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To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Pair bonding in humans and other socially monogamous species can have positive effects on health and well-being. These attachments also come with the potential for challenges such as separation, jealousy, or grief. Much of the work on the neurobiology of pair bonding in non-human primates has been carried out in coppery titi monkeys (Plecturocebus cupreus), a monogamous South American monkey, although these studies have been primarily in males. In the current study, we utilized female titi monkeys to experimentally examine responses to their monogamous male partner vs. a male stranger or being alone. Positron emission tomography (PET) scans were performed on eight adult female titi monkeys from well-established pairs. We used a within-subjects design in which each female underwent three different conditions after the fluorodeoxyglucose F18 (FDG) injection: a) the subject was reunited with her partner, b) encountered a stranger, or c) was alone in the experimental cage. Behavioural observations were recorded, and plasma assayed for cortisol. Females housed alone showed higher cortisol compared with either the partner or stranger conditions. FDG uptake was higher in the amygdala and hippocampus when interacting with the stranger than the partner. Proximity modulated the relationship between social condition and FDG uptake in several areas. Females entered into mutual proximity more frequently with the partner than with the stranger. Female titi monkeys have different physiological, neural, and behavioural reactions to being with their partner, a stranger male, or being alone.

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.

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.

Coppery titi monkeys maintain pair bonds through affiliative behaviours (e.g. tail twining, maintaining social proximity). Findings from previous studies suggest that the amount of time pairs spend in affiliative contact is not stable over time within pairs and differs across pairs. The present study investigates several predictors (temperament, age at pairing, pregnancy status and presence of infant) that may help explain observed changes in affiliation over time and between pairs. We hypothesized that affiliation varies for individual dyads and that time-varying and dyad level predictors explain variability in affiliation. We analysed pair affiliation using scan samples collected five times per day for 1 year for 29 pairs. We used Bayesian nonlinear mixed-effects effects modelling to test the effects of predictors. Pregnancy predicted higher affiliation levels (ϒ02 = 0.40, 95% highest posterior density interval (HPDI): [0.21, 0.58]). The presence of an infant and aggression did not predict variability in affiliation. Models would not converge when we included age at pairing, so we cannot draw conclusions about the role of age in affiliation. Findings from this study suggest that time-varying predictors like pregnancy status help explain the large degree of variability observed in affiliative interactions between partners in this species. It is possible that hormonal changes associated with pregnancy are driving changes in affiliative behaviours in pairs. An alternative explanation is that pairs that are more affiliative to begin with are more likely to get pregnant. Future studies will assess whether these patterns persist in subsequent pairings.

Social monogamy is a reproductive strategy characterized by pair living and defense of a common territory. Pair bonding, sometimes displayed by monogamous species, is an affective construct that includes preference for a specific partner, distress upon separation, and the ability of the partner to buffer against stress. Many seahorse species show a monogamous social structure in the wild, but their pair bond has not been well studied. We examined the gene expression of lined seahorses (Hippocampus erectus) during and after the process of pairing in the laboratory as well as color change (luminance), a potential form of social communication and behavioral synchrony between pair mates. When a seahorse of either sex was interacting with its pair mate, their changes in luminance ("brightness") were correlated and larger than when interacting with an opposite-sex stranger. At the conclusion of testing, subjects were euthanized, RNA was extracted from whole brains and analyzed via RNA sequencing. Changes in gene expression in paired males versus those that were unpaired included processes governing metabolic activity, hormones and cilia. Perhaps most interesting is the overlap in gene expression change induced by pairing in both male seahorses and male prairie voles, including components of hormone systems regulating reproduction. Because of our limited sample size, we consider our results and interpretations to be preliminary, and prompts for further exploration. Future studies will expand upon these findings and investigate the neuroendocrine and genetic basis of these behaviors.

