known about the distribution of OT and OT receptors (OTR) within the neocortex. Using autoradiographic and neuroanatomical techniques, we characterized the cortical distribution of OT receptors (OTR) in prairie voles, a socially monogamous rodent species. We found that OTR density was low in the primary sensory areas (including primary somatosensory and auditory regions) but was quite high in association regions (including temporal and parietal association areas, and prelimbic regions). In the primary motor area as well as the temporal and parietal association areas, we observed differences in OTR density across cortical layers. Specifically, cortical layers 2/3 and 5 exhibited greater OTR density than layer 4. Our results point to a role for OT in integrating sensory and motor in the prairie vole brain, providing a complementary mechanism for the modulation of social interactions. Given the ability of early social experience and developmental manipulations of OT to affect the brain and behavior, these results suggest a novel mechanism for how OT may influence cortical organization.

The earliest and most prevalent sensory experience includes tactile, thermal, and olfactory stimulation delivered to the young via contact with the mother, and in some mammals, the father. Prairie voles (Microtus ochrogaster), like humans, are biparental and serve as a model for understanding the impact of parent/offspring interactions on the developing brain. Prairie voles also exhibit natural variation in the level of tactile stimulation delivered by the parents to the offspring, and this has been well documented and quantified. Previous studies revealed that adult prairie vole offspring who received either high (HC) or low (LC) tactile contact from their parents have differences in the size of cortical fields and the connections of somatosensory cortex. In the current investigation, we examined gene expression, intraneocortical connectivity, and cortical thickness in newborn voles to appreciate when differences in HC and LC offspring begin to emerge. We observed differences in developmentally regulated genes, as well as variation in prelimbic and anterior cingulate cortical thickness at postnatal Day 1 (P1) in HC and LC voles. Results from this study suggest that parenting styles, such as those involving high or low physical contact, impact the developing neocortex via very early sensory experience as well as differences in epigenetic modifications that may emerge in HC and LC voles.

Abstract: Background: Prairie–forest ecotones are ecologically important for biodiversity and ecological processes. While these ecotones cover small areas, their sharp gradients in land cover promote rich ecological interaction and high conservation value. Our objective was to understand how historical and current fire occurrences and human development influenced the Palouse Prairie–forest ecotone. We used General Land Office survey field notes about the occurrence of bearing trees to locate historical (1870s to 1880s) prairie, pine savanna, and forest at the eastern edge of the bioregion. We combined LANDFIRE Existing Vegetation classes to contrast historical land cover with current land cover. We reconstructed historical fire occurrence (1650 to 1900) from fire-scarred trees. We used fire and lightning records from 1992 to 2015 to interpret the role of people and lightning. Results: Historically, the ecotone was a matrix of prairie with extensive savanna and some forest. More than half of the ecotone area was prairie, which is now dominated by agriculture, with some residential development. The 16% of the landscape that was pine savanna is now forest or shrubs, agriculture, perennial vegetation under the Conservation Reserve Program, or developed; no savanna now exists. Forests covered 12% of the ecotone and these are still mostly forest. Fires were historically frequent, occurring on average every 5 to 8 years at most sites. Lightning was not frequent but could likely have been sufficient to ignite fires that could spread readily given the rolling terrain and long fire season. Conclusions: Fire was far more frequent historically than currently. Conservation, restoration, and other ongoing land-use changes will likely result in more continuous vegetation and hence fuel for fires. Lightning and people may ignite fires that therefore spread readily in the future. Understanding the past and potential future of fire in the Palouse Prairie bioregion may help us live with fire while conserving ecological values here and in similar prairie–forest ecotones.

In prairie voles (Microtus ochrogaster), biparental care of offspring is typical, and paternal absence in the pre-weaning development of offspring alters biobehavioral development. We sought to determine whether this altered development is due to the absence of specific paternal qualities or a general reduction in pup-directed care. We compared the biobehavioral development of pups reared under conditions of biparental (BPC), maternal-plus-alloparental (MPA; i.e., mother and older sister), and maternal only (MON) care. Older sisters provided a quantity of care equal to or greater than that of fathers. Growth rate and developmental milestones were unaffected by family composition, with the exception of earlier fur growth in MON conditions. In adulthood, we tested behaviors on an elevated plus maze, spontaneous alloparental care, and partner preference formation. We found no significant differences on the elevated plus maze and only marginal differences in alloparental care. While both female and male MON individuals showed deficits in partner preference formation, MPA females showed typical partner preference formation. However, the alloparental substitution of fathers was not sufficient for the typical development of partner preference formation in males. We conclude that paternal care plays a differentially important role in the social development of female and male prairie vole offspring.

