RESUMEN
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.
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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.
Asunto(s)
Hipocampo , Neuronas , Ratas , Masculino , Femenino , Animales , Hipocampo/fisiología , Neuronas/fisiología , Medio SocialRESUMEN
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.
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Núcleo Accumbens , Apareamiento , Animales , Femenino , Pradera , Conducta Social , Arvicolinae/fisiología , Proteínas de Unión al ADN/farmacologíaRESUMEN
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.
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Pradera , Conducta Social , Masculino , Femenino , Humanos , Animales , Arvicolinae/fisiología , ApareamientoRESUMEN
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.
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Cromosomas , Mamíferos , Femenino , Ratas , AnimalesRESUMEN
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.
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Pradera , Conducta Social , Animales , Arvicolinae/metabolismo , Cognición , Masculino , Conducta Sexual Animal/fisiologíaRESUMEN
The neuropeptides oxytocin and vasopressin and their receptors have established roles in the regulation of mammalian social behavior including parental care, sex, affiliation and pair-bonding, but less is known regarding their relationship to social dominance and subordination within social hierarchies. We have previously demonstrated that male mice can form stable linear dominance hierarchies with individuals occupying one of three classes of social status: alpha, subdominant, subordinate. Alpha males exhibit high levels of aggression and rarely receive aggression. Subdominant males exhibit aggression towards subordinate males but also receive aggression from more dominant individuals. Subordinate males rarely exhibit aggression and receive aggression from more dominant males. Here, we examined whether variation in social status was associated with levels of oxytocin (OTR) and vasopressin 1a (V1aR) receptor binding in socially relevant brain regions. We found that socially dominant males had significantly higher OTR binding in the nucleus accumbens core than subordinate animals. Alpha males also had higher OTR binding in the anterior olfactory nucleus, posterior part of the cortical amygdala and rostral lateral septum compared to more subordinate individuals. Conversely, alpha males had lower V1aR binding in the rostral lateral septum and lateral preoptic area compared to subordinates. These observed relationships have two potential explanations. Preexisting individual differences in the patterns of OTR and V1aR binding may underlie behavioral differences that promote or inhibit the acquisition of social status. More likely, the differential social environments experienced by dominant and subordinate animals may shift receptor expression, potentially facilitating the expression of adaptive social behaviors.
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Encéfalo/metabolismo , Jerarquia Social , Oxitocina/metabolismo , Receptores de Vasopresinas/metabolismo , Agresión/fisiología , Animales , Masculino , Ratones , Ratones Endogámicos ICR , Núcleo Accumbens/metabolismo , Apareamiento , Receptores de Oxitocina/metabolismo , Conducta Social , Predominio Social , Medio Social , Vasopresinas/metabolismoRESUMEN
Although prairie vole (Microtus ochrogaster) social behavior is well-characterized in adults, surprisingly little is known about the development of social behavior in voles. Further, the overwhelming majority of studies in prairie voles examine social behavior in a reproductive context. Here, we examine developmental plasticity in affiliation and aggression and their underlying neural correlates. Using sexually naïve males, we characterized interactions with an age-matched, novel, same-sex conspecific in four different age groups that span pre-weaning to adulthood. We found that prosocial behavior decreased and aggression increased as males matured. Additionally, pre-weaning males were more prosocial than nonsocial, whereas post-weaning males were more nonsocial than prosocial. We also examined nonapeptide neural activity in response to a novel conspecific in brain regions important for promoting sociality and aggression using the immediate early gene cFos. Assessment of developmental changes in neural activity showed that vasopressin neurons in the medial bed nucleus of the stria terminalis exhibit functional plasticity, providing a potential functional mechanism that contributes to this change in sociality as prairie voles mature. This behavioral shift corresponds to the transition from a period of allopatric cohabitation with siblings to a period of time when voles disperse and presumably attempt to establish and defend territories. Taken together our data provide a putative mechanism by which brain and behavior prepare for the opportunity to pairbond (characterized by selective affiliation with a partner and aggression toward unfamiliar conspecifics) by undergoing changes away from general affiliation and toward selective aggression, accounting for this important life history event.