Across many species, endocannabinoids play an important role in regulating social play, reward, and anxiety. These processes are mediated through at least two distinct cannabinoid receptors (CB), CB1 and CB2. CB1 expression is found in appreciable densities across regions of the brain that integrate memory with socio-spatial information; many of these regions have been directly linked to the neurobiology of pair bonding in monogamous species. Using receptor autoradiography, we provide the first distributional map of CB1 within the brains of closely related monogamous prairie voles and promiscuous meadow voles, and compare receptor densities across sexes and species in limbic regions. We observe CB1-specific signal using [3H] CP-55,940 and [3H] SR141716A, though the latter exhibited a lower signal to noise ratio. We confirmed the presence of CB2 in prairie vole spleen tissue using [3H] CP-55,940. However, we found no evidence of CB2 in the brain using either [3H] CP-55,940 or [3H] A-836,339. The overall distribution of putative CB1 in the brain was similar across vole species and followed the pattern of CB1 expression observed in other species-high intensity binding within the telencephalon, moderate binding within the diencephalon, and mild binding within the mesencephalon and metencephalon (aside from the cerebellar cortex). However, we found profound differences in CB1 densities across species, with prairie voles having higher CB1 binding in regions implicated in social attachment and spatial memory (e.g., periaqueductal gray, hippocampus). These findings suggest that CB1 densities, but not distribution, correlate with the social systems of vole species.

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.

With apologies, an incorrect author list was given in the article. An additional author, Chris von Rueden, (Jepson School of Leadership Studies, University of Richmond) also contributed to this work. Author Ryan Schacht's affiliation was out-of-date. His correct affiliation is: Department of Anthropology, East Carolina University.

Monogamy appears to have become the predominant human mating system with the emergence of highly unequal agricultural populations that replaced relatively egalitarian horticultural populations, challenging the conventional idea-based on the polygyny threshold model-that polygyny should be positively associated with wealth inequality. To address this polygyny paradox, we generalize the standard polygyny threshold model to a mutual mate choice model predicting the fraction of women married polygynously. We then demonstrate two conditions that are jointly sufficient to make monogamy the predominant marriage form, even in highly unequal societies. We assess if these conditions are satisfied using individual-level data from 29 human populations. Our analysis shows that with the shift to stratified agricultural economies: (i) the population frequency of relatively poor individuals increased, increasing wealth inequality, but decreasing the frequency of individuals with sufficient wealth to secure polygynous marriage, and (ii) diminishing marginal fitness returns to additional wives prevent extremely wealthy men from obtaining as many wives as their relative wealth would otherwise predict. These conditions jointly lead to a high population-level frequency of monogamy.

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.

Highly valued food items are often used as rewards to reinforce an animal's behavior. For social species, social interaction is rewarding and can drive an individual's behavior as well. In the currently study, we wanted to compare the efficacy of a food reward and a social reward on object discrimination learning in socially monogamous titi monkeys. We hypothesized that titi monkeys would perform more accurately for a social reward (their pair mate) than for a food reward (a highly desired food item). Eleven adult titi monkeys were tested with a two-object visual discrimination task for both types of reward. The colors and shapes of the objects in the two-object discrimination task were counterbalanced across subjects. During each trial, subjects were shown two objects, and the trial ended when the subject touched the reinforced shape (S+) or after 5 min. A correct trial was defined as one when the subject touched S+ first. We found that 45.5% of subjects were able to learn the task with a social reward, and 83.3% were able to learn the task with a food reward. We found that subjects balked more often and had fewer correct trials for the social reward. Finally, subjects took longer to approach the shapes for a social reward, possibly indicating lower motivation to engage in the task when a social reward is used compared to a food reward. Although significantly fewer subjects met criteria of success with the social reward than with the food reward, our results show that titi monkeys can learn a visual discrimination task with either type of reward.

Genetic monogamy is rare-at least at the level of a species-and monogamy can exist in the absence of sexual fidelity. Rather than focusing on mating exclusivity, it has become common to use the term "social monogamy" to describe a cluster of social features, including the capacity for selective and lasting social bonds, central to what humans call "love." Socially monogamous mammals often exhibit selective aggression toward strangers and form extended families. These features of social monogamy in mammals are supported by patterns of hormonal function originating in the neurobiology of maternity, including oxytocin, as well as a more primitive vasopressin pathway. Another key feature of social monogamy is reduced sexual dimorphism. Processes associated with sexual differentiation offer clues to the mysteries surrounding the evolution of monogamy. Although there is consistency in the necessary ingredients, it is likely that there is no single recipe for social monogamy. As reviewed here, genes for steroids and peptides and their receptors are variable and are subject to epigenetic regulation across the lifespan permitting individual, gender and species variations and providing substrates for evolution. Reduced sensitivity to gonadal androgens, and a concurrent increased reliance on vasopressin (for selective defense) and oxytocin (for selective affiliation) may have offered pathways to the emergence of social monogamy.

