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.

Social experiences shape song preference learning independently of developmental exposure to song.

Communication governs the formation and maintenance of social relationships. The interpretation of communication signals depends not only on the signal's content but also on a receiver's individual experience. Experiences throughout life may interact to affect behavioural plasticity, such that a lack of developmental sensory exposure could constrain adult learning, while salient adult social experiences could remedy developmental deficits. We investigated how experiences impact the formation and direction of female auditory preferences in the zebra finch. Zebra finches form long-lasting pair bonds and females learn preferences for their mate's vocalizations. We found that after 2 weeks of cohabitation with a male, females formed pair bonds and learned to prefer their partner's song regardless of whether they were reared with ('normally reared') or without ('song-naive') developmental exposure to song. In contrast, females that heard but did not physically interact with a male did not prefer his song. In addition, previous work has found that song-naive females do not show species-typical preferences for courtship song. We found that cohabitation with a male ameliorated this difference in preference. Thus, courtship and pair bonding, but not acoustic-only interactions, strongly influence preference learning regardless of rearing experience, and may dynamically drive auditory plasticity for recognition and preference.

Benefits of Pair-Bond Duration on Reproduction in a Lifelong Monogamous Cooperative Passerine.

AbstractLong-term social and genetic monogamy is rare in animals except birds, but even in birds it is infrequent and poorly understood. We investigated possible advantages of monogamy in a colonial, facultative cooperatively breeding bird from an arid, unpredictable environment, the sociable weaver (Philetairus socius). We documented divorce and extrapair paternity of 703 pairs over 10 years and separated effects of pair duration from breeding experience by analyzing longitudinal and cross-sectional datasets. Parts of the colonies were protected from nest predation, thereby limiting its stochastic and thus confounding effect on fitness measures. We found that 6.4% of sociable weaver pairs divorced and 2.2% of young were extrapair. Longer pair-bonds were associated with more clutches and fledglings per season and with reproducing earlier and later in the season, when snake predation is lower, but not with increased egg or fledgling mass or with nestling survival. Finally, the number of helpers at the nest increased with pair-bond duration. Results were similar for protected and unprotected nests. We suggest that long-term monogamy is associated with a better capacity for exploiting a temporally unpredictable environment and helps to form larger groups. These results can contribute to our understanding of why long-term monogamy is frequently associated with unpredictable environments and cooperation.

Prairie voles as a model for adaptive reward remodeling following loss of a bonded partner.

Loss of a loved one is a painful event that substantially elevates the risk for physical and mental illness and impaired daily function. Socially monogamous prairie voles are laboratory-amenable rodents that form life-long pair bonds and exhibit distress upon partner separation, mirroring phenotypes seen in humans. These attributes make voles an excellent model for studying the biology of loss. In this review, we highlight parallels between humans and prairie voles, focusing on reward system engagement during pair bonding and loss. As yearning is a unique feature that differentiates loss from other negative mental states, we posit a model in which the homeostatic reward mechanisms that help to maintain bonds are disrupted upon loss, resulting in yearning and other negative impacts. Finally, we synthesize studies in humans and voles that delineate the remodeling of reward systems during loss adaptation. The stalling of these processes likely contributes to prolonged grief disorder, a diagnosis recently added to the Diagnostic and Statistical Manual for Psychiatry.

Evidence for individual vocal recognition in a pair-bonding poison frog, Ranitomeya imitator.

Individually distinctive vocalizations are widespread in nature, although the ability of receivers to discriminate these signals has only been explored through limited taxonomic and social lenses. Here, we asked whether anuran advertisement calls, typically studied for their role in territory defense and mate attraction, facilitate recognition and preferential association with partners in a pair-bonding poison frog (Ranitomeya imitator). Combining no- and two-stimulus choice playback experiments, we evaluated behavioral responses of females to male acoustic stimuli. Virgin females oriented to and approached speakers broadcasting male calls independent of caller identity, implying that females are generally attracted to male acoustic stimuli outside the context of a pair bond. When pair-bonded females were presented with calls of a mate and a stranger, they showed significant preference for calls of their mate. Moreover, behavioral responses varied with breeding status: females with eggs were faster to approach stimuli than females that were pair bonded but did not currently have eggs. Our study suggests a potential role for individual vocal recognition in the formation and maintenance of pair bonds in a poison frog and raises new questions about how acoustic signals are perceived in the context of monogamy and biparental care.

Intense Body Contact Increases Homosexual Pair Bond Stability in Female Japanese Macaques (Macaca fuscata).

