Color change as a potential behavioral strategy

Within species, color morphs may enhance camouflage, improve communication and/or confer reproductive advantage. However, in the male cichlid Astatotilapia burtoni, body color may also signal a behavioral strategy. A. burtoni live in a lek-like social system in Lake Tanganyika, Africa where bright blue or yellow territorial (T) males (together ~ 10–30% of the population) are reproductively capable and defend territories containing food with a spawning site. In contrast, non-territorial (NT) males are smaller, cryptically colored, shoal with females and have regressed gonads. Importantly, males switch between these social states depending on their success in aggressive encounters. Yellow and blue morphs were thought to be adaptations to particular habitats, but they co-exist both in nature and in the laboratory. Importantly, individual males can switch colors so we asked whether color influences behavioral and hormonal profiles. When pairing territorial males with opposite colored fish, yellow males became dominant over blue males significantly more frequently. Moreover, yellow T males had significantly higher levels of 11-ketotosterone than blue T males while only blue NT males had higher levels of the stress hormone cortisol compared to the other groups. Thus color differences alone predict dominance status and hormone profiles in T males. Since T males can and do change color, this suggests that A. burtoni may use color as a flexible behavioral strategy.     

Territorial male color predicts agonistic behavior of conspecifics in a color polymorphic species

Male cichlid fish, Astatotilapia burtoni, live in a lek-likesocial system in shore pools of Lake Tanganyika, Africa, asone of two distinct social phenotypes: territorial (T) malesthat comprise approximately 10–30% of the population andnonterritorial (NT) males that make up the rest. T males arebrightly colored either blue or yellow with chromatic body patternsand are larger, reproductively capable, and defend territoriescontaining a food resource used to entice females to spawn withthem. NT males are camouflage colored, smaller, have regressedgonads, and shoal with females. Importantly, males shift betweenthese social states depending on their success in aggressiveencounters. It is not known whether there is a difference betweenyellow and blue T morphs. Here we asked whether T males preferentiallydefend their territory against a male of the same or oppositecolor. T males observed in social groups had agonistic interactionspredominantly with neighboring T males of the opposite color,and yellow morphs initiated significantly more aggressive interactions.When agonistic preference was tested experimentally, T maleshad significantly more agonistic interactions toward males ofthe opposite color, and yellow T males became territorial inthe majority of those interactions. Taken together, these resultssuggest that male coloration is an important social signal amongneighboring T males in this species and support the hypothesisthat T males differentially direct agonistic behavior dependingon the color of neighboring males.     

Social Opportunity Rapidly Regulates Expression of CRF and CRF Receptors in the Brain during Social Ascent of a Teleost Fish,Astatotilapia burtoni

In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF₁ receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR₁ and CRFR₂ receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.     

Behavioral and physiological plasticity: Rapid changes during social ascent in an African cichlid fish

In many vertebrates, reproduction is regulated by social interactions in which dominant males control access to females and food. Subordinate males that displace dominant individuals must rapidly adopt behavioral and physiological traits of the higher rank to gain reproductive success. To understand the process of phenotypic plasticity during social ascent, we analyzed the temporal expression pattern of dominance behaviors and circulating androgen levels when socially-suppressed males of an African cichlid fish Astatotilapia burtoni ascended in status. These experiments tested a prediction of the ‘challenge hypothesis’ that, during periods of social instability, male androgen levels are higher than during socially stable times. We found that socially and reproductively suppressed males perform territorial and reproductive behaviors within minutes of an opportunity to ascend in status, and that animals switch from initial expression of territorial behaviors to more reproductive behaviors during territory establishment. Following this rapid response, social stability may be achieved within 1-3 days of social ascent. Consistent with predictions of the ‘challenge hypothesis’, circulating 11-ketotestosterone (11-KT) levels were elevated within 30 min following social opportunity, coincident with increased aggressive behavior. However, territorial behaviors and serum 11-KT levels were then dissociated by 72 h after social ascent, suggesting either rapid social stability and/or increased physiological potential for androgen production. This behavioral and physiological plasticity in male A. burtoni suggests that perception of social opportunity triggers a suite of quick changes to facilitate rapid transition towards reproductive success, and reveals important features of social ascent not previously recognized.     