Understanding the neurobiology of social bonding in non-human primates is a critical step in understanding the evolution of monogamy, as well as understanding the neural substrates for emotion and behavior. Coppery titi monkeys (Callicebus cupreus) form strong pair bonds, characterized by selective preference for their pair mate, mate-guarding, physiological and behavioral agitation upon separation, and social buffering. Mate-guarding, or the "maintenance" phase of pair bonding, is relatively under-studied in primates. In the current study, we used functional imaging to examine how male titi monkeys viewing their pair mate in close proximity to a stranger male would change regional cerebral glucose metabolism. We predicted that this situation would challenge the pair bond and induce "jealousy" in the males. Animals were injected with [18F]-fluorodeoxyglucose (FDG), returned to their cage for 30 min of conscious uptake, placed under anesthesia, and then scanned for 1 hour on a microPET P4 scanner. During the FDG uptake, males (n=8) had a view of either their female pair mate next to a stranger male ("jealousy" condition) or a stranger female next to a stranger male (control condition). Blood and cerebrospinal fluid samples were collected and assayed for testosterone, cortisol, oxytocin, and vasopressin. Positron emission tomography (PET) was co-registered with structural magnetic resonance imaging (MRI), and region of interest analysis was carried out. Bayesian multivariate multilevel analyses found that the right lateral septum (Pr(b>0)=93%), left posterior cingulate cortex (Pr(b>0)=99%), and left anterior cingulate (Pr(b>0)=96%) showed higher FDG uptake in the jealousy condition compared to the control condition, while the right medial amygdala (Pr(b>0)=85%) showed lower FDG uptake. Plasma testosterone and cortisol concentrations were higher during the jealousy condition. During the jealousy condition, duration of time spent looking across at the pair mate next to a stranger male was associated with higher plasma cortisol concentrations. The lateral septum has been shown to be involved in mate-guarding and mating-induced aggression in monogamous rodents, while the cingulate cortex has been linked to territoriality. These neural and physiological changes may underpin the emotion of jealousy, which can act in a monogamous species to preserve the long-term integrity of the pair.

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.

Pair bonding leads to increases in dopamine D1 receptor (D1R) binding in the nucleus accumbens of monogamous prairie voles. In the current study, we hypothesized that there is similar up-regulation of D1R in a monogamous primate, the titi monkey (Callicebus cupreus). Receptor binding of the D1R antagonist [11 C]-SCH23390 was measured in male titi monkeys using PET scans before and after pairing with a female. We found that within-subject analyses of pairing show significant increases in D1R binding in the lateral septum, but not the nucleus accumbens, caudate, putamen, or ventral pallidum. The lateral septum is involved in a number of processes that may contribute to social behavior, including motivation, affect, reward, and reinforcement. This region also plays a role in pair bonding and paternal behavior in voles. Our observations of changes in D1R in the lateral septum, but not the nucleus accumbens, suggest that there may be broadly similar dopaminergic mechanisms underlying pair bonding across mammalian species, but that the specific changes to neural circuitry differ. This study is the first research to demonstrate neuroplasticity of the dopamine system following pair bonding in a non-human primate; however, substantial variability in the response to pairing suggests the utility of further research on the topic.

Social bonds are necessary for many mammals to survive and reproduce successfully. These bonds (i.e. pair-bonds, friendships, filial bonds) are characterized by different periods of development, longevity and strength. Socially monogamous species display certain behaviors not seen in many other mammals, such as adult pair-bonding and male parenting. In our studies of prairie voles (Microtus ochrogaster) and titi monkeys (Callicebus cupreus), we have examined the neurohormonal basis of these bonds. Here, we discuss the evidence from voles that aspects of adolescent and adult social behavior are shaped by early experience, including changes to sensory systems and connections, neuropeptide systems such as oxytocin and vasopressin, and alterations in stress responses. We will compare this with what is known about these processes during development and adulthood in other mammalian species, both monogamous and non-monogamous, and how our current knowledge in voles can be used to understand the development of and variation in social bonds. Humans are endlessly fascinated by the variety of social relationships and family types displayed by animal species, including our own. Social relationships can be characterized by directionality (either uni- or bi-directional), longevity, developmental epoch (infant, juvenile or adult) and strength. Research on the neurobiology of social bonds in animals has focused primarily on 'socially monogamous' species, because of their long-term, strong adult affiliative bonds. In this Review, we attempt to understand how the ability and propensity to form these bonds (or lack thereof), as well as the display of social behaviors more generally, are transmitted both genomically and non-genomically via variation in parenting in monogamous and non-monogamous species.

