The Evolution of Mate Attachment.

AbstractWhether natural selection leads to attachment in monogamous pair bonds has seldom been addressed. Operationally defining attachment as a behavioral modifier that decreases divorce probability with pair duration, we develop a model for the evolution of attachment. If divorce (the ending of a pair bond when both individuals survive to the next breeding season) is more likely to occur out of poor-quality reproductive opportunities (i.e., poor territory or low-quality mate), individuals in experienced pairs are more likely to be found in high-quality opportunities. Consequently, when divorce decisions occur using imperfect information from reproductive success, pair duration provides individuals with information about the quality of their reproductive opportunity and attachment can evolve. We show that high survival rates, divorce propensities, and probabilities of nest failure favor the evolution of attachment. Attachment is also more likely to evolve when individuals can directly assess the quality of their reproductive opportunity (as opposed to relying on imperfect information from reproductive success), when the quality of the reproductive opportunity has adult survival ramifications, and when divorce coevolves with attachment. We show that our core conclusions are robust to a variety of assumptions using individual-based simulations. Our results clarify how attachment can be adaptive and suggest that studying pair bonds as dynamic entities is a promising avenue for future work.

Hypothalamic vasopressin neural densities are higher in male Mongolian gerbils after separation from a pair bond partner and may facilitate behavior to form a new bond.

Although pair bonding has been studied for several decades, only somewhat recently have researchers began studying the neural consequences of separation from a pair bond partner. Here we examined the impact of partner separation on the socially monogamous Mongolian gerbil. Using a within-subjects design, we assessed nonsocial, nonreproductive, and reproductive behavior in male gerbils pre- and post- either 4 weeks of cohabitation with or separation from a pair bond partner. We then conducted an immediate early gene study to examine the influence of partner separation on hypothalamic oxytocin and vasopressin neural responses to interactions with a novel, opposite-sex conspecific.

Effects of oxytocin receptor agonism on acquisition and expression of pair bonding in male prairie voles.

There is much interest in targeting the activity in the oxytocin system to regulate social bonding. However, studies with exogenous administration of oxytocin face the caveats of its low stability, poor brain permeability and insufficient receptor specificity. The use of a small-molecule oxytocin receptor-specific agonist could overcome these caveats. Prior to testing the potential effects of a brain-penetrant oxytocin receptor agonist in clinical settings, it is important to assess how such an agonist would affect social bonds in animal models. The facultatively monogamous prairie voles (Microtus ochrogaster), capable of forming long-term social attachments between adult individuals, are an ideal rodent model for such testing. Therefore, in a series of experiments we investigated the effects of the recently developed oxytocin receptor-specific agonist LIT-001 on the acquisition and expression of partner preference, a well-established model of pair bonding, in prairie voles. LIT-001 (10 mg/kg, intraperitoneal), as expected, facilitated the acquisition of partner preference when administered prior to a 4hr cohabitation. In contrast, while animals injected with vehicle after the 4hr cohabitation exhibited significant partner preference, animals that were injected with LIT-001 did not show such partner preference. This result suggests that OXTR activation during expression of pair bonding can inhibit partner preference. The difference in effects of LIT-001 on acquisition versus expression was not due to basal differences in partner preference between the experiments, as LIT-001 had no significant effects on expression of partner preference if administered following a shorter (2hr-long) cohabitation. Instead, this difference agrees with the hypothesis that the activation of oxytocin receptors acts as a signal of presence of a social partner. Our results indicate that the effects of pharmacological activation of oxytocin receptors crucially depend on the phase of social attachments.

Disruption in cortisol synchrony and pair-dissolution in the serially monogamous convict cichlid (Amatitlania nigrofasciata).

Endocrine synchronization is a biological process often associated with social bonding. The mechanisms that mediate this process have been well studied in many vertebrate clades with evolved complex social behaviors. However, studies focusing on such processes in the less neurologically complex teleost clade are surprisingly lacking. In this study, we investigated the hypothesis that mated pairs of convict cichlids (Amatitlania nigrofasciata) perform cortisol synchronization and that the disruption of this might accompany pair-bond instability. Mated pairs were subjected to both behavioral and non-invasive waterborne hormonal assays to better understand the biological complexity of endocrine synchrony and its role in pair-bonding. Baseline cortisol assays indicated a positive correlation between male and female cortisol levels. Individuals that were subjected to a prolonged separation from their mate exhibited a negative correlation in cortisol synchrony after being reunited with their mate. Cortisol synchrony was disrupted, but pairs did not show a significant variance of intrapair aggression after initial pair reunion. However, more than half of the pairs that received the stressor exhibited significantly higher levels of intrapair aggression than their time matched controls approximately 1-7 days following this reunion, indicating pair-dissolution. Concurrently, pairs who underwent the stressor but maintained their bonds did not display an increase in intrapair aggression and also re-synchronized their cortisol levels. Not only does this study provide crucial insights in regard to the role of cortisol synchrony in serially monogamous systems, but it also suggests that the mechanisms that mediate the synchronization of endocrine through the formation of social bonds are more evolutionarily conserved than originally thought.

The social and defensive function of olfactory behaviors in a pair-living sexually monogamous primate.

Olfactory behaviors serve a wide variety of social functions in mammals. Odor may signal information about attributes of individuals important for mating and reproduction. Olfactory behaviors, such as scent-marking, may also function as part of home range or resource defense strategies. We assessed the potential social and home range defense functions of olfactory behavior in a pair-living and sexually monogamous primate, Azara's owl monkey (Aotus azarae), in the Argentinian Chaco. This is the most extensive investigation of owl monkey olfactory behaviors in the wild. Individuals regularly performed olfactory behaviors (group mean + SD = 1.3 + 0.5 per hour). The patterns were generally comparable to those observed in studies of captive owl monkeys, except that urine washing was the most common behavior in the wild, as opposed to scent-marking and genital inspections. Most olfactory behaviors were performed by adults, and there were striking sex differences in genital inspections: almost all consisted of an adult male inspecting the paired adult female. These findings suggest that olfactory behaviors play an important role in signaling and coordinating reproduction among owl monkeys, particularly during periods of female conception and pregnancy. Additionally, our research indicates that these behaviors may also serve as a defense strategy for maintaining the core area of their home ranges. This study offers the first assessment of the role of olfactory behaviors in reproductive contexts and home range defense in pair-living, monogamous platyrrhine primates.

Epigenetic aging studies of pair bonding in prairie voles.

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

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.

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.

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.

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.

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.