Epigenetic aging studies of pair bonding in prairie voles.

The quality of romantic relationships can predict health consequences related to aging. DNA methylation-based biomarkers of aging accurately estimate chronological age. We developed several highly accurate epigenetic aging clocks, based on highly conserved mammalian CpGs, for the socially monogamous prairie vole (Microtus ochrogaster). In addition, our dual-species human-vole clock accurately measured relative age and illustrates high species conservation of epigenetic aging effects. Next, we assessed how pair bonding impacts epigenetic aging. We did not find evidence that pair-bonded voles exhibit accelerated or decelerated epigenetic aging effects in blood, ear, liver, or brain tissue. Our epigenome wide association study identified CpGs in five genes strongly associated with pair bonding: Foxp4, Phf2, Mms22l, Foxb1, and Eif1ad. Overall, we present accurate DNA methylation-based estimators of age for a species of great interest to researchers studying monogamy in animals. We did not find any evidence that sex-naive animals age differently from pair-bonded animals.

Paternal absence and increased caregiving independently and interactively shape the development of male prairie voles at subadult and adult life stages.

The influence of maternal caregiving is a powerful force on offspring development. The absence of a father during early life in biparental species also has profound implications for offspring development, although it is far less studied than maternal influences. Moreover, we have limited understanding of the interactive forces that maternal and paternal caregiving impart on offspring. We investigated if behaviorally upregulating maternal care compensates for paternal absence on prairie vole (Microtus ochrogaster) pup development. We used an established handling manipulation to increase levels of caregiving in father-absent and biparental families, and later measured male offspring behavioral outcomes at sub-adulthood and adulthood. Male offspring raised without fathers were more prosocial (or possibly less socially anxious) than those raised biparentally. Defensive behavior and responses to contextual novelty were also influenced by the absence of fathers, but only in adulthood. Offensive aggression and movement in the open field test changed as a function of life-stage but not parental exposure. Notably, adult pair bonding was not impacted by our manipulations. Boosting parental care produced males that moved more in the open field test. Parental handling also increased oxytocin immunoreactive cells within the supraoptic nucleus of the hypothalamus (SON), and in the paraventricular nucleus (PVN) of biparentally-reared males. We found no differences in vasopressinergic cell groups. We conclude that male prairie voles are contextually sensitive to the absence of fathers and caregiving intensity. Our study highlights the importance of considering the ways early experiences synergistically shape offspring behavioral and neural phenotypes across the lifespan.

Re-wiring of the bonded brain: Gene expression among pair bonded female prairie voles changes as they transition to motherhood.

Motherhood is a costly life-history transition accompanied by behavioral and neural plasticity necessary for offspring care. Motherhood in the monogamous prairie vole is associated with decreased pair bond strength, suggesting a trade-off between parental investment and pair bond maintenance. Neural mechanisms governing pair bonds and maternal bonds overlap, creating possible competition between the two. We measured mRNA expression of genes encoding receptors for oxytocin (oxtr), dopamine (d1r and d2r), mu-opioids (oprm1a), and kappa-opioids (oprk1a) within three brain areas processing salience of sociosensory cues (anterior cingulate cortex; ACC), pair bonding (nucleus accumbens; NAc), and maternal care (medial preoptic area; MPOA). We compared gene expression differences between pair bonded prairie voles that were never pregnant, pregnant (~day 16 of pregnancy), and recent mothers (day 3 of lactation). We found greater gene expression in the NAc (oxtr, d2r, oprm1a, and oprk1a) and MPOA (oxtr, d1r, d2r, oprm1a, and oprk1a) following the transition to motherhood. Expression for all five genes in the ACC was greatest for females that had been bonded for longer. Gene expression within each region was highly correlated, indicating that oxytocin, dopamine, and opioids comprise a complimentary gene network for social signaling. ACC-NAc gene expression correlations indicated that being a mother (oxtr and d1r) or maintaining long-term pair bonds (oprm1a) relies on the coordination of different signaling systems within the same circuit. Our study suggests the maternal brain undergoes changes that prepare females to face the trade-off associated with increased emotional investment in offspring, while also maintaining a pair bond.