Relatively little is known about serotonergic involvement in pair-bonding despite its putative role in regulating social behavior. Here we sought to determine if pharmacological elevation of serotonin 1A (5-HT1A) receptor activity would lead to changes in social behavior in pair-bonded male titi monkeys (Callicebus cupreus). Adult males in established heterosexual pairs were injected daily with the selective 5-HT1A agonist 8-OH-DPAT or saline for 15days using a within-subjects design. Social behavior with the female pair-mate was quantified, and plasma concentrations of oxytocin, vasopressin, and cortisol were measured. When treated with saline, subjects showed reduced plasma oxytocin concentrations, while 8-OH-DPAT treatment buffered this decrease. Treatment with 8-OH-DPAT also led to decreased plasma cortisol 15minutes post-injection and decreased social behavior directed toward the pair-mate including approaching, initiating contact, lipsmacking, and grooming. The reduction in affiliative behavior seen with increased activity at 5-HT1A receptors indicates a substantial role of serotonin activity in the expression of social behavior. In addition, results indicate that the effects of 5-HT1A agonism on social behavior in adulthood differ between rodents and primates.

Mate-guarding and territorial aggression (both intra- and inter-sexual) are behavioral components of social monogamy seen in male coppery titi monkeys (Callicebus cupreus) both in the field and in the laboratory. Methodology for studying these behaviors in captivity facilitates the translation of questions between field and laboratory. In this study, we tested whether exposure to a mirror would stimulate mate-guarding behavior in male titi monkeys, and whether this exposure was accompanied by hormonal changes. Eight males were exposed to a mirror condition (treatment) or the back of the mirror (control) for five sessions, and behavioral responses were filmed. Blood samples were taken to measure levels of cortisol, oxytocin, and vasopressin. Lipsmacks (P

Partner preference, or the selective social preference for a pair mate, is a key behavioral indicator of social monogamy. Standardized partner preference testing has been used extensively in rodents but a single test has not been standardized for primates. The goal of this study was to develop a partner preference test with socially monogamous titi monkeys (Callicebus cupreus) adapted from the widely used rodent test. In Experiment 1, we evaluated the test with pairs of titi monkeys (N = 12) in a three-chambered apparatus for 3 hr. The subject was placed in the middle chamber, with grated windows separating it from its partner on one side and an opposite sex stranger on the other side. Subjects spent a greater proportion of time in proximity to their partners' windows than the strangers', indicating a consistent preference for the partner over the stranger. Touching either window did not differ between partners and strangers, suggesting it was not a reliable measure of partner preference. Subjects chose their partner more than the stranger during catch and release sessions at the end of the test. In Experiment 2, we compared responses of females with current partners (N = 12) in the preference test with other relationship types representing former attachment bonds (N = 13) and no attachment bond (N = 8). Only females from established pair bonds spent significantly more time near their partner's window compared to the stranger's indicating that this measure of preference was unique to current partners. Other measures of preference did not differentiate behavior toward a current partner and other relationship types. This test reproduces behavioral patterns found in previous studies in titi monkeys highlighting the accuracy of this new partner preference test. This test can be used as a standardized measure of partner preference in titi monkeys to quantitatively study pair bonding and evaluate factors influencing partner preference.

This paper is the introduction to a special issue on "'Monogamy' in Primates: Variability, Trends, and Synthesis." The term "monogamy" has undergone redefinition over the years, and is now generally understood to refer to certain social characteristics rather than to genetic monogamy. However, even the term "social monogamy" is used loosely to refer to species which exhibit a spectrum of social structures, mating patterns, and breeding systems. Papers in this volume address key issues including whether or not our definitions of monogamy should change in order to better represent the social and mating behaviors that characterize wild primates; whether or not primate groups traditionally considered monogamous are actually so (by any definition); ways in which captive studies can contribute to our understanding of monogamy; and what selective pressures might have driven the evolution of monogamous and non-monogamous single female breeding systems.