The Japanese macaque (Macaca fuscata) has become a key species for studying homosexual behavior over recent decades. With the non-conceptive nature, their same-sex consortships illustrate that individual partner preferences can exist beyond direct reproductive benefits or apparent sociosexual strategies. An open question is whether the behavior shared between partners in consortship directly affects their choice to remain with a partner. With this study, we examined behavioral aspects underlying consortship temporal patterns in these promiscuous and bisexual primates. While these patterns could be relevant in both homo- and heterosexual consortships, our study primarily focused on female-female pairs. We hypothesized that the stability of consortships (duration and occurrence) is influenced by a pair's sexual behavior, mutual sexual stimulation, and close affiliative inter-mount behaviors involving high-intensity body contact. A semi-free population of Japanese macaques was observed over one mating season. In total, 40 h of focal data on female-female consortship behaviors were analyzed. Forty-six percent of all sexually mature females engaged in homosexual interactions. Our behavioral analyses of female-female pairs found that close body contact, rather than grooming or sexual interactions, was correlated with the stability of homosexual consortships. The greater the amount of huddling and embracing a pair engaged in, the more likely they were to stay together and reunite again. However, the frequency of mounting, rubbing or thrusting had no discernable effect on consortship stability. The results of this study thus add important knowledge to partner qualities in promiscuous primates as well as to inter-group differences of homosexual behavior in Japanese macaques.

Nucleus accumbens dopamine release reflects the selective nature of pair bonds.

In monogamous species, prosocial behaviors directed toward partners are dramatically different from those directed toward unknown individuals and potential threats. Dopamine release in the nucleus accumbens has a well-established role in social reward and motivation, but how this mechanism may be engaged to drive the highly divergent social behaviors directed at a partner or unfamiliar conspecific remains unknown. Using monogamous prairie voles, we first employed receptor pharmacology in partner preference and social operant tasks to show that dopamine is critical for the appetitive drive for social interaction but not for low-effort, unconditioned consummatory behaviors. We then leveraged the subsecond temporal resolution of the fluorescent biosensor, GRABDA, to ask whether differential dopamine release might distinguish between partner and novel social access and interaction. We found that partner seeking, anticipation, and interaction resulted in more accumbal dopamine release than the same events directed toward a novel vole. Further, partner-associated dopamine release decreased after prolonged partner separation. Our results are consistent with a model in which dopamine signaling plays a prominent role in the appetitive aspects of social interactions. Within this framework, differences in partner- and novel-associated dopamine release reflect the selective nature of pair bonds and may drive the partner- and novel-directed social behaviors that reinforce and cement bonds over time. This provides a potential mechanism by which highly conserved reward systems can enable selective, species-appropriate social behaviors.

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.

Attachment across the lifespan: Examining the intersection of pair bonding neurobiology and healthy aging.

Increasing evidence suggests that intact social bonds are protective against age-related morbidity, while bond disruption and social isolation increase the risk for multiple age-related diseases. Social attachments, the enduring, selective bonds formed between individuals, are thus essential to human health. Socially monogamous species like the prairie vole (M. ochrogaster) form long-term pair bonds, allowing us to investigate the mechanisms underlying attachment and the poorly understood connection between social bonds and health. In this review, we explore several potential areas of focus emerging from data in humans and other species associating attachment and healthy aging, and evidence from prairie voles that may clarify this link. We examine gaps in our understanding of social cognition and pair bond behavior. Finally, we discuss physiologic pathways related to pair bonding that promote resilience to the processes of aging and age-related disease. Advances in the development of molecular genetic tools in monogamous species will allow us to bridge the mechanistic gaps presented and identify conserved research and therapeutic targets relevant to human health and aging.

Possible effects of pair bonds on general cognition: Evidence from shared roles of dopamine.

Pair bonding builds on preexisting dopamine connectivity to help form and maintain the bond. The involvement of dopaminergic pathways in pair bonding has stimulated research linking pair bonds to other dopamine-dependent processes, like addiction and social cognition (Burkett & Young, 2012; Yetnikoff, Lavezzi, Reichard, & Zahm, 2014). Less studied is the relationship of pair bonding to non-social cognitive processes. The first half of this review will provide an overview of pair bonding and the role of dopamine within social processes. With a thorough review of the literature, the current study will identify the ways the dopaminergic pathways critical for pair bonding also overlap with cognitive processes. Highlighting dopamine as a key player in pair bonds and non-social cognition will provide evidence that pair bonding can alter general cognitive processes like attention, working memory, cognitive flexibility, and impulse control.

