Stable Pair Bonds Research Articles

Adolescence Predatory Risk Alters Social Behaviors and Cognitive Ability and Central Oxytocin and Vasopressin Expression in Adult Brandt’s Voles

Introduction: Stress during adolescence causes long-term behavioral changes in adulthood. We previously found that adolescent exposure to predatory risk augments adolescent social contact and adult parental behavior in Brandt’s voles (Lasiopodomys brandtii). Methods: Here, we determined whether this experience alters sexual behavior, pair-bond formation, and recognition ability as well as basal HPA axis activity, central oxytocin (OT), and arginine-vasopressin (AVP) expression in adulthood. Results: In the social interaction test, repeated cat odor (CO) exposure enhanced the frequency of lordosis by female voles toward an unfamiliar opposite-sex conspecific. CO voles preferred to engage with their partners after 48-h cohabitation whereas the control groups did not, which may reflect stable pair bonds in the CO treatment group. Furthermore, adolescent exposure to CO inhibited novel object recognition and place recognition ability, while it influenced social recognition only among adult males. No effect of adolescent CO exposure was observed for basal HPA axis activity, showing a habituation effect. Finally, we found that CO exposure increased OT and decreased AVP expression in the hypothalamus, including the paraventricular nucleus and anterior hypothalamus. The levels of OT in the medial amygdala were lower, and AVP in the lateral septum was higher in CO voles compared with the control. Conclusion: These findings demonstrate that adolescent exposure to predator risk promotes adult reproductive behavior of Brandt’s voles. Deficits in recognition ability may necessitate alterations in reproductive strategies to enhance inclusive fitness. OT and AVP systems may play a modulatory role in the alteration of social behaviors elicited by adolescent predatory risk.

Relationship quality underpins pair bond formation and subsequent reproductive performance

Despite the ecological importance of pair bonding, the ontogeny of pair bond formation remains poorly understood. We capitalized on long-term high-resolution tracking of social interactions across replicated colonies of captive zebra finches, Taeniopygia guttata, to map the dynamics of social relationships prior to reproduction and to identify the role that relationship quality plays in subsequent reproductive performance. We found that pairs that developed stronger and more stable social relationships outside the breeding season were more likely to breed together and form a pair bond. Moreover, pairs that formed a stable social relationship initiated reproduction faster than those with less stable pair bonds, while the stability and the length of time since establishment of the pair bond both reduced the probability of divorcing. Our results demonstrate an important link between the ontogeny of social relationships and reproductive benefits that may explain the evolution of long-term monogamy.

New Insights into the Remarkable Difference between CH5- and SiH5.

It has long been known that there is a fundamental difference in the electronic structures of CH5- and SiH5-, two isoelectronic molecules. The former is a saddle point for the SN2 exchange reaction H- + CH4 → [CH5-]‡ → CH4 + H-, while the latter is a stable molecule that is bound relative to SiH4 + H-. SCGVB calculations indicate that this difference is the result of a dramatic difference in the nature of the axial electron pairs in these anions. In SiH5-, the axial pairs represent two stable bonds-a weak recoupled pair bond dyad. In CH5-, the axial electron pairs represent an intermediate transition between the electron pairs in the reactants and those in the products. Furthermore, the axial orbitals at the saddle point in CH5- are highly overlapping, giving rise to strong Pauli repulsion and a high barrier for the SN2 exchange reaction.

Defending as a unit: sex- and context-specific territorial defence in a duetting bird