Interaction effects of corticosterone and experience on aggressive behavior in the green anole lizard

Aggressive encounters are accompanied by a release of stress hormone, and this corticosterone (CORT) secretion could influence aggressive behavior in subsequent encounters. We investigated the modulating effects of CORT on aggressive behavior in the context of a 5-day social experience in male green anole lizards. In Experiment 1, we measured plasma CORT levels in animals that were exposed for different times to aggressive males. In Experiment 2, using metyrapone, a CORT synthesis blocker, we tested whether CORT secretion in response to the aggressive stimulus plays a role in experience-dependent facilitation of aggressive behavior. We hypothesized that aggressive encounters would increase plasma CORT levels, and that blocking CORT synthesis with metyrapone treatment during the aggressive encounter would cause an animal to become more aggressive. We also tested whether blocking CORT would interfere with the influence of 5-day social experience on animals' behavior in a subsequent aggressive encounter. Animals that were exposed to another male showed higher plasma CORT levels immediately after the 10 min encounter than animals exposed to the non-social video, and this high level was maintained through day 5. Within the aggressive video groups, in Experiment 2, there was a distinctly different pattern in displays depending on drug condition: vehicle-injected animals showed gradual increases followed by decreases in aggressive behavioral responses to the video as the five days proceeded (habituation), while animals injected with metyrapone started out with high aggressive behavior and did not decrease behavioral responses at later trials (no habituation). Finally, when tested with a novel conspecific on day 6, animals previously injected with metyrapone showed no higher aggression than did animals previously injected with vehicle and exposed to the aggressive video. These results suggest that blocking CORT synthesis during the exposure to the aggressive video induced animals to remain aggressive toward the repetitive stimulus without habituating, while not becoming more aggressive than controls toward a novel challenger.     

Behavioral response to familiar and unfamiliar neighbors in a territorial cichlid, <Emphasis Type="Italic">Neolamprologus pulcher</Emphasis>

Some territorial species have been shown to react more aggressively toward unfamiliar conspecifics than established neighbors, a behavior referred to as the dear enemy phenomenon. Laboratory experiments were conducted to determine whether males of a territorial African cichlid, Neolamprologus pulcher, can discriminate between size-matched familiar and unfamiliar male neighbors and whether they respond more aggressively toward unfamiliar males. It was found that males spent significantly more time near the territorial boundary that they shared with unfamiliar neighbors and directed significantly more aggressive behavior toward these individuals.     

Circulating androgens are influenced by parental nest defense in a wild teleost fish

While social interactions influence vertebrate endocrine regulation, the dynamics of regulation in relation to specific behaviors have not been clearly elucidated. In the current study, we investigated whether androgens (testosterone) or glucocorticoids (cortisol) play a functional role in aggressive offspring defense behavior in wild smallmouth bass (Micropterus dolomieu), a teleost fish with sole paternal care. We measured circulating testosterone and cortisol concentrations in plasma samples taken from parental males following a simulated nest intrusion by a common nest predator, the bluegill sunfish (Lepomis macrochirus). To understand whether endocrine regulation changes across the parental care period, we looked both at males guarding fresh eggs and at males guarding hatched embryos. Plasma testosterone levels increased in males subjected to a simulated nest intrusion when compared to sham controls. Testosterone concentrations in males guarding embryos were lower than in males guarding fresh eggs, but circulating testosterone was positively correlated with the level of aggression towards the nest predator at both offspring development stages. However, there was no increase in cortisol levels following a simulated nest intrusion, and no relationship between cortisol and any measured parameter. These results suggest that androgens play an important role in promoting aggressive nest defense behavior in teleost fish.     