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Adaptación Fisiológica/fisiología , Agresión/fisiología , Arvicolinae/fisiología , Neuronas/fisiología , Maduración Sexual/fisiología , Conducta Social , Vasopresinas/metabolismo , Agresión/psicología , Animales , Encéfalo/metabolismo , Química Encefálica , Femenino , Masculino , Neuronas/metabolismo , Caracteres Sexuales , Conducta Sexual Animal/fisiologíaRESUMEN
PURPOSE: To report ophthalmic examination findings and intraocular pressures (IOPs) in wild-caught African giant pouched rats (Cricetomys ansorgei and gambianus) from Tanzania and Ghana. PROCEDURES: After being placed under general anesthesia for examination, slit-lamp biomicroscopy before and after pharmacologic mydriasis and indirect ophthalmoscopy was performed. Eyes were fluorescein stained and IOPs measured by rebound tonometry using the TonoVet® . RESULTS: Thirty-two sexually mature pouched rats (64 eyes) were examined, including 16 males and 16 females. The mean IOP (± standard deviation) was 7.7 (±2.9) mmHg. Fluorescein staining was negative in all eyes. One or more ocular abnormalities were detected in 21 pouched rats (35 eyes). These ocular lesions included the following: lens opacities (n = 23 eyes), persistent pupillary membranes (n = 5), chorioretinal scarring (n = 3), corneal vascularization (n = 2), palpebral margin defect with focal trichiasis (n = 2), phthisis bulbi (n = 1), and posterior synechiae (n = 1). Lens opacities included incipient anterior cortical opacities (n = 7), immature cataract (n = 6), incipient nuclear opacities (n = 5), punctate pigment on anterior lens capsule (n = 2 eyes), incipient suture tip opacities (n = 2), and hypermature cataract (n = 1). CONCLUSIONS: Ocular abnormalities were common in the evaluated population of giant pouched rats; however, most of the detected lesions were mild and believed to have minimal impact on vision. Rebound tonometry with the TonoVet® was a reliable and simple technique to measure IOPs in the anesthetized pouched rats.
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Catarata/veterinaria , Presión Intraocular/fisiología , Ratas/fisiología , Animales , Animales Salvajes , Catarata/fisiopatología , Femenino , Ghana , Masculino , Tanzanía , Tonometría Ocular/veterinariaRESUMEN
Sex differences are well documented and are conventionally associated with intense sex-specific selection. For example, spatial memory is frequently better in males, presumably due to males' tendency to navigate large spaces to find mates. Alternatively, monogamy (in which sex-specific selection is relatively relaxed) should diminish or eliminate differences in spatial ability and the mechanisms associated with this behavior. Nevertheless, phenotypic differences between monogamous males and females persist, sometimes cryptically. We hypothesize that sex-specific cognitive demands are present in monogamous species that will influence neural and behavioral phenotypes. The effects of these demands should be observable in spatial learning performance and neural structures associated with spatial learning and memory. We analyzed spatial memory performance, hippocampal volume and cell density, and hippocampal oxytocin receptor (OTR) expression in the socially monogamous prairie vole. Compared to females, males performed better in a spatial memory and spatial learning test. Although we found no sex difference in hippocampal volume or cell density, male OTR density was significantly lower than females, suggesting that performance may be regulated by sub-cellular mechanisms within the hippocampus that are less obvious than classic neuroanatomical features. Our results suggest an expanded role for oxytocin beyond facilitating social interactions, which may function in part to integrate social and spatial information.
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Arvicolinae , Hipocampo/metabolismo , Receptores de Oxitocina/metabolismo , Caracteres Sexuales , Memoria Espacial/fisiología , Animales , Arvicolinae/metabolismo , Arvicolinae/psicología , Cognición/fisiología , Femenino , Masculino , Oxitocina/metabolismoRESUMEN
Social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. We asked if social experience before and after weaning influenced adult social cognition in male prairie voles. Animals were raised either with or without fathers and then either housed singly or in sibling pairs. Males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social recognition or dissociate spatial from social information. We also examined oxytocin and vasopressin receptors (OTR and V1aR) in areas of the forebrain associated with social behaviour and memory. Pre- and post-wean experience differentially altered receptor expression in several structures. Of note, OTR in the lateral septum-an area in which oxytocin inhibits social recognition-was greatest in animals that did not clearly demonstrate social recognition. The combination of absentee fathers on V1aR in the retrosplenial cortex and single housing on OTR in the septohippocampal nucleus produced a unique phenotype previously found to be associated with poor reproductive success in nature. We demonstrate that interactive effects of early life experiences throughout development have tremendous influence over brain-behaviour phenotype and can buffer potentially negative outcomes due to social deprivation.
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Arvicolinae/fisiología , Receptores de Oxitocina/genética , Receptores de Vasopresinas/genética , Discriminación Social , Medio Social , Destete , Animales , Arvicolinae/psicología , Encéfalo/metabolismo , Cognición , Padre , Expresión Génica , Masculino , Receptores de Oxitocina/metabolismo , Receptores de Vasopresinas/metabolismo , Memoria EspacialRESUMEN
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.
