Future social rank: forecasting status in the green anole (Anolis carolinensis)

Predicting the future social standing of an individual without aggressive social interaction may seem contradictory, as formation of social rank depends on agonistic interactions. In the lizard Anolis carolinensis, predicting social rank is possible using latency to eyespot formation (sympathetic darkening of postorbital skin from green to black during stressful agonistic interactions), because they form more rapidly in male lizards that become dominant. Darkened eyespots also inhibit aggressive behavior. As the timing of eyespot formation appears to be an important component of stress responsiveness and future social status, we hypothesized that a proactive disposition toward non-aggressive behavior, such as feeding and courtship, would be associated with aggressiveness. We assessed the relationship between rank and the temporal dynamics of eyespot formation, latencies to aggressive display, feeding, and reproductive behavior. Male lizards that became dominant were faster to respond to all types of stimuli tested (aggression, feeding, and courtship). The temporal dynamics of the neuroendocrine stress response appear to influence the motivation for behavioral response. Animals that recover from stress more quickly also eat, court, and fight more readily. In summary, this work suggests that latencies to aggressive, reproductive, and feeding behavior, as well as eyespot signals, are reliable predictors of future social status of individual male A. carolinensis.     

Visible sympathetic activity as a social signal in Anolis carolinensis: changes in aggression and plasma catecholamines

Darkening of postorbital skin in Anolis carolinensis occurs during stressful situations and is stimulated by sympathetic activation of beta(2)-adrenergic receptors via adrenal catecholamines. This eyespot forms more rapidly in dominant males during social interaction. Eyespot darkening (green to black) appears to function as a social signal communicating sympathetic activation and limiting aggressive interaction. To assess the value of the eyespot as a social signal, males were painted postorbitally with green, black, or red paint. Each male was exposed to a mirror following acclimation to the cage. The total number of aggressive displays toward the mirror image was greatest when eyespots were masked by green paint. In contrast, black or red artificial eyespots, regardless of size, inhibited biting behavior toward the mirror image. The most aggressive males, those who saw a reflected opponent with no eyespot (hidden with green paint), had significantly higher levels of all plasma catecholamines. These results suggest that A. carolinensis use information from the eyespot to assess their opponent's readiness to fight and thereby determine whether to be aggressive. Darkened eyespots are capable of inhibiting aggression, whereas aggressive displays from an opponent in the mirror without darkened eyespots do not. Darkened eyespots reflect rapid changes in plasma NE, DA, and Epi that may signal dominant social status.     

Does serotonin influence aggression? comparing regional activity before and during social interaction

Serotonin is widely believed to exert inhibitory control over aggressive behavior and intent. In addition, a number of studies of fish, reptiles, and mammals, including the lizard Anolis carolinensis, have demonstrated that serotonergic activity is stimulated by aggressive social interaction in both dominant and subordinate males. As serotonergic activity does not appear to inhibit agonistic behavior during combative social interaction, we investigated the possibility that the negative correlation between serotonergic activity and aggression exists before aggressive behavior begins. To do this, putatively dominant and more aggressive males were determined by their speed overcoming stress (latency to feeding after capture) and their celerity to court females. Serotonergic activities before aggression are differentiated by social rank in a region-specific manner. Among aggressive males baseline serotonergic activity is lower in the septum, nucleus accumbens, striatum, medial amygdala, anterior hypothalamus, raphe, and locus ceruleus but not in the hippocampus, lateral amygdala, preoptic area, substantia nigra, or ventral tegmental area. However, in regions such as the nucleus accumbens, where low serotonergic activity may help promote aggression, agonistic behavior also stimulates the greatest rise in serotonergic activity among the most aggressive males, most likely as a result of the stress associated with social interaction.     

Dynamics and mechanics of social rank reversal

Stable social relationships are rearranged over time as resources such as favored territorial positions change. We test the hypotheses that social rank relationships are relatively stable, and although social signals influence aggression and rank, they are not as important as memory of an opponent. In addition, we hypothesize that eyespots, aggression and corticosterone influence serotonin and N-methyl-D-aspartate (NMDA) systems in limbic structures involved in learning and memory. In stable adult dominant-subordinate relationships in the lizard Anolis carolinensis, social rank can be reversed by pharmacological elevation of limbic serotonergic activity. Any pair of specific experiences: behaving aggressively, viewing aggression or perceiving sign stimuli indicative of dominant rank also elevate serotonergic activity. Differences in the extent of serotonergic activation may be a discriminating and consolidating factor in attaining superior rank. For instance, socially aggressive encounters lead to increases in plasma corticosterone that stimulate both serotonergic activity and expression of the NMDA receptor subunit 2B (NR_2B) within the CA₃ region of the lizard hippocampus. Integration of these systems will regulate opponent recognition and memory, motivation to attack or retreat, and behavioral and physiological reactions to stressful social interactions. Contextually appropriate social responses provide a modifiable basis for coping with the flexibility of social relationships.     

