PHYLOGENETIC ANALYSIS OF THE EVOLUTION OF ALTERNATIVE SOCIAL BEHAVIOR IN THE MANAKINS (AVES: PIPRIDAE)

Phylogenetic analyses of lekking, lek spatial organization, and cooperative and coordinated lek display in the manakins (Aves: Pipridae) demonstrate that variation in social behavior in the group has a strong, phylogenetic component. Two of the three classes of social behavior examined also show significant phylogenetic constraints. Current adaptive plasticity models are insufficient to explain the phylogenetic variation in these behaviors in the manakins. These findings support the conclusion that vertebrate reproductive social behavior has an evolutionary history, and that it is not determined solely by adaptive individual plasticity to current conditions. The evolution of social behavior, particularly through sexual selection, can have historical consequences that can limit subsequent behavioral adaptation.     

Characteristics of the social life of bonnet macaques (Macaca radiata)

The social behavior of wild bonnet macaques impresses upon us a peculiality and uniqueness which is different from other macaques. Although there is a clear-cut ranking relationship among adult males and they carry out their proper social roles according to each situation, many social behaviors are carried out independently of or ignoring the ranking order. The animals are organized in a flexible and tolerant social unit, but they don't abandon the advantages of group life.The uniqueness of bonnet behavior and society is recognized to be related to the highly developed individuality of this species.     

Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors

The early-life social environment has profound effects on brain development and subsequent expression of social behavior. Oxytocin and vasopressin are expressed and released in the brain and are important regulators of social behavior. Accordingly, the early social environment may alter social behaviors via changes in the oxytocin and/or vasopressin systems. To test this hypothesis, and to gain mechanistic insights, rodent models mimicking either a deprived (e.g. maternal separation) or enriched (e.g. neonatal handling) early social environment have been utilized. Findings indeed show that differences in the quality of the early social environment are associated with brain region-specific alterations in oxytocin and vasopressin expression and oxytocin receptor and vasopressin 1a receptor binding. Early social environment-induced changes in oxytocin and vasopressin systems were associated with changes in several forms of social behavior, including maternal care, aggression, play-fighting, and social recognition. First studies provide evidence for a causal link between altered vasopressin responsiveness and impairments in social recognition in rats exposed to maternal separation and a role for epigenetic mechanisms to explain persistent increases in vasopressin expression in mice exposed to maternal separation. Overall, initial findings suggest that oxytocin and vasopressin systems may mediate early social environment-induced alterations in social behavior. Additional comprehensive studies will be necessary to advance our understanding to what extent changes in oxytocin and vasopressin underlie early social environment-induced alterations in social behavior. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Social behavior adaptations of gibbon (Hylobates lar) in a controlled environment

A population of six adolescent—adult gibbons (three males and three females) were observed in a controlled environment in order to assess any social behavior adaptations related to forced aggregation and to a physical environment which differed from the native habitat in that there were no predators, no food scarcity and the geographic range was limited to 1.5 acres. Data on location, size and composition of naturally formed social groupings revealed that certain gibbons avoided social contact with certain others. This observation is discussed in relation toChance's (1967) concept of “attention structure.” It is viewed as representative of a dominance hierarchy serving gibbons as a social behavior adaptation when forced to aggregate.     

Neuropeptides and the evolution of social behavior

Comparative studies over the past year have revealed two new insights into the role of neuropeptides in the evolution of social behaviors. First, across vertebrate taxa, certain neuropeptide effects appear to be gender-specific. Second, species variations in receptor gene structure can alter neuropeptide receptor distribution and thereby contribute to species differences in social behavior.     

Network analysis as a tool to understand social development in spider monkeys

The emerging field of network science has demonstrated that an individual's connectedness within their social network has cascading effects to other dimensions of life. Like humans, spider monkeys live in societies with high fission–fusion dynamics, and are remarkably social. Social network analysis (SNA) is a powerful tool for quantifying connections that may vary as a function of initiating or receiving social behaviors, which has been described as shifting social roles. In primatology, the SNA literature is dominated by work in catarrhines, and has yet to be applied to the study of development in a platyrrhine model. Here, SNA was utilized in combination with R-Index social role calculation to characterize social interaction patterns in juvenile and adult Colombian spider monkeys (Ateles fusciceps rufiventris). Connections were examined across five behaviors: embrace, face-embrace, grooming, agonism, and tail-wrapping from 186 hr of observation and four network metrics. Mann–Whitney U tests were utilized to determine differences between adult and juvenile social network patterns for each behavior. Face-embrace emerged as the behavior with different network patterns for adults and juveniles for every network metric. With regard to social role, juveniles were receivers, not initiators, for embrace, face-embrace, and grooming (ps < .05). Network and social role differences are discussed in light of social development and aspects of the different behaviors.     

Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism

Current theory recognizes the adaptive value of maternal effects in shaping offspring phenotypes in response to selective pressures and vindicates the value of these traits in fostering adaptation and speciation. Yolk androgens in birds are a relatively well-known maternal effect and have been linked to adaptations related to development, coloniality life, and sexual selection. We tested whether interspecific patterns of yolk androgen levels (androstenedione and testosterone) were related to interspecific variation in development, sexual selection, and coloniality. First, we found no relationship between androgen levels and duration of development as reflected by incubation and nestling periods. However, androstenedione concentration was positively related to the relative duration of the incubation period and negatively related to the relative duration of the nestling period. These relationships were confirmed by analyses of phylogenetically independent contrasts. We suggest that androstenedione concentration may have evolved as a mechanism to shift the relative duration of development between the egg and nestling stages in response to selective pressures that differentially affect the duration of each stage. Second, neither plumage dichromatism nor mating system explained significant variation in yolk androgen levels after correction for similarity among species due to common descent. This finding indicates that sexual selection has not been an important selective pressure for this maternal effect. Third, we found a highly significant positive relationship between degree of breeding coloniality and concentration of androstenedione but not testosterone. These effects were confirmed in analyses of contrasts controlling for similarity due to common descent. Since the relationship with coloniality was different for each androgen, it is unlikely that increased levels of androgens in highly colonial species are a mere consequence of elevated androgen levels in mothers. Rather, our results suggest that high levels of androstenedione in eggs of colonial species are an adaptation to colony life, possibly related to the production of highly competitive phenotypes. In conclusion, from a comparative perspective, the results of this study support the role of maternal effects in promoting adaptation to certain environmental pressures.     

Postpartum depression: Etiology,treatment and consequences for maternal care

This article is part of a Special Issue “Parental Care”. Pregnancy and postpartum are associated with dramatic alterations in steroid and peptide hormones which alter the mothers' hypothalamic pituitary adrenal (HPA) and hypothalamic pituitary gonadal (HPG) axes. Dysregulations in these endocrine axes are related to mood disorders and as such it should not come as a major surprise that pregnancy and the postpartum period can have profound effects on maternal mood. Indeed, pregnancy and postpartum are associated with an increased risk for developing depressive symptoms in women. Postpartum depression affects approximately 10–15% of women and impairs mother–infant interactions that in turn are important for child development. Maternal attachment, sensitivity and parenting style are essential for a healthy maturation of an infant's social, cognitive and behavioral skills and depressed mothers often display less attachment, sensitivity and more harsh or disrupted parenting behaviors, which may contribute to reports of adverse child outcomes in children of depressed mothers. Here we review, in honor of the “father of motherhood”, Jay Rosenblatt, the literature on postnatal depression in the mother and its effect on mother–infant interactions. We will cover clinical and pre-clinical findings highlighting putative neurobiological mechanisms underlying postpartum depression and how they relate to maternal behaviors and infant outcome. We also review animal models that investigate the neurobiology of maternal mood and disrupted maternal care. In particular, we discuss the implications of endogenous and exogenous manipulations of glucocorticoids on maternal care and mood. Lastly we discuss interventions during gestation and postpartum that may improve maternal symptoms and behavior and thus may alter developmental outcome of the offspring.     

Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin

The maternal brain undergoes remarkable physiological and behavioral changes in the peripartum period to meet the demands of the offspring. Here, the brain neuropeptides oxytocin and vasopressin, together with prolactin, play important roles. These neuropeptides are critically involved in the regulation of maternal behavior. Furthermore, reduced anxiety in lactation is another adaptation of the maternal brain. Therefore, a link between maternal behavior and maternal anxiety has been repeatedly postulated. This is supported by our studies in rats bred for high (HAB) and low (LAB) anxiety-related behavior. While female HAB rats become less anxious in lactation, their anxiety level is still four times higher compared with LAB dams. Interestingly, HAB dams display an intense and protective mothering style including increased arched back nursing and pup retrieval whereas LAB dams display only low levels of maternal care. The amount of maternal care directed towards the pups correlates with the mother's innate anxiety. In addition to differences in maternal care, HAB dams are also more protective as they show heightened aggression against a virgin intruder compared with the less aggressive LAB dams. The level of maternal aggression correlates with both their innate anxiety level as well as with the release of oxytocin and vasopressin in hypothalamic and limbic brain areas. Importantly, manipulations of the brain oxytocin and vasopressin systems alter maternal behavior and — depending on the brain region — can also alter the dam's anxiety. Thus, the mother's innate anxiety determines her maternal performance and oxytocin and vasopressin are involved in both parameters.     