Divorce rate in monogamous birds increases with male promiscuity and migration distance.

Socially monogamous birds may break up their partnership by a so-called 'divorce' behaviour. Divorce rates vary immensely across avian taxa that have a predominantly monogamous social mating system. Although various factors associated with divorce have been tested, broad-scale drivers of divorce rate remain contentious. Moreover, the influence of sexual roles in divorce still needs further investigation because of the conflicting interests of males and females over mating and fertilization. Here, we applied phylogenetic comparative methods to analyse one of the largest datasets ever compiled that included divorce rates from published studies of 186 avian species from 25 orders and 61 families. We tested correlations between divorce rate and a group of factors: 'promiscuity' of both sexes (propensity to polygamy), migration distance and adult mortality. Our results showed that only male promiscuity, but not female promiscuity, had a positive relationship with divorce rate. Furthermore, migration distance was positively correlated with divorce rate, whereas adult mortality rate showed no direct relationship with divorce rate. These findings indicated that divorce might not be a simple adaptive (by sexual selection) or non-adaptive strategy (by accidental loss of a partner) in birds but it could be a mixed response to sexual conflict and stress from the ambient environment.

How to be a good partner and father? The role of adult males in pair bond maintenance and parental care in Javan gibbons.

In pair-living species, female and male pairs may maintain stable social bonds by adjusting spatial and social associations. Nevertheless, each sex invests differently to maintain the pair bond, and the investment can depend on the presence of paternal care or 'male services.' While most species live in pairs, the sex responsible for pair bond maintenance in gibbons is still controversial. We investigated pair bond maintenance and parental care in three pairs of wild Javan gibbons in Gunung Halimun-Salak National Park, Indonesia, for over 21 months. We found that Javan gibbon fathers groomed their offspring more than adult females, especially as offspring got older. While both parents increased playing time with offspring when offspring became older and more independent, fathers played with offspring 20 times more than mothers on average. Grooming within Javan gibbon pairs was male-biased, suggesting that pair bond maintenance was heavily the job of males. However, offspring age as a proxy for paternal care did not affect the pair bond maintenance. Our study highlights that adult male Javan gibbons may have an important role in pair bond maintenance and the care of juveniles.

Male-male relationships in chimpanzees and the evolution of human pair bonds.

The evolution of monogamy has been a central question in biological anthropology. An important avenue of research has been comparisons across "socially monogamous" mammals, but such comparisons are inappropriate for understanding human behavior because humans are not "pair living" and are only sometimes "monogamous." It is the "pair bond" between reproductive partners that is characteristic of humans and has been considered unique to our lineage. I argue that pair bonds have been overlooked in one of our closest living relatives, chimpanzees. These pair bonds are not between mates but between male "friends" who exhibit enduring and emotional social bonds. The presence of such bonds in male-male chimpanzees raises the possibility that pair bonds emerged earlier in our evolutionary history. I suggest pair bonds first arose as "friendships" and only later, in the human lineage, were present between mates. The mechanisms for these bonds were co-opted for male-female bonds in humans.

Male song of the Aquatic Warbler, a promiscuous bird without paternal care, is more complex than previously thought.

The Aquatic Warbler Acrocephalus paludicola is one of the rarest European passerines and is characterised by promiscuity, lack of pair-bonds and female-only parental care. This makes the species an important model for studying the function of avian courtship song. The song of the Aquatic Warbler consists of whistle and rattle phrases produced as discontinuous A-, B- and C-songs, which are built by a single rattle, a rattle and a whistle, and more than two phrases of both kinds, respectively. The A- and B-songs are thought to be aggressive signals in male-male interactions, while C-songs are thought to be important for female choice. Here, we analysed recordings of 40 individually marked males, and determined the phrase repertoire. The enumerated repertoire (males recorded for ≥ 10 min) ranged from 16 to 158 (mean 99), however, it did not capture the complete phrase repertoires. We then used models from species diversity ecology to estimate the actual phrase repertoire size, which ranged between 18 and 300 phrases (mean 155). The estimated repertoire was predicted by the number of C-songs. The rattle repertoire was larger than the whistle repertoire, and both positively correlated with the number of C-songs. Our study indicates that male Aquatic Warblers have highly complex phrase repertoires that vary widely in size. Their courtship song is flexible and efficient, enabling relative song complexity to be demonstrated in a short sample, thus facilitating both female attraction through the quick presentation of large phrase repertoires and rival deterrence through the production of many short and simple A- and B-songs.