Behavioral coping strategies in a cichlid fish: the role of social status and acute stress response in direct and displaced aggression

The African cichlid fish, Astatotilapia burtoni, has a complex social system with a sophisticated social hierarchy that offers unique opportunities to understand how social rank and its physiological substrates relate to behavioral strategies. In A. burtoni, a small fraction of the males are dominant (T, territorial), as distinguished by being large, brightly colored, reproductively active, and aggressively defending territories. In contrast, the majority of males are non-dominant (NT, non-territorial), being smaller, drably colored, sexually immature, and typically schooling with females. The social system is regulated by aggressive interactions between males and behavioral responses to aggression can be direct or displaced with respect to the animal that acts. To determine whether direct and displaced behaviors are differentially exhibited by T and NT males, individuals were shown a video presentation of a dominant male displaying aggressively. Analysis of aggressive acts toward the video display and displaced activity toward a tank mate revealed that T males exhibited more direct behavior (toward the video display), while NT males engaged in more displaced behavior (toward tank mates). Because similar experiments with primates suggest that shifts in behavioral strategies are linked to changes in the stress response (as measured by circulating cortisol levels), we measured cortisol levels of T and NT males following exposure to the aggressive stimulus. Although in some animals subordinate males are reported to have higher cortisol levels, here we show that in A. burtoni the endocrine response to specific situations can vary considerably even among animals of the same status. Interestingly, NT males with intermediate cortisol levels showed more directed behavior while NT males with both high and low cortisol levels showed more displaced. This suggests an optimal physiological stress response in NT males that predisposes them to challenge aggressors perhaps making it more likely for them to ascend in status.     

The role of substance P in stress and anxiety responses

Summary. Substance P (SP) is one of the most abundant peptides in the central nervous system and has been implicated in a variety of physiological and pathophysiological processes including stress regulation, as well as affective and anxiety-related behaviour. Consistent with these functions, SP and its preferred neurokinin 1 (NK1) receptor has been found within brain areas known to be involved in the regulation of stress and anxiety responses. Aversive and stressful stimuli have been shown repeatedly to change SP brain tissue content, as well as NK1 receptor binding. More recently it has been demonstrated that emotional stressors increase SP efflux in specific limbic structures such as amygdala and septum and that the magnitude of this effect depends on the severity of the stressor. Depending on the brain area, an increase in intracerebral SP concentration (mimicked by SP microinjection) produces mainly anxiogenic-like responses in various behavioural tasks. Based on findings that SP transmission is stimulated under stressful or anxiety-provoking situations it was hypothesised that blockade of NK1 receptors may attenuate stress responses and exert anxiolytic-like effects. Preclinical and clinical studies have found evidence in favour of such an assumption. The status of this research is reviewed here.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

The endocrine stress-response and social status in the wild baboon

The relationship between social status and the testosterone and cortisol stress responses was studied in male olive baboons living in their natural environment in Kenya. (1) A variety of measures of social status are correlated with each other but are not correlated with aggressiveness or frequency of fighting. (2) Aggressiveness is positively correlated with high testosterone titers. (3) In contrast, copulatory success is not correlated with testosterone titer. Instead, it is associated with the change of testosterone levels with time; successful males increase testosterone titers in response to stress while subordinates show declines. (4) Finally, those same males with high rates of copulation showed the lowest initial cortisol levels but showed relatively faster and greater cortisol elevations following stress.     