The origins of music in auditory scene analysis and the roles of evolution and culture in musical creation

Whether music was an evolutionary adaptation that conferred survival advantages or a cultural creation has generated much debate. Consistent with an evolutionary hypothesis, music is unique to humans, emerges early in development and is universal across societies. However, the adaptive benefit of music is far from obvious. Music is highly flexible, generative and changes rapidly over time, consistent with a cultural creation hypothesis. In this paper, it is proposed that much of musical pitch and timing structure adapted to preexisting features of auditory processing that evolved for auditory scene analysis (ASA). Thus, music may have emerged initially as a cultural creation made possible by preexisting adaptations for ASA. However, some aspects of music, such as its emotional and social power, may have subsequently proved beneficial for survival and led to adaptations that enhanced musical behaviour. Ontogenetic and phylogenetic evidence is considered in this regard. In particular, enhanced auditory–motor pathways in humans that enable movement entrainment to music and consequent increases in social cohesion, and pathways enabling music to affect reward centres in the brain should be investigated as possible musical adaptations. It is concluded that the origins of music are complex and probably involved exaptation, cultural creation and evolutionary adaptation.     

Conservatism and Adaptability during Squirrel Radiation: What Is Mandible Shape Telling Us?

Both functional adaptation and phylogeny shape the morphology of taxa within clades. Herein we explore these two factors in an integrated way by analyzing shape and size variation in the mandible of extant squirrels using landmark-based geometric morphometrics in combination with a comparative phylogenetic analysis. Dietary specialization and locomotion were found to be reliable predictors of mandible shape, with the prediction by locomotion probably reflecting the underlying diet. In addition a weak but significant allometric effect could be demonstrated. Our results found a strong phylogenetic signal in the family as a whole as well as in the main clades, which is in agreement with the general notion of squirrels being a conservative group. This fact does not preclude functional explanations for mandible shape, but rather indicates that ancient adaptations kept a prominent role, with most genera having diverged little from their ancestral clade morphologies. Nevertheless, certain groups have evolved conspicuous adaptations that allow them to specialize on unique dietary resources. Such adaptations mostly occurred in the Callosciurinae and probably reflect their radiation into the numerous ecological niches of the tropical and subtropical forests of Southeastern Asia. Our dietary reconstruction for the oldest known fossil squirrels (Eocene, 36 million years ago) show a specialization on nuts and seeds, implying that the development from protrogomorphous to sciuromorphous skulls was not necessarily related to a change in diet.     

Quantitative analysis of small group interaction in rhesus monkeys

The effect of role relations on social interaction in small groups of rhesus monkeys was examined quantitatively, through use of an interval scale of social behavior. Concurrent pair interactions were tabulated for all possible combinations in 24 triad groups: Six groups containing three males; six groups containing three females; six groups of one male, two females; and six groups of two males and one female. A specific behavior which involves participation of all three animals at once, the incitement interaction, was found to quantitatively alter each monkey's reaction to other social behaviors displayed at the same time. The interaction demonstrates the monkeys' attention to and manipulation of role relations. In all triad types one could quantitatively document the fact that the most subordinate monkey established a role with the most dominant monkey which allowed it some freedom to behave less submissively when interacting with the middle ranking monkey. This general phenomenon in role relations may contribute to group cohesiveness.     

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in S?o Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piauí state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus.     

Peripherally administered non-peptide oxytocin antagonist, L368,899, accumulates in limbic brain areas: a new pharmacological tool for the study of social motivation in non-human primates

Central administration of oxytocin (OT) antagonists inhibits maternal and sexual behavior in non-primates, providing the strongest experimental evidence that endogenous OT facilitates these behaviors. While there have been a few reports that ICV administration of OT increases social behaviors in monkeys, no studies to date have assessed the effects of OT antagonists. Therefore, we studied in rhesus monkeys whether L368,899, a non-peptide antagonist produced by Merck that selectively blocks the human uterine OT receptor, penetrates the CNS after peripheral administration and alters female maternal and sexual behavior. In two studies in four male monkeys, L368,899 was injected iv (1 mg/kg) after which (1) CSF samples were collected at intervals over 4 h and (2) brains were collected at 60 min. Assay of samples confirmed that iv-administered L368,899 entered CSF and accumulated in the hypothalamus, septum, orbitofrontal cortex, amygdala and hippocampus, but not other areas. An adult female monkey was tested for interest in either an infant or sexual behavior, receiving a different iv treatment prior to each test (1 or 3 mg/kg of L368,899 or saline). OT antagonist treatment reduced or eliminated interest in the infant and sexual behavior. These results, although preliminary, are the first to directly implicate endogenous OT in activation of primate maternal interest and sexual behavior. While it remains to be empirically demonstrated that peripherally administered L368,899 blocks central OT receptors, our behavioral findings suggest that this non-peptide antagonist may facilitate testing OT involvement in a variety of social and other behaviors in primates.     