Behaviours such as territorial defence represent functionally integrated traits that underlie multiple behavioural variables such as physical and acoustic responses. Characterizing the multivariate structure of such traits is fundamental to understand their evolution. In bird species that form stable pair bonds and are territorial year-round, both sexes are expected to defend their territory; however, the role that each sex plays in defending their shared territory remains largely unknown. Evidence for the sex-roles during territorial defence is mixed and sex- and context-specific characterizations of territorial defence embracing the multivariate nature of the trait are currently lacking. Here, we investigated sex- and context-specific variation in a hypothesised latent variable called ‘territorial defence’ and tested whether duets were part of territorial defence in a wild population of rufous hornero (Furnarius rufus). To do so, we combined a simulated territorial intrusion approach during nest building and provisioning contexts with a structural equation modelling approach. Our results showed that, in males and females, the six measured behavioural variables were linked by a single latent trait, territorial defence, in both contexts. Flights over the decoy and duet songs were equally good proxies of territorial defence. Although males were defending more the territory than females, pair members showed a positive correlation in their behaviour. The structural equation modelling framework enabled us to capture a complex correlation pattern among behavioural variables, expanding upon a classic body of research on territorial defence. Thus, the combination of classical behavioural approaches with sophisticated statistical analyses brings new exciting possibilities to the field of behavioural ecology. Territorial defence is a key behaviour in territorial species as it plays a major role in an individual’s reproductive success and survival. Additionally, territorial defence has been proposed as one possible evolutionary driver of duetting behaviour, one of the most fascinating vocal behaviours in birds. As behaviours are evolutionary characters, they must be studied in a multivariate framework. In this study, we focused on characterizing territorial defence during a simulated territorial intrusion in an integrative manner using a structural equation modelling framework. We did so in male and female rufous horneros (Aves: Furnaridae) across two breeding contexts, while simultaneously testing theoretical predictions about the role of duetting behaviour as key part of territorial defence. Overall, our study provides for the first time a sex- and context-comparison of the multivariate, latent variable ‘territorial defence’ in duetting birds, while highlighting the potential of combining field behavioural approaches with structural equation modelling.

The benefits of pair bond tenure in the cooperatively breeding pied babbler (Turdoides bicolor).

The benefits of stable pair bonds (that persist between breeding attempts) have been well described, but are relatively less well known in cooperatively breeding species. If pair bonds are beneficial, then it is possible that the bond between the behaviorally and socially dominant pair may influence factors such as reproductive success and group stability in cooperative species. Here, we used long‐term data to investigate the relationships between pair bond tenure, reproductive success, and group stability in the cooperatively breeding pied babbler (Turdoides bicolor). Pair bond tenure positively influenced both the number of offspring recruited annually per pair and total reproductive success (over entire pair bond duration), indicating that pair bond tenure has an important influence on reproductive success. The likelihood of immigration into the group was lower for groups containing a bonded pair with long tenure, indicating that the duration of pair bonds may impact group stability. These findings suggest that pair tenure, a hitherto relatively unexplored factor in cooperative species, may have an important influence on group dynamics.

Individual Variation in Social Behaviours of Male Lab-reared Prairie voles (Microtus ochrogaster) is Non-heritable and Weakly Associated with V1aR Density

The genetic and environmental factors that contribute to pair bonding behaviour remain poorly understood. Prairie voles (Microtus ochrogaster) often, but not always, form stable pair bonds and present an ideal model species for investigating the genetic and environmental factors that influence monogamy. Here, we assessed variation in partner preference, a measure of pair bonding, and related social behaviours in a population of laboratory-reared prairie voles under controlled environmental conditions. We evaluated to what extent variation in these behaviours correlate with vasopressin 1a receptor (V1aR) expression in the ventral pallidum (VP) and retrosplenial cortex (RSC), and estimated the heritability of these behaviours and V1aR expression. We found substantial variation in partner preference and measures of aggression, paternal care, and anxiety-like behaviours, but no correlation between these traits. We also found variation in V1aR density in the VP and RSC can account for behavioural components of paternal care and aggression, but not in partner preference. Heritability estimates of variation in partner preference were low, yet heritability estimates for V1aR expression were high, indicating that the extensive variation in partner preference observed within this population is due largely to environmental plasticity.

Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish.