Characterization of oxytocin and vasopressin receptors in the Southern giant pouched rat and comparison to other rodents.

Vasopressin and oxytocin are well known and evolutionarily ancient modulators of social behavior. The distribution and relative densities of vasopressin and oxytocin receptors are known to modulate the sensitivity to these signaling molecules. Comparative work is needed to determine which neural networks have been conserved and modified over evolutionary time, and which social behaviors are commonly modulated by nonapeptide signaling. To this end, we used receptor autoradiography to determine the distribution of vasopressin 1a and oxytocin receptors in the Southern giant pouched rat (Cricetomys ansorgei) brain, and to assess the relative densities of these receptors in specific brain regions. We then compared the relative receptor pattern to 23 other species of rodents using a multivariate ANOVA. Pouched rat receptor patterns were strikingly similar to hamsters and voles overall, despite the variation in social organization among species. Uniquely, the pouched rat had dense vasopressin 1a receptor binding in the caudate-putamen (i.e., striatum), an area that might impact affiliative behavior in this species. In contrast, the pouched rat had relatively little oxytocin receptor binding in much of the anterior forebrain. Notably, however, oxytocin receptor binding demonstrated extremely dense binding in the bed nucleus of the stria terminalis, which is associated with the modulation of several social behaviors and a central hub of the social decision-making network. Examination of the nonapeptide system has the potential to reveal insights into species-specific behaviors and general themes in the modulation of social behavior.

Dorsal CA1 lesions of the hippocampus impact mating tactics in prairie voles by shifting non-monogamous males' use of space to resemble monogamous males.

Alternative mating tactics within mating systems are characterized by discrete patterns of spatio-temporal overlap with same-and opposite-sex conspecifics and mating-relevant outcomes. Socially monogamous "residents" maintain relatively small home range sizes, have territories that almost exclusively overlap with their mating partners, and are more likely to produce offspring than non-bonded "wandering" conspecifics. Because mating tactics appear to be so closely tied to patterns of space use, differences in spatial cognitive abilities might differentially impact individual males' decisions to adopt a particular mating tactic and/or how efficient they are within their chosen mating tactic. Yet few studies have considered how the hippocampus, a brain region important for encoding cognitive maps and for processing contextual information, might impact how individuals adopt mating tactics or the spatio-temporal behaviors closely associated with them. We assessed the impact of lesions to the dorsal CA1 (dCA1) region of the hippocampus on male prairie vole space use, reproductive success, and mating tactics in semi-natural outdoor field conditions. Interestingly, dCA1 lesions did not impact the proportion of males that adopted resident or wandering mating tactics, and dCA1 lesions did not impact a male's ability to form a pair bond in the lab. In contrast, we found that lesioning the dCA1 shifted the home range size of reproductively successful and unsuccessful males. Furthermore, we found that patterns of space use among residents were unaffected by dCA1 lesions, whereas wanderers with dCA1 lesions showed pronounced reductions of their space use habits and resembled non-lesioned residents. Collectively, our study supports the hypothesis that wanderer male prairie voles rely on dCA1-mediated spatial cognition to navigate their world in a way that resident males do not. Such differences might have implications for how individuals efficiently attract and defend mates, obtain resources, defend territories, and outcompete rivals.

Bonding against the odds: Male prairie vole response to the "widow effect" among females.