The opioid system is involved in infant-mother bonds and adult-adult bonds in many species. We have previously shown that μ opioid receptors (MORs) and κ opioid receptors (KORs) are involved in regulating the adult attachment of the monogamous titi monkey. The present study sought to determine the distribution of MOR and KOR in the titi monkey brain using receptor autoradiography. We used [(3)H][D-Ala(2),N-Me-Phe(4),Gly(5)-ol]-enkephalin (DAMGO) to label MORs and [(3)H]U69,593 to label KORs. MOR binding was heterogeneous throughout the titi monkey brain. Specifically, MOR binding was observed in the cingulate gyrus (CG), striatum, septal regions, diagonal band, amygdala, hypothalamus, hippocampus, and thalamus. Binding was particularly dense in the septum, medial amygdala, paraventricular nucleus of the hypothalamus, mediodorsal thalamus with moderate binding in the nucleus accumbens. Consistent with other primate species, MOR were also observed in "neurochemically unique domains of the accumbens and putamen" (NUDAPs). In general KOR binding was more homogenous. KORs were primarily found in the CG, striatum, amygdala and hippocampus. Dense KOR binding was observed in the claustrum. Relative MOR and KOR binding in the titi monkey striatum was similar to other humans and primates, but was much lower compared to rodents. Relative MOR binding in the titi monkey hypothalamus was much greater than that found in rodents. This study was the first to examine MOR and KOR binding in a monogamous primate. The location of these receptors gives insight into where ligands may be acting to regulate social behavior and endocrine function.

The μ opioid receptor (MOR) and κ opioid receptor (KOR) have been implicated in pair-bond formation and maintenance in socially monogamous species. Utilizing monogamous titi monkeys (Callicebus cupreus), the present study examined the potential role opioids play in modulating the response to separation, a potent challenge to the pair-bond. In Experiment 1, paired male titi monkeys were separated from their pair-mate for 30-min and then received saline, naloxone (1.0mg/kg), morphine (0.25mg/kg), or the KOR agonist, U50,488 (0.01, 0.03, or 0.1mg/kg) in a counter-balanced fashion, immediately prior to a 30-min reunion with their mate. Blood samples were collected immediately prior to and after the reunion. Males receiving morphine approached females less, initiated contact less, and females broke contact with the males less. The increase in cortisol in response to naloxone was greater compared to vehicle, and the increase in cortisol in response to the high dose of U50,488 compared to vehicle approached significance. In Experiment 2, paired males were treated with the KOR antagonist, GNTI (0.1, 0.3, or 1.0mg/kg), or saline 24h prior to a 60-min separation from their mate. Blood samples were collected at the time of injection and immediately before and after separation. Administration of the low dose of GNTI decreased the locomotor component of the separation response compared to vehicle. The present study found that the opioid system is involved in both the affiliative and separation distress components of a pair-bond, and these components are regulated by different opioid receptors.

AbstractMonogamy is ethnographically peculiar as an ethical ideal and emerged in the Early Middle Ages as a form of sexual repression imposed by the Church and employed by secular authorities to decompose powerful elite lineages. In its continued modern form, the independent and isolated monogamous household has been advanced as socially optimal by economists and as essential to civilization by anthropologists.   Although marriage, as a rightful claim on the sexuality of a woman, is a nearly universal institution, recent legislation and judicial opinion in both Europe and the United States have abrogated this basic marital right with the new crime of “marital rape”, thereby undermining the essential and defining characteristic of marriage. It is argued herein that these changes reflect the loss of relevance and significance of the domestic household to contemporary systems of capital accumulation; and it is in this new context that same-sex marriage becomes feasible.