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Arvicolinae , Conducta Materna , Núcleo Accumbens , Apareamiento , Receptores Opioides mu , Animales , Femenino , Arvicolinae/genética , Receptores Opioides mu/genética , Receptores Opioides mu/metabolismo , Conducta Materna/fisiología , Núcleo Accumbens/metabolismo , Embarazo , Receptores de Oxitocina/genética , Receptores de Oxitocina/metabolismo , Receptores Opioides kappa/genética , Receptores Opioides kappa/metabolismo , Giro del Cíngulo/metabolismo , Área Preóptica/metabolismo , Receptores de Dopamina D1/genética , Receptores de Dopamina D1/metabolismoRESUMEN
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.
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Encéfalo , Receptores de Oxitocina , Receptores de Vasopresinas , Animales , Receptores de Oxitocina/metabolismo , Receptores de Vasopresinas/metabolismo , Masculino , Encéfalo/metabolismo , Roedores/metabolismo , Ratas , Especificidad de la Especie , Autorradiografía , Arvicolinae/metabolismo , Oxitocina/metabolismo , Cricetinae , Conducta Social , FemeninoRESUMEN
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.
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Envejecimiento , Arvicolinae , Metilación de ADN , Epigénesis Genética , Animales , Arvicolinae/genética , Envejecimiento/genética , Femenino , Masculino , Apareamiento , Islas de CpGRESUMEN
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.
RESUMEN
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.
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Pradera , Viudez , Animales , Masculino , Femenino , Conducta Sexual Animal/fisiología , Apareamiento , Arvicolinae/fisiología , Conducta SocialRESUMEN
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.
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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.
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Estrógenos , Reproducción , Animales , Femenino , Muridae , Estradiol , Evolución BiológicaRESUMEN
Despite its well-described role in female affiliation, the influence of oxytocin on male pairbonding is largely unknown. However, recent human studies indicate that this nonapeptide has a potent influence on male behaviors commonly associated with monogamy. Here we investigated the distribution of oxytocin receptors (OTR) throughout the forebrain of the socially monogamous male prairie vole (Microtus ochrogaster). Because males vary in both sexual and spatial fidelity, we explored the extent to which OTR predicted monogamous or non-monogamous patterns of space use, mating success and sexual fidelity in free-living males. We found that monogamous males expressed higher OTR density in the nucleus accumbens than non-monogamous males, a result that mirrors species differences in voles with different mating systems. OTR density in the posterior portion of the insula predicted mating success. Finally, OTR in the hippocampus and septohippocampal nucleus, which are nuclei associated with spatial memory, predicted patterns of space use and reproductive success within mating tactics. Our data highlight the importance of oxytocin receptor in neural structures associated with pairbonding and socio-spatial memory in male mating tactics. The role of memory in mating systems is often neglected, despite the fact that mating tactics impose an inherently spatial challenge for animals. Identifying mechanisms responsible for relating information about the social world with mechanisms mediating pairbonding and mating tactics is crucial to fully appreciate the suite of factors driving mating systems. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.
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Receptores de Oxitocina/fisiología , Conducta Sexual Animal/fisiología , Conducta Social , Animales , Arvicolinae , Encéfalo/anatomía & histología , Química Encefálica/fisiología , Corteza Cerebral/metabolismo , Corteza Cerebral/fisiología , Femenino , Hipocampo/metabolismo , Hipocampo/fisiología , Fenómenos de Retorno al Lugar Habitual , Relaciones Interpersonales , Masculino , Memoria/fisiología , Núcleo Accumbens/metabolismo , Núcleo Accumbens/fisiología , Apareamiento , Receptores de Vasopresinas/fisiología , Tabique del Cerebro/metabolismo , Tabique del Cerebro/fisiología , Percepción Espacial/fisiología , TelemetríaRESUMEN
Limbic-associated cortical areas, such as the medial prefrontal and retrosplenial cortex (mPFC and RS, respectively), are involved in the processing of emotion, motivation, and various aspects of working memory and have been implicated in mating behavior. To determine whether the independent evolution of mating systems is associated with a convergence in cortical mechanisms, we compared the size of mPFC and RS between the monogamous prairie vole (Microtus ochrogaster) and the promiscuous meadow vole (Microtus pennsylvanicus), and between the monogamous California mouse (Peromyscus californicus) and the promiscuous white-footed mouse (Peromyscus leucopus). For both promiscuous mice and voles, the mPFC occupied a significantly larger percentage of total cortex than in the monogamous species. No significant differences were observed for the RS or overall cortex size with respect to mating system, supporting the convergent evolution of mPFC size, specifically. Individual differences in the mating behavior of male prairie voles (wandering versus pair-bonding), presumably facultative tactics, were not reflected in the relative size of the mPFC, which is likely a heritable trait. Given the importance of the mPFC for complex working memory, particularly object-place and temporal order memory, we hypothesize that the relatively greater size of the mPFC in promiscuous species reflects a greater need to remember multiple individuals and the times and locations in which they have been encountered in the home range.