Colonial animals often form stable pair bonds, returning to the same site to breed with the same partner every year. Familiarity with both partner and breeding site has the potential to enhance an individual's reproductive success. However, it is often unknown whether the mating system arises because of site fidelity, mate fidelity or both. Here, observational and experimental studies are used to identify causal links between site fidelity and pair formation in a group-living coral reef cardinalfish, Sphaeramia nematoptera. A long-term field tagging study was undertaken to quantify site and mate attachment. This was followed by both mate removal and mate transplant experiments to test whether the prolonged association with home sites was primarily because of mate or site fidelity. Adult S. nematoptera exhibited a prolonged association with home sites and partners, with some pairs lasting more than 4months at the same site. A Bayesian mixed effect model showed that individuals in pairs were more likely to remain site attached, regardless of sex and maturity. Following mate removal, 78% of S. nematoptera found a new partner within 2weeks on the same site, supporting the hypothesis that individuals primarily exhibit site fidelity. This was confirmed by the partner translocation experiment, with only 1 of 24 fish following their translocated partner to a new site. In these cardinalfish, strong site attachment facilitates long-lasting pair bonds, as well as new pair formation when necessary, suggesting that site rather than mate fidelity is the major driver of the reproductive system.

Adult sex ratio and social status predict mating and parenting strategies in Northern Ireland.

Evidence from animal species indicates that a male-biased adult sex ratio (ASR) can lead to higher levels of male parental investment and that there is heterogeneity in behavioural responses to mate scarcity depending on mate value. In humans, however, there is little consistent evidence of the effect of the ASR on pair-bond stability and parental investment and even less of how it varies by an individual's mate value. In this paper we use detailed census data from Northern Ireland to test the association between the ASR and pair-bond stability and parental investment by social status (education and social class) as a proxy for mate value. We find evidence that female, but not male, cohabitation is associated with the ASR. In female-biased areas women with low education are less likely to be in a stable pair-bond than highly educated women, but in male-biased areas women with the lowest education are as likely to be in a stable pair-bond as their most highly educated peers. For both sexes risk of separation is greater at female-biased sex ratios. Lastly, our data show a weak relationship between parental investment and the ASR that depends on social class. We discuss these results in the light of recent reformulations of parental investment theory.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Sex Differences in Reconciliation Behavior After Romantic Conflict

Prior research shows that patterns of mate selection, attraction, and expulsion are the product of evolved sex differences in computational adaptations. Within long-term romantic relationships, men typically prioritize information relevant to a mate’s reproductive (i.e., sexual) value whereas women more often prioritize a mate’s willingness to invest romantic (i.e., emotional) resources into a stable pair-bond. Although these differences in preference are well established within mate selection and relationship maintenance literature, relatively fewer studies have examined differences in how men and women reconcile after romantic conflict. Using an act nomination procedure, the present research tests the prediction that men and women differ by which partner reconciliation behaviors they evaluate as most effective in resolving a romantic conflict. In study 1, participants nominated common reconciliation behaviors which were subsequently sorted into 21 distinct actions. In study 2, participants rated each behavior by how effectively it would resolve conflict if performed by their romantic partner. Overall, acts suggesting emotional commitment were expected to be rated as most effective. Men were expected to rate actions which signal sexual accessibility as more effective compared to women. Women were expected to rate acts which signal emotional accessibility as more effective compared to men (study 2). Results were largely consistent with our predictions, though notable deviations are documented and discussed within the context of contemporary romantic relationship research.

Allopreening in birds is associated with parental cooperation over offspring care and stable pair bonds across years.

Individuals of many species form bonds with their breeding partners, yet the mechanisms maintaining these bonds are poorly understood. In birds, allopreening is a conspicuous feature of interactions between breeding partners and has been hypothesized to play a role in strengthening and maintaining pair bonds within and across breeding attempts. Many avian species, however, do not allopreen and the relationship between allopreening and pair bonding across species remains unexplored. In a comparative analysis of allopreening and pair bond behavior, we found that allopreening between breeding partners was more common among species where parents cooperate to rear offspring. The occurrence of allopreening was also associated with an increased likelihood that partners would remain together over successive breeding seasons. However, there was no strong evidence for an association between allopreening and sexual fidelity within seasons or time spent together outside the breeding season. Allopreening between partners was also no more common in colonial or cooperatively breeding species than in solitary species. Analyses of evolutionary transitions indicated that allopreening evolved from an ancestral state of either high parental cooperation or high partner retention, and we discuss possible explanations for this. Overall, our results are consistent with an important role for allopreening in the maintenance of avian pair bonds.