The coppery titi monkey (Callicebus cupreus) is a socially monogamous New World primate that has been studied in the field and the laboratory to investigate the behavioral neuroendocrinology of primate pair bonding and parental care. Arginine vasopressin has been shown to influence male titi monkey pair-bonding behavior, and studies are currently underway to examine the effects of oxytocin on titi monkey behavior and physiology. Here, we use receptor autoradiography to identify the distribution of arginine vasopressin 1a receptor (AVPR1a) and oxytocin receptors (OXTR) in hemispheres of titi monkey brain (n=5). AVPR1a are diffuse and widespread throughout the brain, but the OXTR distribution is much more limited, with the densest binding being in the hippocampal formation (dentate gyrus, CA1 field) and the presubiculum (layers I and III). Moderate OXTR binding was detected in the nucleus basalis of Meynert, pulvinar, superior colliculus, layer 4C of primary visual cortex, periaqueductal gray (PAG), pontine gray, nucleus prepositus, and spinal trigeminal nucleus. OXTR mRNA overlapped with OXTR radioligand binding, confirming that the radioligand was detecting OXTR protein. AVPR1a binding is present throughout the cortex, especially in cingulate, insular, and occipital cortices, as well as in the caudate, putamen, nucleus accumbens, central amygdala, endopiriform nucleus, hippocampus (CA4 field), globus pallidus, lateral geniculate nucleus, infundibulum, habenula, PAG, substantia nigra, olivary nucleus, hypoglossal nucleus, and cerebellum. Furthermore, we show that, in the titi monkey brain, the OXTR antagonist ALS-II-69 is highly selective for OXTR and that the AVPR1a antagonist SR49059 is highly selective for AVPR1a. Based on these results and the fact that both ALS-II-69 and SR49059 are non-peptide, small-molecule antagonists that should be capable of crossing the blood-brain barrier, these two compounds emerge as excellent candidates for the pharmacological manipulation of OXTR and AVPR1a in future behavioral experiments in titi monkeys and other primate species.

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a 'monogamy window', because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that 'point of view' is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton's rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.

The role of opioid receptors in infant-mother attachment has been well established. Morphine, a preferential μ opioid receptor (MOR) agonist, attenuates separation distress vocalizations and decreases physical contact between infant and mother. However, there is little research on how opioid receptors are involved in adult attachment. The present study used the monogamous titi monkey (Callicebus cupreus) to explore the role of opioid receptors in the behavioral and physiological components of pair-bonding. In Experiment 1, paired male titi monkeys (N=8) received morphine (0.1, 0.5, or 1.0mg/kg), the opioid antagonist naloxone (1.0mg/kg), vehicle, or a disturbance control and were filmed with their pair-mate for 1h. In Experiment 2, the same eight males received morphine (0.25mg/kg), naloxone (1.0mg/kg), vehicle, or a disturbance control and were filmed for an hour without their pair-mates. All video sessions were scored for social and non-social behaviors. Blood was sampled immediately prior to drug administration and at the end of the hour session. Plasma was assayed for cortisol, oxytocin, and vasopressin. In Experiment 1, opioid manipulation had no effect on affiliative behaviors; however, morphine dose-dependently decreased locomotor behavior and increased scratching. In Experiment 2 in which males were separated from their pair-mates, naloxone increased locomotion. Morphine dose-dependently attenuated the rise in cortisol, while naloxone potentiated the increase of cortisol. The cortisol increase following naloxone administration was greater when a male was alone compared to when the male was with his pair-mate. Naloxone increased vasopressin but only when the male was tested without his pair-mate. The present study found that the absence of a pair-mate magnified naloxone's effects on stress-related hormones and behaviors, suggesting that the presence of a pair-mate can act as a social buffer against the stress-inducing effects of naloxone.

The monogamous prairie vole displays developmental sensitivity to early pharmacological manipulation in a number of species-typical social behaviors. The long-term consequences of altering the neonatal dopamine system are not well characterized. This study examined whether early manipulation of the dopamine system, a known mediator of adult prairie vole social behavior, during neonatal development would affect adult aggressive and attachment behaviors. Eight-day-old pups were given a single treatment with either 1 mg/kg of SKF38393 (D1 agonist), quinpirole (D2 agonist), SCH23390 (D1 antagonist), eticlopride (D2 antagonist), or saline vehicle. As adults, animals received tests for intrasexual aggression and partner preference. Activation of D1-like receptors in pups impaired partner preference formation, but had no effect on aggression. Other neonatal treatments had no effect on their behavior as adults. To determine whether D1 activation in pups induced changes in dopamine receptor expression, we performed autoradiography on striatal tissue from a second cohort of saline-treated and SKF38393-treated animals. Although sex differences were observed, we found no treatment differences in D1 or D2 receptor binding in any striatal subregion. This study shows that exposure to a single early pharmacological alteration of dopamine receptor activity may have long-term effects on the social behavior of prairie voles.