Aggressive Behavior and Courtship Rejection in Brightly and Plainly Colored Female Keeled Earless Lizards (Holbrookia propinqua)

Relationships between bright secondary sexual coloration and behavior were studied in female Holbrookia propinqua, which develop striking orange and yellow colors during the breeding season. In tethered introduction studies, brightly colored females performed aggressive courtship rejection behaviors toward conspecific males; plainly colored females were not aggressive toward males, but attempted to avoid them. Responses of females of the two color patterns toward conspecific females of both color phases were not detectably different. Experimental introductions of lizards with coloration modified by paint showed that females of both color patterns recognize any other lizard bearing the bright female colors as female, regardless of actual sex. Both the orange and yellow components were shown to contribute to sex recognition. The yellow component alone allowed accurate sex identification, but only half the females responded to males painted with only the orange female component as if they were females. Because females did not behave differently toward other females on the basis of coloration, the hypothesis that bright coloration evolved as an adaptive signal between females is rejected. The dark ventrolateral stripes of male and plainly colored females did not appear to affect intraspecific social responses by females.     

The possibility of sex and nymph discrimination by the male cockroach,Nauphoeta cinerea

The possibility of sex and nymph discrimination by males was investigated in the cockroach,Nauphoeta cinerea (Olivier). A sexually mature male takes a courting position toward a sexually mature female when he comes into contact with her and recognizes her through antennal contact. In contrast, males often behave aggressively toward each other: they bite at each others; wings and/or legs, chase each other and antennate mutually. The male, however, does not show conspicuous behavior (mating behavior or aggressive behavior) toward nearby nymphs. The male produces audible sounds when he courts a sexually mature but non-receptive female who does not respond to his courtship behavior. We found that the male also stridulates after he repeatedly courts immature teneral females, males and (last-instar) nymphs. After the bodies of teneral insects are sclerotized, the male shows courship and stridulation behavior toward sexually mature but non-receptive females but not toward mature males and nymphs. At this stage the male begins to behave aggressively toward other post-teneral mature males. We think that the variability of the sexually mature male's behavior toward other conspecifics (courtship behavior toward female, aggressive behavior toward male and no conspicuous response toward nymph) results from the male's recognition of adult and nymph.     

Social Network Analysis of Male Dominance in the Paper Wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Social aggression is a pervasive feature of insect societies. In eusocial Hymenoptera, aggression among females can affect task performance and competition over direct reproduction (egg laying); in most species males participate in social interactions relatively rarely. Males of the independent-founding paper wasp Mischocyttarus mastigophorus are exceptional: they are aggressive toward female nestmates, leading us to explore the function of this unusual behavior. We applied social network analyses to data on M. mastigophorus social aggression to quantify sex differences in giving and receiving social aggression. The network analyses supported the pattern of biased male aggression toward female nestmates; females are relatively rarely aggressive to males. We then asked whether male aggression toward females was biased by females’ relative ovary development. Males were more aggressive toward females with better-developed ovaries, opposite to patterns of aggression among females. Because food brought to the colonies is often monopolized by dominant females, we suggest that males direct aggression toward socially dominant females with better-developed ovaries to obtain food. The implications of biased male aggression for female task performance and physiology are unknown.

     

Social plasticity in non-territorial male African cichlid fish <Emphasis Type="Italic">Astatotilapia burtoni</Emphasis>

The African cichlid fish Astatotilapia burtoni represents a valuable model system for studies of social decision-making due to its socially mediated phenotypic plasticity. The males reversibly transition in social status from reproductively dominant and territorial (DOM) to submissive and non-territorial (SUB). Males are traditionally categorized into these two behavioral phenotypes by observational scoring. There is evidence, however, that this dichotomous categorization might not capture the behavioral plasticity displayed by individuals transitioning between SUB and DOM status. To test this concept, we used focal observations of intrasexual conflict behavior in fish communities combined with a modified analysis of the ethogram typically used in A. burtoni. Results revealed a cluster of males close to the crossover point between SUB and DOM status as defined by the traditional dominance index. These intermediate males showed the highest frequency of intrasexual conflict behaviors, distinct behavioral responses to threats, and body pigment signaling displays that distinguish them from prototypical SUBs and DOMs. As such, our results provide a noninvasive behavioral metric to categorize A. burtoni males into three groups, thus further capturing the complex social dynamic of this model organism.     