Ontogenetic shifts in the social behaviour of pairing coral reef rabbitfishes (Siganidae)

ABSTRACTAdult rabbitfishes (Siganidae) differ from most other herbivorous coral reef fishes by forming stable pair bonds throughout their adult lives. However, little is known about the early life stages of rabbitfishes, and no quantitative evidence regarding the ontogeny of pairing behaviour exists to date. This study describes the abundance, distribution and ontogeny of social associations in juvenile rabbitfishes on the mid-shelf reefs around Lizard Island, Great Barrier Reef, Australia. Using underwater visual censuses, we surveyed an area of 5728 m2 across three distinct habitat types, revealing that the abundance of juveniles varies significantly among species, size class and exposure level. Furthermore, we demonstrate a pronounced ontogenetic shift in the social associations of juveniles of Siganus doliatus and Siganus corallinus, changing from primarily solitary individuals in the smallest size class (<50 mm) to predominantly paired individuals in the larger size classes (50–100 mm and 100–150 mm). In this context, we report the presence of several mixed-species pairs of rabbitfishes, providing the first evidence for this behaviour within the family. This supports previous research, which posits that there are strong ecological drivers, rather than a solely reproductive basis, for pairing behaviour in rabbitfishes. Based on our results, we suggest that further exploration of the ecology of early life stages of herbivorous reef fishes will increase our knowledge about ecological processes on coral reefs.

Generalized Valence Bond Description of Chalcogen-Nitrogen Compounds. III. Why the NO-OH and NS-OH Bonds Are So Different.

Crabtree et al. recently reported the microwave spectrum of nitrosyl-O-hydroxide (trans-NOOH), an isomer of nitrous acid, and found that this molecule has the longest O-O bond ever observed: 1.9149 Å ± 0.0005 Å. This is in marked contrast to the structure of the valence isoelectronic trans-NSOH molecule, which has a normal NS-OH bond length and strength. Generalized valence bond calculations show that the long bond in trans-NOOH is the result of a weak through-pair interaction that singlet couples the spins of the electrons in singly occupied orbitals on the hydroxyl radical and nitrogen atom, an interaction that is enhanced by the intervening lone pair of the oxygen atom in NO. The NS-OH bond is the result of the formation of a stable recoupled pair bond dyad, which accounts for both its length and strength.

Lizard movement tracks: variation in path re-use behaviour is consistent with a scent-marking function.

Individual movement influences the spatial and social structuring of a population. Animals regularly use the same paths to move efficiently to familiar places, or to patrol and mark home ranges. We found that Australian sleepy lizards (Tiliqua rugosa), a monogamous species with stable pair-bonds, repeatedly used the same paths within their home ranges and investigated whether path re-use functions as a scent-marking behaviour, or whether it is influenced by site familiarity. Lizards can leave scent trails on the substrate when moving through the environment and have a well-developed vomeronasal system to detect and respond to those scents. Path re-use would allow sleepy lizards to concentrate scent marks along these well-used trails, advertising their presence. Hypotheses of mate attraction and mating competition predict that sleepy lizard males, which experience greater intra-sexual competition, mark more strongly. Consistent with those hypotheses, males re-used their paths more than females, and lizards that showed pairing behaviour with individuals of the opposite sex re-used paths more than unpaired lizards, particularly among females. Hinterland marking is most economic when home ranges are large and mobility is low, as is the case in the sleepy lizard. Consistent with this strategy, re-used paths were predominantly located in the inner 50% home range areas. Together, our detailed movement analyses suggest that path re-use is a scent marking behaviour in the sleepy lizard. We also investigated but found less support for alternative explanations of path re-use behaviour, such as site familiarity and spatial knowledge. Lizards established the same number of paths, and used them as often, whether they had occupied their home ranges for one or for more years. We discuss our findings in relation to maintenance of the monogamous mating system of this species, and the spatial and social structuring of the population.