Early experiences can alter adaptive emotional responses necessary for social behavior as well as physiological reactivity in the face of challenge. In the highly social prairie vole (Microtus ochrogaster), manipulations in early life or hormonal treatments specifically targeted at the neuropeptides oxytocin (OT) and arginine vasopressin (AVP), have long-lasting, often sexually dimorphic, consequences for social behavior. Here we examine the hypothesis that behavioral changes associated with differential early experience, in this case handling the family during the first week of life, may be mediated by changes in OT or AVP or their brain receptors. Four early treatment groups were used, differing only in the amount of manipulation received during the first week of life. MAN1 animals were handled once on post-natal day 1; MAN1 treatment produces a pattern of behavior usually considered typical of this species, against which other groups were compared. MAN1-7 animals were handled once a day for post-natal days 1-7, MAN 7 animals were handled once on post-natal day 7, and MAN0 animals received no handling during the first week of life. When tested following weaning, males in groups that had received manipulation during the first few days of life (MAN1 and MAN1-7) displayed higher alloparenting than other groups. Neuroendocrine measures, including OT receptor binding and OT and AVP immunoreactivity, varied by early treatment. In brain areas including the nucleus accumbens, bed nucleus of stria terminalis and lateral septum, MAN0 females showed increased OT receptor binding. MAN1 animals also displayed higher numbers of immunoreactive OT cell bodies in the supraoptic nucleus. Taken together these findings support the broader hypothesis that experiences in the first few days of life, mediated in part by sexually dimorphic changes in neuropeptides, especially in the receptor for OT, may have adaptive consequences for sociality and emotion regulation.

We examined intergenerational and epigenetic effects of early handling manipulations on the social behavior of the prairie vole (Microtus ochrogaster), a monogamous rodent. Laboratory-born parents and their newborn pups were assigned to either a MAN0 "zero handling" manipulation (transfer with a cup during weekly cage changes) or a MAN1 "gloved handling" manipulation (transfer with a gloved hand). Previous studies from our laboratory (Bales et al., 2007) showed that MAN0 juvenile males that received this manipulation as pups are less alloparental and that MAN0 adult females that received this manipulation as pups display impaired pair-bonding. In the present study, when MAN0 and MAN1 pups reached adulthood, they were mated in three combinations (MAN1 female x MAN1 male; MAN0 female x MAN1 male; MAN1 female and MAN0 male). Once the pairs produced offspring, we examined their parental behavior towards their own pups. The offspring of these pairings (F2 generation) also were tested as juveniles for alloparental behavior. MAN1 females paired with a MAN0 male displayed higher levels of parenting behaviors. In the F2 generation, juvenile offspring with a MAN0 parent were less alloparental than were offspring from other pairs. These results suggest that early experiences can be transmitted intergenerationally.

Stress and anxiety play a role in many psychological processes including social behavior. The present study examines the effects of urocortin II (UCN II) on spontaneous parental behavior in adult prairie voles (Microtus ochrogaster). UCN II was found to increase passive parental behavior in voles while not affecting any stress-related measures. Delineating the mechanism of this change will aid in our understanding of the regulation of parenting.

The neurobiology of social bonding, despite its relevance to human mental health, has been studied primarily in rodents. In this study we used position emission tomography (PET), registered with structural magnetic resonance imaging (MRI) to investigate central glucose uptake in 17 males of a monogamous primate species, the titi monkey (Callicebus cupreus). Twelve pair-bonded males (including six with a lesion of the prefrontal cortex) and five lone males were scanned. The five lone males were re-scanned 48 h after pairing with a female. Significant differences in glucose uptake were found between males in long-term pair-bonds and lone males in areas including the nucleus accumbens, ventral pallidum, medial preoptic area, medial amygdala, and the supraoptic nucleus of the hypothalamus. In paired before and after comparisons, males showed significant changes following pairing in the right nucleus accumbens and ventral pallidum but not in other areas. Lesioned males showed significantly higher uptake in the posterior cingulate cortex than all other males. These results indicate some basic similarities between rodents and primates in the formation and maintenance of selective social bonds, but emphasize the importance of studying long-term maintenance in addition to short-term formation of social bonds.