In prairie voles (Microtus ochrogaster), biparental care of offspring is typical, and paternal absence in the pre-weaning development of offspring alters biobehavioral development. We sought to determine whether this altered development is due to the absence of specific paternal qualities or a general reduction in pup-directed care. We compared the biobehavioral development of pups reared under conditions of biparental (BPC), maternal-plus-alloparental (MPA; i.e., mother and older sister), and maternal only (MON) care. Older sisters provided a quantity of care equal to or greater than that of fathers. Growth rate and developmental milestones were unaffected by family composition, with the exception of earlier fur growth in MON conditions. In adulthood, we tested behaviors on an elevated plus maze, spontaneous alloparental care, and partner preference formation. We found no significant differences on the elevated plus maze and only marginal differences in alloparental care. While both female and male MON individuals showed deficits in partner preference formation, MPA females showed typical partner preference formation. However, the alloparental substitution of fathers was not sufficient for the typical development of partner preference formation in males. We conclude that paternal care plays a differentially important role in the social development of female and male prairie vole offspring.

Amyloid formation by amylin contributes to β-cell dysfunction in type 2 diabetes. The features that control the amyloidogenicity and toxicity of amylin are not understood. Not all species form islet amyloid, and its presence or absence correlates with the in vitro behavior of the polypeptide. Rats do not develop type 2 diabetes or islet amyloid, and rat amylin is non-amyloidogenic, except at very high concentrations. This has led to the notion that rodent amylins are non-amyloidogenic. Prairie vole amylin has an unusual sequence compared to those of human and rat amylin, including nonconservative Lys-1 to Glu and Asn-22 to Gly substitutions. The first reduces the net charge on the peptide, while the second disrupts a potential network of side chain hydrogen bonds in the amyloid fiber, a so-called Asn ladder. The prairie vole polypeptide forms amyloid more slowly than human amylin and is considerably less cytotoxic. An Asn-22 to Gly substitution in human amylin significantly reduces toxicity, increasing the effective concentration of amylin required to reach 50% toxicity by >7-fold, but has modest effects on the time to form amyloid. A Lys-1 to Glu replacement has a weaker effect but does reduce toxicity relative to that of human amylin, without having a significant impact on the time to form amyloid. The effect of the Lys-1 to Glu substitution on amyloid kinetics is more significant in Tris buffer than in phosphate-buffered saline. This work demonstrates that the N-terminus of amylin plays a role in modulating toxicity and highlights the key role of position 22.

AbstractBackgroundPrairie–forest ecotones are ecologically important for biodiversity and ecological processes. While these ecotones cover small areas, their sharp gradients in land cover promote rich ecological interaction and high conservation value. Our objective was to understand how historical and current fire occurrences and human development influenced the Palouse Prairie–forest ecotone. We used General Land Office survey field notes about the occurrence of bearing trees to locate historical (1870s to 1880s) prairie, pine savanna, and forest at the eastern edge of the bioregion. We combined LANDFIRE Existing Vegetation classes to contrast historical land cover with current land cover. We reconstructed historical fire occurrence (1650 to 1900) from fire-scarred trees. We used fire and lightning records from 1992 to 2015 to interpret the role of people and lightning.ResultsHistorically, the ecotone was a matrix of prairie with extensive savanna and some forest. More than half of the ecotone area was prairie, which is now dominated by agriculture, with some residential development. The 16% of the landscape that was pine savanna is now forest or shrubs, agriculture, perennial vegetation under the Conservation Reserve Program, or developed; no savanna now exists. Forests covered 12% of the ecotone and these are still mostly forest. Fires were historically frequent, occurring on average every 5 to 8 years at most sites. Lightning was not frequent but could likely have been sufficient to ignite fires that could spread readily given the rolling terrain and long fire season.ConclusionsFire was far more frequent historically than currently. Conservation, restoration, and other ongoing land-use changes will likely result in more continuous vegetation and hence fuel for fires. Lightning and people may ignite fires that therefore spread readily in the future. Understanding the past and potential future of fire in the Palouse Prairie bioregion may help us live with fire while conserving ecological values here and in similar prairie–forest ecotones.