Ontogenic development of dyadic social relationships: Assessing individual roles

Socialization processes lead to creation and differentiation of social relationships. It is often difficult to qualify them, especially due to ontogenic changes of social behavior. In this paper, an attempt is made to assess the role of each partner in a dyad by defining the quality of their overall relationship. A Social Investment Index (SII) was devised to describe these roles throughout ontogeny. SII is expressed as (G% — R%)/2, where G% and R% represent the difference between the sum of cohesive behaviors and that of disruptive behaviors divided by the overall sum of these behaviors given (G%) or received (R%) by one individual in a dyad. Results from a longitudinal study of the development of social behavior in one infant mangabey (Cercocebus albigena albigena) are used as an example. The developmental changes of the SII are presented in three dyads in a single-male group: mother-infant; “aunt”-infant; and juvenile male-infant.     

Endocrine and neuroendocrine regulation of fathering behavior in birds

This article is part of a Special Issue "Parental Care".Although paternal care is generally rare among vertebrates, care of eggs and young by male birds is extremely common and may take on a variety of forms across species. Thus, birds provide ample opportunities for investigating both the evolution of and the proximate mechanisms underpinning diverse aspects of fathering behavior. However, significant gaps remain in our understanding of the endocrine and neuroendocrine influences on paternal care in this vertebrate group. In this review, I focus on proximate mechanisms of paternal care in birds. I place an emphasis on specific hormones that vary predictably and/or unpredictably during the parental phase in both captive and wild birds: prolactin and progesterone are generally assumed to enhance paternal care, whereas testosterone and corticosterone are commonly—though not always correctly—assumed to inhibit paternal care. In addition, because endocrine secretions are not the sole mechanistic influence on paternal behavior, I also explore potential roles for certain neuropeptide systems (specifically the oxytocin–vasopressin nonapeptides and gonadotropin inhibitory hormone) and social and experiential factors in influencing paternal behavior in birds. Ultimately, mechanistic control of fathering behavior in birds is complex, and I suggest specific avenues for future research with the goal of narrowing gaps in our understanding of this complexity. Such avenues include (1) experimental studies that carefully consider not only endocrine and neuroendocrine mechanisms of paternal behavior, but also the ecology, phylogenetic history, and social context of focal species; (2) investigations that focus on individual variation in both hormonal and behavioral responses during the parental phase; (3) studies that investigate mechanisms of maternal and paternal care independently, rather than assuming that the mechanistic foundations of care are similar between the sexes; (4) expansion of work on interactions of the neuroendocrine system and fathering behavior to a wider array of paternal behaviors and taxa (e.g., currently, studies of the interactions of testosterone and paternal care largely focus on songbirds, whereas studies of the interactions of corticosterone, prolactin, and paternal care in times of stress focus primarily on seabirds); and (5) more deliberate study of exceptions to commonly held assumptions about hormone–paternal behavior interactions (such as the prevailing assumptions that elevations in androgens and glucocorticoids are universally disruptive to paternal care). Ultimately, investigations that take an intentionally integrative approach to understanding the social, evolutionary, and physiological influences on fathering behavior will make great strides toward refining our understanding of the complex nature by which paternal behavior in birds is regulated.     

Intercorrelations of maternal and infant behaviors inMacaca mulatta

Matrices of correlation coefficients among 38 behaviors of 32 mother-infant pairs are presented as an aid to future investigations involving experimental manipulations of the development of maternal and infant behaviors in the rhesus monkey. Such matrices are particularly useful when employed in the construction of social behavior scoring systems.     

Evidence for the functions of surface‐active behaviors in humpback whales (Megaptera novaeangliae)

As part of their social sound repertoire, migrating humpback whales (Megaptera novaeangliae) perform a large variety of surface‐active behaviors, such as breaching and repetitive slapping of the pectoral fins and tail flukes; however, little is known about what factors influence these behaviors and what their functions might be. We investigated the potential functions of surface‐active behaviors in humpback whale groups by examining the social and environmental contexts in which they occurred. Focal observations on 94 different groups of whales were collected in conjunction with continuous acoustic monitoring, and data on the social and environmental context of each group. We propose that breaching may play a role in communication between distant groups as the probability of observing this behavior decreased significantly when the nearest whale group was within 4,000 m compared to beyond 4,000 m. Involvement in group interactions, such as the splitting of a group or a group joining with other whales, was an important factor in predicting the occurrence of pectoral, fluke, and peduncle slapping, and we suggest that they play a role in close‐range or within‐group communication. This study highlights the potentially important and diverse roles of surface‐active behaviors in the communication of migrating humpback whales.