Although pair bonding is the preferred mating tactic among socially monogamous prairie voles, naturalistic observations have demonstrated many males remain non-bonded. Moreover, although males readily re-bond after the loss of a partner, females do not (i.e., the "widow effect'). Few studies have attempted to address why so many males remain non-bonded or if a reluctance of re-bonding in females contributes to this outcome. We investigate how female bonding history impacts male pair bond formation. Specifically, we test two alternative hypotheses for how sexually naïve males will behave when paired with widow females. The fecundity hypothesis predicts males will avoid bonding with widow females and be more receptive to novel bond-naïve females. The preference to bond hypothesis predicts males will choose to bond and express a partner preference, irrespective of if a pair-mate is a widow or sexually naïve. Our results demonstrated that males expressed a partner preference for females regardless of their social history. These data support the preference to bond hypothesis and suggest natural variation in bonding may not be strongly due to males forgoing bonding opportunities.

Plasticity in parental behavior and vasopressin: responses to co-parenting, pup age, and an acute stressor are experience-dependent.

Introduction: The impact of variation in parental caregiving has lasting implications for the development of offspring. However, the ways in which parents impact each other in the context of caregiving is comparatively less understood, but can account for much of the variation observed in the postnatal environment. Prairie voles (Microtus ochrogaster) demonstrate a range of postnatal social groups, including pups raised by biparental pairs and by their mothers alone. In addition to the challenges of providing parental care, prairie vole parents often experience acute natural stressors (e.g., predation, foraging demands, and thermoregulation) that could alter the way co-parents interact. Methods: We investigated how variation in the experience of raising offspring impacts parental behavior and neurobiology by administering an acute handling stressor on prairie vole families of single mothers and biparental parents over the course of offspring postnatal development. Results: Mothers and fathers exhibited robust behavioral plasticity in response to the age of their pups, but in sex-dependent ways. Pup-directed care from mothers did not vary as a function of their partner's presence, but did covary with the number of hypothalamic vasopressin neurons in experience-dependent ways. The relationship between vasopressin neuron numbers and fathers' behaviors was also contingent upon the stress handling manipulation, suggesting that brain-behavior associations exhibit stress-induced plasticity. Conclusion: These results demonstrate that the behavioral and neuroendocrine profiles of adults are sensitive to distinct and interacting experiences as a parent, and extend our knowledge of the neural mechanisms that may facilitate parental behavioral plasticity.

Motherhood and DREADD manipulation of the nucleus accumbens weaken established pair bonds in female prairie voles.

Monogamous pair bonding has evolved to enhance reproductive success and ensure offspring survival. Although the behavioral and neural mechanisms regulating the formation of pair bonds have been relatively well outlined, how these relationships are regulated and maintained across the lifetime of an individual remains relatively unexplored. One way to explore this is to study the maintenance of a social bond across a major life-history transition. The transition to motherhood is among the most poignant moments in the life history of a female, and is associated with significant neural and behavioral changes and shifting priorities. The nucleus accumbens (NAc) is known to modulate social valence and is central to mammalian pair bonding. In this study, we investigated two mechanisms driving variation in bond strength in the socially monogamous prairie vole (Microtus ochrogaster). We manipulated neural activity of the NAc at two distinct stages of life-history, before and after the birth of offspring, to assess how neural activity and social contexts modulate female pair bond strength. Our results showed DREADD (Designer Receptor Exclusively Activated by Designer Drugs) inhibition of the NAc decreases affiliative behavior towards the mating partner, whereas DREADD activation of the NAc increases affiliative behavior of strangers, thereby decreasing social selectivity. We also found a robust "birth effect" on pair bond strength, such that bonds with partners were weakened after the birth of offspring, an effect not attributable to the amount of cohabitation time with a partner. Overall, our data support the hypotheses that NAc activity modulates reward/saliency within the social brain in different ways, and that motherhood comes with a cost for the bond strength between mating partners.

A test of the social behavior network reveals differential patterns of neural responses to social novelty in bonded, but not non-bonded, male prairie voles.