The present study examines the developmental consequences of neonatal exposure to oxytocin on adult social behaviors in female prairie voles (Microtus ochrogaster). Female neonates were injected within 24 h of birth with isotonic saline or one of four dosages of oxytocin (OT). As adults, females were tested in an elevated plus-maze paradigm (a measure of anxiety and exploratory behavior), and for alloparental behavior and partner preferences. At 2 mg/kg OT, females took longer to approach pups, but were the only group to form a statistically significant within-group partner preference. At 4 mg/kg OT, females retrieved pups significantly more frequently but no longer displayed a partner preference; while females treated developmentally with 8 mg/kg spent significantly more time in side-to-side contact with a male stranger than any other treatment group. OT may have broad developmental consequences, but these effects are not linear and may both increase and decrease the propensity to display behaviors such as pair-bonding.

The goal of this study was to examine the effects of early life experiences on the subsequent expression of traits characteristic of social monogamy in prairie voles (Microtus ochrogaster). During cage changes parents and their offspring were either transferred between cages in a cup (zero manipulation, MAN0) or with a gloved hand (one manipulation, MAN1). Following weaning the offspring were tested for alloparental behavior. In adulthood they were tested for the capacity to form partner preferences, behavior in an elevated plus-maze (EPM), and corticosterone levels. MAN0 males (but not females) showed lower levels of alloparental behavior than MAN1 males. MAN0 females (but not males) were less likely to form pair bonds than MAN1 females. MAN0 animals of both sexes were less exploratory in the EPM than MAN1 counterparts. These experiments support the hypothesis that behaviors used to characterize monogamy are vulnerable in a sex-specific manner to early experience.

Developmental exposure to oxytocin (OT) or oxytocin antagonists (OTAs) has been shown to cause long-lasting and often sexually dimorphic effects on social behaviors in prairie voles (Microtus ochrogaster). Because regulation of social behavior in monogamous mammals involves central receptors for OT, arginine vasopressin (AVP), and dopamine, we examined the hypothesis that the long-lasting, developmental effects of exposure to neonatal OT or OTA might reflect changes in the expression of receptors for these peptides. On postnatal day 1, prairie voles were injected intraperitoneally with either OT (1 mg/kg), an OTA (0.1 mg/kg), saline vehicle, or were handled only. At approximately 60 days of age, vasopressin V1a receptors, OT receptors (OTR) and dopamine D2 receptor binding were quantified using receptor autoradiography in brain tissue taken from males and females. Significant treatment effects on V1a binding were found in the bed nucleus of the stria terminalis (BNST), cingulate cortex (CgCtx), mediodorsal thalamus (MdThal), medial preoptic area of the hypothalamus (MPOA), and lateral septum (LS). The CgCtx, MPOA, ventral pallidum, and LS also showed significant sex by treatment interactions on V1a binding. No significant treatment or sex differences were observed for D2 receptor binding. No significant treatment difference was observed for OTR receptor binding, and only a marginal sex difference. Changes in the neuropeptide receptor expression, especially the V1a receptor, may help to explain sexually dimorphic changes in behavior that follow comparable neonatal manipulations.

Apparently monogamous animals often prove, upon genetic inspection, to mate polygamously. Seahorse males provide care in a brood pouch. An earlier genetic study of the Western Australian seahorse demonstrated that males mate with only one female for each particular brood. Here we investigate whether males remain monogamous in sequential pregnancies during a breeding season. In a natural population we tagged males and sampled young from two successive broods of 14 males. Microsatellite analyses of parentage revealed that eight males re-mated with the same female, and six with a new female. Thus, in this first study to document long-term genetic monogamy in a seahorse, we show that switches of mates still occur. Polygynous males moved greater distances between broods, and tended to have longer interbrood intervals, than monogamous males, suggesting substantial costs associated with the breaking of pair bonds which may explain the high degree of social monogamy in this fish genus.

This paper explores the workings of stratified societies in which there is primogeniture and where the nobility practice monogamous marriage with a double standard of sexual fidelity. We model a simple stratified society and define the reproductive values of the male and female nobility relative to that of commoners. We then explore implications of the hypothesis that preferences have evolved to favor maximization of reproductive value. The hypothesis is tested against fragmentary data from ancient civilizations and quite detailed information about the British aristocracy in the seventeenth and eighteenth centuries.