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.

Initial compatibility during a "Speed-Dating" test predicts postpairing affiliation in titi monkeys (Plecturocebus cupreus).

Behavioral compatibility plays a critical role in shaping how potential mates interact with and evaluate each other and whether they choose to pursue a relationship. Compatibility is especially important for mate choice and relationship quality in pair-bonding species that form long-term attachments between mates. Although this process has been studied in humans and birds, relatively few studies have investigated it in non-human primates. In this study, we investigated whether pairing titi monkeys (Plecturocebus cupreus) based on initial compatibility increased postpairing affiliation between mates. Subjects were 12 unpaired adult titi monkeys (two cohorts of three males and three females). We determined each subject's initial interest in each opposite-sex potential mate in their cohort across a series of six 30-min interaction periods (i.e., "speed-dates"). To determine initial compatibility, we used the Social Relations Model to calculate relationship effects in initial interest (how much each subject uniquely preferred each potential mate beyond their own affiliative disposition and their partner's popularity). We then paired monkeys in a way that maximized net relationship effects between pairs, and measured longitudinal pair affiliation (Proximity, Contact, Tail Twining, and Combined Affiliation) for 6 months postpairing using daily scan-sample observations and monthly home-cage video recordings. Multilevel models showed that, on average, the six speed-dating pairs exhibited higher levels of Tail Twining (determined from scan-sample observations; ß = 0.31) compared to a group of 13 age-matched colony pairs that were determined quasi-randomly without quantifying compatibility. The degree of initial compatibility within speed-dating pairs also predicted higher levels of Combined Affiliation (determined from video recordings) at earlier post-pairing time points, with the association peaking at 2 months postpairing (ß = 0.57). These findings suggest that initial compatibility facilitates pair bonding in titi monkeys. We conclude by discussing how the speed-dating design can be used for colony management to inform pair-housing decisions.

Is the pair bond a human universal? An analytical essay.

I argue the impulse to form a dyadic love bond and not the desire for sexual release accounts for the formation of a universality of the pair bond. This impulse is not recent but has been a pervasive force throughout human history. Recently, a reversionist position has argued we are more of a hybrid species that easily and readily shifts between a pair bond and a plural partner family arrangement. Although most humans live out their lives in a sexually monogamous union, it is not something that comes easily or naturally. Sexual monogamy requires adopting an ethical stance and personal dedication to maintain it. This raises the question: if humans need to be vigilant in their moral commitment to remain sexually faithful, does this vigilance extend also to the domain of love? Is it possible to find greater contentment and life-satisfaction in forming simultaneously sexual and emotional unions with a variety of individuals. This is the central question that lies at the core of the pair bond deniers who insist humans are not a pair bond species and can find fulfilment in a pluralistic love bond. I probe (below) the social and emotional nuances associated with what it means to be in an enduring love bond through exploring the social and psychological complexities often associated with being in love. I will then discuss efforts by groups and individuals who have sought to establish social bonds not organised around an exclusive pair bond, and what their efforts reveal about underlying human psychology. My analysis concludes with rendering an assessment of the relative success of the social and personal experiments in the search to find a more fulfilling arena for love.

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.

Recovering from a broken heart.

A molecular signature found in the brains of monogamous prairie voles begins to decay after prolonged separation from their partner.

Partner separation rescues pair bond-induced decreases in hypothalamic oxytocin neural densities.

Studies in prairie voles (Microtus ochrogaster) have shown that although formation of the pair bond is accompanied by a suite of behavioral changes, a bond between two voles can dissolve and individuals can form new pair bonds with other conspecifics. However, the neural mechanisms underlying this behavioral flexibility have not been well-studied. Here we examine plasticity of nonapeptide, vasopressin (VP) and oxytocin (OT), neuronal populations in relation to bonding and the dissolution of bonds. Using adult male and female prairie voles, animals were either pair bonded, co-housed with a same-sex sibling, separated from their pair bond partner, or separated from their sibling. We examined neural densities of VP and OT cell groups and observed plasticity in the nonapeptide populations of the paraventricular nucleus of the hypothalamus (PVN). Voles that were pair bonded had fewer PVN OT neurons, suggesting that PVN OT neural densities decrease with pair bonding, but increase and return to a pre-pair bonded baseline after the dissolution of a pair bond. Our findings suggest that the PVN nonapeptide cell groups are particularly plastic in adulthood, providing a mechanism by which voles can exhibit context-appropriate behavior related to bond status.