The social behavior network (SBN) has provided a framework for understanding the neural control of social behavior. The original SBN hypothesis proposed this network modulates social behavior and should exhibit distinct patterns of neural activity across nodes, which correspond to distinct social contexts. Despite its tremendous impact on the field of social neuroscience, no study has directly tested this hypothesis. Thus, we assessed Fos responses across the SBN of male prairie voles (Microtus ochrogaster). Virgin/non-bonded and pair bonded subjects were exposed to a sibling cagemate or pair bonded partner, novel female, novel male, novel meadow vole, novel object, or no stimulus. Inconsistent with the original SBN hypothesis, we did not find profoundly different patterns of neural responses across the SBN for different contexts, but instead found that the SBN generated significantly different patterns of activity in response to social novelty in pair bonded, but not non-bonded males. These findings suggest that non-bonded male prairie voles may perceive social novelty differently from pair bonded males or that SBN functionality undergoes substantial changes after pair bonding. This study reveals novel information about bond-dependent, context-specific neural responsivity in male prairie voles and suggests that the SBN may be particularly important for processing social salience. Further, our study suggests there is a need to reconceptualize the framework of how the SBN modulates social behavior.

Extreme plasticity of reproductive state in a female rodent.

Successful sexual reproduction relies on the coordination of multiple biological systems, yet traditional concepts of biological sex often ignore the natural plasticity in morphology and physiology underlying sex. Most female mammals develop a patent (i.e., opened) vaginal entrance (introitus) prenatally or postnatally before or during puberty, usually under the influence of estrogens, and remain patent for the remainder of their lifespan1. An exception is the southern African giant pouched rat (Cricetomys ansorgei), whose vaginal introitus remains sealed well into adulthood2. Here, we explore this phenomenon and report that the reproductive organs and the vaginal introitus can undergo astounding and reversible transformation. Non-patency is characterized by reduced uterine size and the presence of a sealed vaginal introitus. Furthermore, the female urine metabolome shows that patent and non-patent females profoundly differ in their urine content, a reflection of differences in physiology and metabolism. Surprisingly, patency state did not predict fecal estradiol or progesterone metabolite concentrations. Exploring the plasticity that exists in reproductive anatomy and physiology can uncover that traits long considered 'fixed' in adulthood can become plastic under specific evolutionary pressures. Moreover, the barriers to reproduction that such plasticity creates present unique challenges to maximizing reproductive potential.

Effects of social context manipulation on dorsal and ventral hippocampal neuronal responses.

The hippocampus is critical for contextual memory and has recently been implicated in various kinds of social memory. Traditionally, studies of hippocampal context coding have manipulated elements of the background environment, such as the shape and color of the apparatus. These manipulations produce large shifts in the spatial firing patterns, a phenomenon known as remapping. These findings suggest that the hippocampus encodes and differentiates contexts by generating unique spatial firing patterns for each environment a subject encounters. However, we do not know whether the hippocampus encodes social contexts defined by the presence of particular conspecifics. We examined this by exposing rats to a series of manipulations of the social context, including the presence of familiar male, unfamiliar male and female conspecifics, in order to determine whether remapping is a plausible mechanism for encoding socially-defined contexts. Because the dorsal and ventral regions of the hippocampus are thought to play different roles in spatial and social cognition, we recorded neurons in both regions. Surprisingly, we found little evidence of remapping in response to manipulation of the social context in either the dorsal or ventral hippocampus, although we saw typical remapping in response to changing the background color. This result suggests that remapping is not the primary mechanism for encoding different social contexts. However, we found that a subset of hippocampal neurons fired selectively near the cages that contained the conspecifics, and these responses were most prevalent in the ventral hippocampus. We also found a striking increase in the spatial information content of ventral hippocampal firing patterns. These results indicate that the ventral hippocampus is sensitive to changes in the social context and neurons that respond selectively near the conspecific cages could play an important, if not fully understood role in encoding the conjunction of conspecifics, their location and the environment.

Lateral septum DREADD activation alters male prairie vole prosocial and antisocial behaviors, not partner preferences.