Social status does not predict corticosteroid levels in postdispersal male spotted hyenas

In social species with low rates of direct male competition levels of corticosteroids should not correlate with social status. Male spotted hyenas acquire social status by observing strict queuing conventions over many years, and thus levels of male-male aggression are low, and male social status and tenure are closely correlated. In this study, we investigated whether the low rate of direct male competition in spotted hyenas was reflected in fecal corticosteroid levels of adult males in the Serengeti National Park. Also, interactions with dominant females may influence corticosteroid levels of males, and it has been suggested recently that males with a long tenure (high rank) are more stressed by females than males with a short tenure (low rank). We tested whether there is a difference in the likelihood of being aggressively challenged by dominant females between long-tenured and short-tenured males. Short-tenured males were more likely to elicit an aggressive response by females than long-tenured males, but previous work suggests that they also interacted less frequently with females, thus avoiding putting themselves in a potentially stressful situation. Thus, as expected, the comparison of males in three different clans revealed no correlation between social status or tenure and fecal corticosteroid levels. However, males of the largest clan had the highest levels of fecal corticosteroids, possibly reflecting higher rates of social interactions in larger clans.     

Social status,immune response and parasitism in males: a meta-analysis

In male vertebrates, two conflicting paradigms—the energetic costs of high dominance rank and the chronic stress of low rank—have been proposed to explain patterns of immune function and parasitism. To date, neither paradigm has provided a complete explanation for status-related differences in male health. Here, we applied meta-analyses to test for correlations between male social status, immune responses and parasitism. We used an ecoimmunological framework, which proposes that males should re-allocate investment in different immune components depending on the costs of dominance or subordination. Spanning 297 analyses, from 77 studies on several vertebrate taxa, we found that most immune responses were similar between subordinate and dominant males, and neither dominant nor subordinate males consistently invested in predictable immune components. However, subordinate males displayed significantly lower delayed-type hypersensitivity and higher levels of some inflammatory cytokines than dominant males, while dominant males exhibited relatively lower immunoglobulin responses than subordinate males. Despite few differences in immunity, dominant males exhibited consistently higher parasitism than subordinate males, including protozoan blood parasites, ectoparasites and gastrointestinal helminths. We discuss our results in the context of the costs of dominance and subordination and advocate future work that measures both parasitism and immune responses in wild systems.     

Sperm competition within a dominance hierarchy: investment in social status vs. investment in ejaculates

There is increasing recognition that male-male competition can take many forms, but as yet the form is not predictable a priori. Many recent studies have focused attention on how males in disadvantaged mating roles compensate through sperm competition. However, mating systems in which subordinate males are reproductively suppressed, particularly through the stress of social interactions, may limit the ability of males to respond by increasing investment in sperm quality. We examined the interaction between social status and ejaculate tactics in Nauphoeta cinerea, a cockroach that has a mating system with well-characterized dominance hierarchies. Both social experience with other males and social status influenced aspects of ejaculates. The stress of social interactions reduced the size of the ejaculate and number of sperm inseminated. In ejaculates formed prior to social experience, however, males that go on to become dominant inseminated more sperm than males that go on to become subordinate, suggesting innate differences among males. Our results show that though selection for increased success in sperm competition for subordinate males in a hierarchy can occur, both the traits and the way in which the balance between pre- and post-copulatory strategies is negotiated will depend on specific details of the mating system. These details will include how the physiological effects of social interactions may limit selection through male-male competition.     

Social status,behavior, and central serotonergic responsivity in female cynomolgus monkeys

The relationship between social status, behavioral characteristics, and central serotonergic function was examined in eight adult female cynomolgus monkeys (Macaca fascicularis). The subjects were housed in four-member social groups for 6 months. Social behavior was observed three times a week. The early follicular phase of the menstrual cycle was determined based on the occurrence of menses, and the prolactin response to acute administration of fenfluramine HCl during the early follicular phase was used as a measure of net brain serotonergic responsivity. Delta prolactin responses (the prolactin response to fenfluramine minus baseline concentrations) were lower in dominant than in subordinate females. Dominant females were more aggressive and less submissive than subordinates. Likewise, females with the lowest delta prolactin concentrations were more aggressive and less submissive than females that had relatively large increases in prolactin. Delta prolactin responses also correlated negatively with percent time eating and investigating in close proximity to penmates, and correlated positively with percent time scanning anxiously while alone. The same pattern of correlation was noted between social status and the aforementioned affiliative behaviors. It was concluded that high central serotonergic responsivity may be associated with low rates of aggression, high rates of submission, and subordinate social status in female cynomolgus monkeys. © 1995 Wiley-Liss, Inc.     