Developmental exposure to selective serotonin reuptake inhibitor (SSRI) increases the risk of Autism Spectrum Disorder (ASD), however, the underlying neurobiology of this effect is not fully understood. Here we used the socially monogamous prairie vole as a translational model of developmental SSRI exposure. Paired female prairie voles (n = 20) were treated with 5 mg/kg subcutaneous fluoxetine (FLX) or saline (SAL) daily from birth of the second litter until the day of birth of the 4th litter. This design created three cohorts of FLX exposure: postnatal exposure in litter 2, both prenatal and postnatal exposure in litter 3, and prenatal exposure in litter 4. Post-weaning, subjects underwent behavioral testing to detect changes in sociality, repetitive behavior, pair-bond formation, and anxiety-like behavior. Quantitative receptor autoradiography was performed for oxytocin, vasopressin 1a, and serotonin 1a receptor density in a subset of brains. We observed increased anxiety-like behavior and reduced sociality in developmentally FLX exposed adults. FLX exposure decreased oxytocin receptor binding in the nucleus accumbens core and central amygdala, and vasopressin 1a receptor binding in the medial amygdala. FLX exposure did not affect serotonin 1A receptor binding in any areas examined. Changes to oxytocin and vasopressin receptors may underlie the behavioral changes observed and have translational implications for the mechanism of the increased risk of ASD subsequent to prenatal SSRI exposure.

Developmental exposure to selective serotonin reuptake inhibitor (SSRI) increases the risk of Autism Spectrum Disorder (ASD), however, the underlying neurobiology of this effect is not fully understood. Here we used the socially monogamous prairie vole as a translational model of developmental SSRI exposure. Paired female prairie voles (n = 20) were treated with 5 mg/kg subcutaneous fluoxetine (FLX) or saline (SAL) daily from birth of the second litter until the day of birth of the 4th litter. This design created three cohorts of FLX exposure: postnatal exposure in litter 2, both prenatal and postnatal exposure in litter 3, and prenatal exposure in litter 4. Post-weaning, subjects underwent behavioral testing to detect changes in sociality, repetitive behavior, pair-bond formation, and anxiety-like behavior. Quantitative receptor autoradiography was performed for oxytocin, vasopressin 1a, and serotonin 1a receptor density in a subset of brains. We observed increased anxiety-like behavior and reduced sociality in developmentally FLX exposed adults. FLX exposure decreased oxytocin receptor binding in the nucleus accumbens core and central amygdala, and vasopressin 1a receptor binding in the medial amygdala. FLX exposure did not affect serotonin 1A receptor binding in any areas examined. Changes to oxytocin and vasopressin receptors may underlie the behavioral changes observed and have translational implications for the mechanism of the increased risk of ASD subsequent to prenatal SSRI exposure.

The neocortex of the prairie vole is composed of three well-defined sensory areas and one motor area: primary somatosensory, visual, auditory areas and the primary motor area respectively. The boundaries of these cortical areas are identifiable very early in development, and have been thought to resist alteration by all but the most extreme physical or genetic manipulations. Here we assessed the extent to which the boundaries of sensory/motor cortical areas can be altered by exposing young prairie voles (Microtus ochrogaster) to a chronic stimulus, high or low levels of parental contact, or an acute stimulus, a single dose of saline, oxytocin (OT), or oxytocin antagonist on the day of birth. When animals reached adulthood, their brains were removed, the cortex was flattened, cut parallel to the pial surface, and stained for myelin to identify the architectonic boundaries of sensory and motor areas. We measured the overall proportion of cortex that was myelinated, as well as the proportion of cortex devoted to the sensory and motor areas. Both the chronic and acute manipulations were linked to significant alterations in areal boundaries of cortical fields, but the areas affected differed with different conditions. Thus, differences in parental care and early exposure to OT can both change cortical organization, but their effects are not identical. Furthermore, the effects of both manipulations were sexually dimorphic, with a greater number of statistically significant differences in females than in males. These results indicate that early environmental experience, both through exposure to exogenous neuropeptides and parental contact, can alter the size of cortical fields.