Although much has been written on the topic of social behavior, many terms referring to different aspects of social behavior have become inappropriately conflated and the specific mechanisms governing them remains unclear. It is therefore critical that we disentangle the prosocial and antisocial elements associated with different forms of social behavior to fully understand the social brain. The lateral septum (LS) mediates social behaviors, emotional processes, and stress responses necessary for individuals to navigate day-to-day social interactions. The LS is particularly important in general and selective prosocial behavior (monogamy) but its role in how these two behavioral domains intersect is unclear. Here, we investigate the effects of chemogenetic-mediated LS activation on social responses in male prairie voles when they are 1) sex-naïve and generally affiliative and 2) after they become pair-bonded and display selective aggression. Amplifying neural activity in the LS augments same-sex social approach behaviors. Despite partner preference formation remaining unaltered, LS activation in pair-bonded males leads to reduced selective aggression while increasing social affiliative behaviors. These results suggest that LS activation alters behavior within certain social contexts, by increasing sex-naïve affiliative behaviors and reducing pair bonding-induced selective aggression with same-sex conspecifics, but not altering bonding with opposite-sex individuals.

Chromosome-scale genome assembly of the African giant pouched rat (Cricetomys ansorgei) and evolutionary analysis reveals evidence of olfactory specialization.

The Southern giant pouched rat, Cricetomys ansorgei, is a large rodent best known for its ability to detect landmines using its impressive sense of smell. Their powerful chemosensory abilities enable subtle discrimination of chemical social signals, and female pouched rats demonstrate a unique reproductive physiology hypothesized to be mediated by pheromonal mechanisms. Thus, C. ansorgei represents a novel mammalian model for chemosensory physiology, social behavior, and pheromonal control of reproductive physiology. We present the first chromosome-scale genomic sequence of the pouched rat encoding 22,671 protein coding genes, including 1571 olfactory receptors, and provide a glance into the evolutionary history of this species. Functional enrichment analysis reveals genetic expansions specific to the pouched rat are enriched for functions related to olfactory specialization. Overall, this assembly is of reference-quality, and will serve as a useful and informative genomic sequence on which we can confidently base future molecular research involving the pouched rat.

Effects of social and environmental contexts on multi-male mating and mixed paternity in socially monogamous female prairie voles.

With whom and how often to mate are fundamental questions that impact individual reproductive success and the mating system. Relatively few studies have investigated female mating tactics compared with males. Here, we asked how differential access to mates influences the occurrence of mixed paternity and overall reproductive success in socially monogamous female prairie voles (Microtus ochrogaster). We created male- and female-biased sex ratios of prairie voles living in semi-natural outdoor enclosures. We ran paternity analyses to determine the identity and number of mating partners females had and the number of offspring produced. We found that 57.1% of females had litters fathered by two or more males when males outnumbered females, and 87.5% of females had litters with more than one father when females outnumbered males. However, the percentage of mixed paternity and the total number of embryos were not statistically different between social contexts. We determined that female fecundity (i.e. number of embryos) correlated with the number of male fathers in each litter across social contexts. Although our study did not support the hypothesis that social context directly influences female mating decisions, it did suggest that female multi-male mating might lead to increased fertilization success under semi-natural conditions.

Synergistic consequences of early-life social isolation and chronic stress impact coping and neural mechanisms underlying male prairie vole susceptibility and resilience.