The correlation between subordinate fish eye colour and received attacks: a negative social feedback mechanism for the reduction of aggression during the formation of dominance hierarchies

Eye darkening has been linked to social status in fish. The subordinate's eyes darken, while the eyes of the dominant fish become pale. Although this phenomenon has been described in salmonid fishes and in the African cichlid Nile tilapia Oreochromis niloticus, it is unclear whether eye darkening correlates with a reduction in aggressive behaviour. Thus, we evaluated the link between social status and eye darkening. We evaluated whether the eye colours of subordinate fish correlate with the frequency of received attacks in a neotropical fish, the pearl cichlid Geophagus brasiliensis. We paired pearl cichlids and quantified both the aggressive behaviour and the eye darkening of each fish. As has been described for Nile tilapia and Atlantic salmon, a clear-cut hierarchical relationship formed, where dominance and subordination were associated with pale and dark eye colours, respectively. Initially, eye colour darkening was positively correlated with the frequency of received attacks; however, a negative association occurred following eye darkening, in which the intensity of aggressive interactions decreased. Thus, fish that initially received a high number of attacks signalled subordination more rapidly and intensely (rapid and dramatic eye darkening), thereby inducing a negative social feedback mechanism that led to reduced aggression.     

Effects of Dominant/Subordinate Social Status on Formalin-Induced Pain and Changes in Serum Proinflammatory Cytokine Concentrations in Mice

Current investigations regarding social stress primarily focus on the health consequences of being in stressful social hierarchies. The repetitive nature of social conflicts seems to favor an induction of hyperalgesia or hypoalgesia, both in rodents and humans. Additionally, social conflicts may affect the immune system. In order to better establish the pain and immune responses to stress, the present study implemented a sensory contact model on 32 male BALB/c mice. Subsequent to establishing a dominance/submissive social relationship, each mouse was injected with formalin (20 μl, 2%) and their pain behavior was scored and serum concentrations of proinflammatory cytokines IL-1 and IL-6, and corticosterone were also measured. Test results revealed that subordinate mice were hypoalgesic during chronic phase of formalin test compared to control and dominant mice (P<0.05). On the other hand, subordinate mice were hyperalgesic compared to dominant mice during the whole acute phase of formalin test (P<0.05). Corticosterone, IL-1 and IL-6 concentrations were much higher in serum of dominant and subordinate mice than in the control group (p<0.05). The results indicated that, although both dominant and subordinate animals displayed an increase in serum corticosterone and proinflammatory cytokines during social interactions, their response to pain perception differently was affected with the social status.     

Neuroendocrine response patterns in dominant and subordinate mice.

The sequence and type of neuroendocrine and behavioral patterns resulting from the development of a social hierarchy in colonies of mice were studied. It was found that dominant males were more active and responded to social interaction with predominantly a sympathetic adrenal-medullary pattern. Subordinate males were less active and predominantly responded with a pituitary adrenal-cortical pattern. The neuroendocrine patterns were reversed when the social position of the animal was reversed. Also the subordinate males demonstrated greater plasma corticosterone responsiveness to ACTH administration and immobilization stress as compared to dominant males.     

The Effect of Social Stress on Chronic Pain Perception in Female and Male Mice

The current investigations on social stress primarily point to the negative health consequences of being in a stressful social hierarchy. The repetitive nature of such stressors seems to affect behavioral response to pain both in rodents and humans. Moreover, a large discrepancy in the possibility of social stresses affecting pain perception in the two genders exists. The present study examined the effect of chronic social stress on nociceptive responses of both sexes by implementing of food deprivation, food intake inequality and unstable social status (cage-mate change every 3 days) for a period of 14 days in 96 Balb/c mice. In this regard we injected 20 µl formalin 2% into the plantar surface of hind paw at the end of stress period and scored pain behaviors of all subjects, then serum concentrations of proinflammatory cytokines were measured. Our results showed that there was significant difference in chronic phase of formalin test following implementation of food deprivation and inequality (P<0.05) as compared to control group, so that pain perception was decreased considerably and this decline in inequality exposed subjects was well above isolated ones (P<0.05); whereas unstable social situation did not affect pain perception. Moreover, IL-1 and IL-6 concentrations in serum of stressed mice of both genders were well above control group (p<0.05). Finally, despite chronic pain perception in control and unstable male subjects was larger than females; the decrease of chronic pain perception in male stressed animals (poverty and inequality experienced subjects) was much more than stressed females. These results revealed that although food deprivation and social inequality can induce hypoalgesia, some socioeconomic situations like social instability don''t affect pain sensation, whereas there were similar increases of proinflammatory cytokines level in all socially stressed subjects. In addition, males display larger hypoalgesic responses to inequality as compared with females.     