The presence of a female influences courtship performance of male manakins

ABSTRACT Coordinated courtship displays are a common feature of species forming long-term pair bonds. In lekking species, on the contrary, there are no stable pair bonds because partners meet only to copulate, and males indicate their quality and/or attractiveness to females by displaying morphological and behavioral traits. In some cases, females interact with these displaying males, but little is known about the role of the females in these encounters. In the Neotropical bearded manakins, females join males in their acrobatic courtship displays in the final phase of mate choice. We hypothesize that females participate in the courtship dance to better assess male motor skill by observing male responses to female signals. We filmed at high speed the courtship displays of 2 species of bearded manakins and compared the displays performed by males alone, where the female is absent from the arena, with those performed together with a female. In addition, we compared the movements of the male with those of the...

Loss of sexual dimorphism is associated with loss of lekking behavior in the green manakin Xenopipo holochora

Manakins (Pipridae) are well know for elaborate male sexual displays and ornate plumage coloration, both of which are thought to have evolved as a consequence of lekking breeding, the prevalent mating system in the family. Less attention has been paid to a handful of ‘drab’ manakin species, in which sexual dimorphism appears to be reduced or absent. Using character reconstruction, we show that these ‘exceptions to the rule’ represent phylogenetically independent cases of losses in sexual dimorphism, and as such could provide a focal group to investigate the link between changes in morphology and in life history (e.g. mating system). We take a first step in this direction by focusing on two subspecies of the putatively monomorphic green manakin Xenopipo holochlora to formally confirm that the species is sexually monomorphic in size and plumage color and test the prediction that sexual monomorphism is associated with the loss of lekking behavior in this species. Our results show that size dimorphism is present but limited in the green manakin, with substantial overlap in male and female morphometric measures, and that sexes are largely monochromatic (including from an avian perspective), despite marked coloration differences between subspecies. Behavioral observations indicate that males do not form leks and do not engage in elaborate sexual displays, that there is no stable pair bond formation, and that females provide parental care alone. These findings are consistent with the idea that changes in mating behavior may have driven changes in morphology in Pipridae, and we encourage similar studies on other drab manakins to better understand this relationship.

Fine-scale genetic assessment of sex-specific dispersal patterns in a multilevel primate society

Like humans, hamadryas baboons (Papio hamadryas) are unusual among primates in having a multilevel social system and stable pair bonds, and are thus a useful model for the evolution of human sociality. While the kinship structure and sex-biased dispersal patterns that underlie human social organization have been extensively elucidated, the impact of these factors on the social system of hamadryas baboons is currently unclear. Here we use genetic analysis of individuals to elucidate the patterns of male and female dispersal across multiple levels of society in a wild population of hamadryas baboons. We characterized 244 members of five hamadryas bands at Filoha, Ethiopia by genotyping one Y-linked and 23 autosomal microsatellite loci and sequencing part of the mitochondrial hypervariable control region I. We found both male and female dispersal to be limited at the level of the band, with more movement of females than males among bands. By integrating long-term behavioral data for Band 1, we also found evidence for male and female philopatry at the clan level. We speculate that male philopatry at the clan level and female dispersal across one-male units and clans may enable both kin-based cooperation among males and the maintenance of kin bonds among females after dispersal. This would mean that, as in humans, kin bonds within both sexes are a core feature of the hamadryas social system, thus contributing to our understanding of the evolution of social organization in humans.