Chronic stress can be challenging, lead to maladaptive coping strategies, and cause negative mental and physical health outcomes. Early-life adversity exposes developing young to physical or psychological experiences that risks surpassing their capacity to effectively cope, thereby impacting their lifetime physical and mental wellbeing. Sensitivity to stressful events, like social isolation, has the potential to magnify stress-coping. Chronic stress through social defeat is an established paradigm that models adverse early-life experiences and can trigger enduring alterations in behavioral and neural phenotypes. To assess the degree to which stress resilience and sensitivity stemming from early-life chronic stress impact sociability, we exposed male prairie voles to chronic social defeat stress (CSDS) during adolescence. We simultaneously exposed subjects to either social isolation (CSDS+Isol) or group housing (CSDS+Soc) during this crucial time of development. On PND41, all subjects underwent a social approach test to examine the immediate impact of isolation, CSDS, or their combined effects on sociability. Unlike the CSDS+Isol group which primarily displayed social avoidance, the CSDS+Soc group was split by individuals exhibiting susceptible or resilient stress phenotypes. Notably, the Control+Soc and CSDS+Soc animals and their cage-mates significantly gained body weight between PND31 and PND40, whereas the Control+Isol and CSDS+Isol animals did not. These results suggest that the effects of early-life stress may be mitigated by having access to social support. Vasopressin, oxytocin, and opioids and their receptors (avpr1a, oxtr, oprk1, oprm1, and oprd1) are known to modulate social and stress-coping behaviors in the lateral septum (LS). Therefore, we did an mRNA expression analysis with RT-qPCR of the avpr1a, oxtr, oprk1, oprm1, and oprd1 genes to show that isolation and CSDS, or their collective influence, can potentially differentially bias sensitivity of the LS to early-life stressors. Collectively, our study supports the impact and dimensionality of early-life adversity because the type (isolation vs. CSDS), duration (acute vs. chronic), and combination (isolation + CSDS) of stressors can dynamically alter behavioral and neural outcomes.

Effects of a GnRH agonist on sex behavior in females of the southern giant pouched rat.

In general, males should be particularly attentive to cues of sexual availability and females should advertise accordingly. Vaginal patency (i.e., the openness of the vagina) is a reliable indicator of sexual maturity; if the vagina is closed, the female is unable to copulate. The southern giant pouched rat (Cricetomys ansorgei) is unusual because females can have fully fused vaginal openings (i.e., vaginal nonpatency) despite being considered 'adults' by other metrics. Moreover, some females reversibly close their vaginal openings. Thus, vaginal patency in the pouched rat is a 'flexible' reproductive state. We subcutaneously implanted a long-acting GnRH agonist (deslorelin), which over time inhibits sex steroid secretion, to better understand the endocrinology and social behavior relating to vaginal patency in this species. We hypothesized that altering GnRH would impact both patency and behavior through its effects on circulating levels of estradiol. Six months of deslorelin treatment did not alter vaginal patency. Behaviorally, deslorelin-treated females spent less time interacting with, and were more aggressive towards males (compared to controls). Notably, deslorelin did not alter female scent marking. We conclude that behavioral receptivity, but not vaginal patency, is impacted by GnRH hormonal cascades in the pouched rat.

Developmental exposure to intranasal vasopressin impacts adult prairie vole spatial memory.

Spatial memory is critical for many tasks necessary for survival (i.e., locating mates and food resources). The two mammalian nonapeptides arginine vasopressin (AVP) and oxytocin (OT) are mechanistically important in modulating memory ability, albeit in contrasting ways. In general, AVP facilitates memory consolidation and retrieval while OT is an amnesic. Although AVP and OT are known to have these memory effects, past work has focused on their impact in social memory with little research on their effects on spatial memory. In this experiment, we tested the impact of AVP and OT on spatial memory as determined by performance in the Morris water maze (MWM). We administered doses of AVP, OT, or saline (a control) intranasally to male prairie voles (Microtus ochrogaster), a species whose spatial memory is hypothesized to impact their mating tactics. We also investigated if acute doses (given immediately prior to the memory trial in the MWM) and chronic doses (given daily during adolescence) had differing impacts on spatial cognition. We found that chronic intranasal administration of AVP during post-wean development improved spatial memory performance. In contrast, both chronic and acute administration of OT and acute administration of AVP had no impact on spatial memory. These results together suggest that 1) chronic exposure to AVP has organizational effects on spatial memory in the prairie vole, and 2) acute administration of nonapeptides does not impact the retrieval of spatial memories.

Multi-Level Effects Driving Cognitive and Behavioral Variability among Prairie Voles: Insights into Reproductive Decision-Making from Biological Levels of Organization.