Polygynandry in a red fox population: implications for the evolution of group living in canids?

Canid social groups are typically thought to consist of extendedfamilies, that is, a dominant breeding pair and related nonbreedingsubordinates, that principally obtain indirect fitness benefitsfrom helping to raise the offspring of the dominant pair. Consequently,the monogamous pair has been viewed as the basic fundamentalunit of canid social organization. However, there have beenfew genetic studies that have tested this assumption. We analyzedthe parentage of red foxes (Vulpes vulpes) in a high-density(19.6–27.7 adult foxes/km²) population in Bristol, UK,to determine (1) whether groups typically produced a singlelitter of cubs annually and (2) whether male and female foxesexhibited monogamous mating strategies. Social monogamy (theproduction of one litter in a social group) was observed orassumed in 54% of breeding attempts (N = 13 group-years). However,polyandrous and polygynous patterns of mating were common. Multiplepaternity was confirmed in 38% of litters (N = 16) containingoffspring with resolved maternity and paternity (N = 30 cubs);when including cubs with unresolved paternity (N = 20), multiple-paternitymay have occurred in 69% of litters. Litters were sired by anaverage of 1.6 identified males (range = 1–4); when includingcubs with unresolved paternity, litters may have been siredby up to seven males. Only 20% (6/30) of cubs with resolvedmaternity and paternity were sired by males within the socialgroup. Within groups, dominant females did not breed with subordinatemales; dominant males did breed with subordinate females. Dominantand subordinate females both produced cubs with dominant andsubordinate males from other social groups. Mean adult relatednessin groups typically ranged from 0.15–0.35, indicativeof second-order rather than first-order relatives.     

Stress ulcer modulation by limbic system structures.

A number of studies suggest that the telencephalic limbic system modulates stress ulcer development. The amygdala is assumed to connect sensory experiences, including stressful stimuli, with the emotional reactions and gastrointestinal effects normally produce. The hippocampal formation (entorhinal cortex, dentate gyrus, hippocampus) is part of a gating system, modulating the organism's coping ability. Changes in transmission in this temporal brain region are linked to individual differences in stress ulcer severity. Interactions among "classical" transmitters and several neuropeptides mediate these differences.     

House sparrows (Passer domesticus) adjust their social status position to their physiological costs

For group-living animals, the maintenance of a position in the social hierarchy may be associated with physiological costs such as increased stress and energy expenditure or suppressed immune functions. In this study, we experimentally manipulated the social status of house sparrows so that each bird experienced two social environments in random sequence: being dominant and subordinate. For 14 males, we investigated how corticosterone concentrations, energy expenditure and immune functions were affected by these changes in social status position. We found that the cost of maintaining a social status position differed between individuals and were related to individual body size. Birds with small body size had increased costs in terms of increased stress responses and reduced cell-mediated immune responses while being experimentally kept as dominants, while birds with large body size had increased costs while they were subordinates. We also found that birds with increased energetic and immunological costs as dominants obtained a low status position in the large group, while birds with increased costs as subordinates obtained a high status position in the large group. In summary, we found that the costs associated with the maintenance of social status position differed between individuals and was related to the individuals' body size. Furthermore, in a large group, individuals maintained a social status position that minimized energetic and immunological costs.     

Male dominance and immunocompetence in a field cricket

Female preference for dominant males has been found in manyspecies, and it is generally thought that winners of male-malecompetition are of superior quality. Success in contests probablydepends on male condition and overall health. Thus, femalescould avoid infection and gain genetic benefits in terms ofmore viable offspring by mating with dominant males. In thepresent study, we tested whether dominant males of the Mediterraneanfield cricket, Gryllus bimaculatus, had higher immunocompetencethan did their subordinates in experimental trials. We foundthat dominant males had better immune defense, as indicatedby significantly higher encapsulation rate and lytic activity,than did subordinate males of the same size. Dominant maleswere also more successful in obtaining matings, but this wasmeasured nonindependently of dominance status. Our results suggestthat a male's dominance status and success in fights may indicatehis immunocompetence to females.