Relationships between pair formation, site fidelity and sex in a coral reef cardinalfish

Coral reef fishes are characterised by extreme site fidelity and are often socially monogamous, forming pair bonds within larger social groups. Despite this, the strong link between reproductive behaviour and site fidelity in such social species is poorly understood. We examine these relationships in the cardinalfish Ostorhinchus cyanosoma on the central Great Barrier Reef. We tagged and followed over 100 individuals for 5 weeks to investigate pair fidelity, and behavioural differences between pairs and singles and between sexes, and we experimentally tested the strength of site and mate fidelity. Tagged pairs were typically highly site attached, and lasted throughout the study period. Sex had very little effect on pairing behaviour or habitat use. Paired individuals showed three times higher site fidelity than single ones, with singles frequently relocating. There was a two-fold increase in the movement of individuals that had their partners experimentally removed. Paired individuals exhibited greater homing success, and homed regardless of whether their mate had been displaced with them or was left on the home site. These results suggest that individuals of this species form at least seasonally stable monogamous pair bonds within larger groups, and that pair formation is closely associated with site fidelity.

Early conditions and fitness: effect of maternal parity on human life-history traits

Stable pair bonds are widespread in humans and reproductive success varies greatly among pairs. Determinants of fitness may be based on testosterone-dependent sexually dimorphic traits. Prenatal condition is a critical period of physical development, and fetal testosterone has a profound effect on adult behavior and reproduction. Maternal parity (the number of previous births) might be a proxy for fetal testosterone because the prenatal level of male sex hormone, testosterone, is previously shown to decrease across parities. Offspring reproductive potential may, therefore, be positively associated with low parity in sons and high in daughters, by different masculinization by testosterone. In this study, we explored the effects of maternal parity on offspring’s subsequent (individual and pair-specific) life histories including number of grandchildren (controlling for age at marriage, number of siblings, social status, and year of birth) in a Norwegian preindustrial society. We found that parity was a positive predictor of daughters’ and negative (but not significantly; P = 0.058) predictor of sons’ subsequent fitness. Furthermore, within the mated pairs, the difference between the parity of their 2 mothers was a strong predictor of each couple’s fitness. Sons born to mothers of low parity married to daughters from mothers with high parity had much higher number of grandchildren than, for example, sons of mothers with high parity married to daughters of mothers with low parity. The result highlights the importance of early prenatal condition on human life histories, particularly pair-bond duration and fitness, and that parity may have an impact on offspring pair-specific fitness in the studied population.

Nomascus leucogenys (Primates: Hylobatidae)

Abstract: Nomascus leucogenys (Ogilby, 1840) is a crested gibbon of northern Vietnam, northern Laos, and southern China. Males are black with white cheeks and females are a rich buff color with a dark brown sagittal crest. It is among the largest of hylobatids (except siamang) and has unusually long arms for a hylobatid. Its diet includes fruits, leaves, small animals, and flowers. It is territorial and lives with stable pair-bonds in nuclear families consisting of a male and female and their offspring. It is “Critically Endangered,” possibly extirpated from China with only isolated populations remaining in Laos and Vietnam.

The impact of sexually abstaining groups on persistence of sexually transmitted infections in populations with ephemeral pair bonds

Individuals often stop reproducing some time before they die. In this paper we compose and analyze a logistic two-sex population model in which individuals form pairs just to mate (i.e. pair bonds are ephemeral) and later move on to sexually abstaining groups. Using this model, we study the impact of sexually abstaining groups on persistence of a benign sexually transmitted infection (STI) in populations with such ephemeral pair bonds. We observe that the presence of sexually abstaining groups cannot prevent an STI from invasion or eliminate it when already present if the transition rates to the sexually abstaining groups are independent of the infection status of individuals (susceptible or infected). On the other hand, if they depend on that status, the presence of sexually abstaining groups can prevent an STI from invasion or eliminate it when present. Specifically, in the simple case of sex-independent vital parameters, this happens if the transition rate of the infected individuals to the sexually abstaining group is higher than the transition rate of the susceptible ones. These results contrast the earlier results based on assuming long-term, stable pair bonds, in which case one is capable of preventing or eliminating the disease with the same isolation rate for the susceptible and infected individuals.