Behavioral phenotypes play an active role in maximizing fitness and shaping the evolutionary trajectory of species by offsetting the ecological and social environmental factors individuals experience. How these phenotypes evolve and how they are expressed is still a major question in ethology today. In recent years, an increased focus on the mechanisms that regulate the interactions between an individual and its environment has offered novel insights into the expression of alternative phenotypes. In this review, we explore the proximate mechanisms driving the expression of alternative reproductive phenotypes in the male prairie vole (Microtus ochrogaster) as one example of how the interaction of an individual's social context and internal milieu has the potential to alter behavior, cognition, and reproductive decision-making. Ultimately, integrating the physiological and psychological mechanisms of behavior advances understanding into how variation in behavior arises. We take a "levels of biological organization" approach, with prime focus placed on the level of the organism to discuss how cognitive processes emerge as traits, and how they can be studied as important mechanisms driving the expression of behavior.

Reciprocal processes of sensory perception and social bonding: an integrated social-sensory framework of social behavior.

Organisms filter the complexity of natural stimuli through their individual sensory and perceptual systems. Such perceptual filtering is particularly important for social stimuli. A shared "social umwelt" allows individuals to respond appropriately to the expected diversity of cues and signals during social interactions. In this way, the behavioral and neurobiological mechanisms of sociality and social bonding cannot be disentangled from perceptual mechanisms and sensory processing. While a degree of embeddedness between social and sensory processes is clear, our dominant theoretical frameworks favor treating the social and sensory processes as distinct. An integrated social-sensory framework has the potential to greatly expand our understanding of the mechanisms underlying individual variation in social bonding and sociality more broadly. Here we leverage what is known about sensory processing and pair bonding in two common study systems with significant species differences in their umwelt (rodent chemosensation and avian acoustic communication). We primarily highlight that (1) communication is essential for pair bond formation and maintenance, (2) the neural circuits underlying perception, communication and social bonding are integrated, and (3) candidate neuromodulatory mechanisms that regulate pair bonding also impact communication and perception. Finally, we propose approaches and frameworks that more fully integrate sensory processing, communication, and social bonding across levels of analysis: behavioral, neurobiological, and genomic. This perspective raises two key questions: (1) how is social bonding shaped by differences in sensory processing?, and (2) to what extent is sensory processing and the saliency of signals shaped by social interactions and emerging relationships?

Support for the parental practice hypothesis: Subadult prairie voles exhibit similar behavioral and neural profiles when alloparenting kin and non-kin.

Parental care is critical for offspring survival in altricial species. Although parents are the most common caregivers, other individuals (e.g., older siblings) can also provide alloparental care. Some have argued that animals engage in alloparental behavior to practice providing care for their eventual offspring, whereas others have argued that alloparental behavior enhances indirect fitness. Proximate measures have the potential to test ultimate functions of behavior. A focus on neural expression of oxytocin and vasopressin (two neuropeptides modulating alloparental care) or neural activation following exposure to related and unrelated individuals could reveal whether practice or investment in indirect fitness explains alloparental behavior. This study examined alloparental behaviors and neural responses in prairie voles (Microtus ochrogaster), a species that engages in alloparental behavior. Subadult (independent, yet sexually immature) male prairie voles were exposed to one of four stimuli: same-age sibling, neonatal sibling, unrelated neonate, or inanimate neonate-sized object. We assessed alloparental behaviors and quantified cFos protein expression in oxytocin and vasopressin neuronal populations of the paraventricular nucleus of the hypothalamus and the supraoptic nucleus of the hypothalamus in response to stimulus exposure. We detected no differences in cFos and nonapeptide co-localization among stimulus groups. Subjects performed similar amounts of alloparental care toward related and unrelated neonates, but not other subadults or inanimate objects. Notably, caregiving did not differ based on kin-status. The lack of difference in alloparenting toward related and non-related neonates suggests that alloparental care in prairie voles primarily serves to provide subadults with parental practice.