Paternal behavior in the Mongolian gerbil (Meriones unguiculatus): Estrogenic and androgenic regulation

Here, we analyzed the effects of testosterone (T) and its metabolites, estradiol (E₂) and dihydrotestosterone (DHT), on the onset of paternal behavior in virgin male Mongolian gerbils (Meriones unguiculatus). We hypothesized that T and E₂, but not DHT, would facilitate the onset of paternal behavior. Seventy males displaying aggression toward pups were selected through a paternal behavior screening test. Forty males were bilaterally castrated. Of them, 10 were implanted with T, 10 with E₂, and 10 with DHT, and 10 received no treatment. Another 30 males underwent a sham procedure. In these gerbils, T, E₂ and DHT were measured to obtain the basal levels of these hormones. After treatment, the paternal behavior test was conducted again. Blood samples were obtained immediately after the administration of the test for the quantification of T, E₂ and DHT by radioimmunoassay. Surprisingly, 100% of the males that received T, E₂ and DHT implants stopped being aggressive and became paternal. Castrated and sham-operated males displayed no changes in their aggressive behaviors. This is the first report that T and its metabolites are involved in neuroendocrine mechanisms that inhibit aggression toward pups and facilitate paternal behavior in virgin male Mongolian gerbils. In addition, this is the first report of regulation of paternal behavior in a rodent by estrogenic and androgenic pathways.     

Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences

Territorial aggression is influenced by many social and environmental factors. Since aggression is a costly behavior, individuals should account for multiple factors such as population density or reproductive status before engaging in aggression. Previous work has shown that male California mice (Peromyscus californicus) respond to winning aggressive encounters by initiating aggression more quickly in future encounters, and we investigated the physiological basis for this effect. We found that injections that produced a transient increase in testosterone (T) following an aggressive encounter caused males to behave more aggressively in an encounter the following day. Experience alone was not enough to change aggression, as males treated with saline injections showed no change in aggression. The effect of T injections on aggression was androgen-based, as the inhibition of aromatase did not block the T injections from increasing aggression. Aromatase inhibition did, however, increase aggression in the initial aggression tests (before application of T or saline injections), and aromatase activity in the bed nucleus of the stria terminalis (BNST) was negatively correlated with aggression. A previous study suggested that aromatase activity in the BNST decreases after males become fathers. Thus, distinct neuroendocrine mechanisms allow male California mice to adjust aggressive behavior in response to changes in social and reproductive status.     

Social context affects behavior,preoptic area gene expression,and response to D2 receptor manipulation during territorial defense in a cichlid fish

Social context often has profound effects on behavior, yet the neural and molecular mechanisms which mediate flexible behavioral responses to different social environments are not well understood. We used the African cichlid fish, Astatotilapia burtoni, to examine aggressive defense behavior across three social contexts representing different motivational states: a reproductive opportunity, a familiar male and a neutral context. To elucidate how differences in behavior across contexts may be mediated by neural gene expression, we examined gene expression in the preoptic area, a brain region known to control male aggressive and sexual behavior. We show that social context has broad effects on preoptic gene expression. Specifically, we found that the expression of genes encoding nonapeptides and sex steroid receptors are upregulated in the familiar male context. Furthermore, circulating levels of testosterone and cortisol varied markedly depending on social context. We also manipulated the D2 receptor (D2R) in each social context, given that it has been implicated in mediating context‐dependent behavior. We found that a D2R agonist reduced intruder‐directed aggression in the reproductive opportunity and familiar male contexts, while a D2R antagonist inhibited intruder‐directed aggression in the reproductive opportunity context and increased aggression in the neutral context. Our results demonstrate a critical role for preoptic gene expression, as well as circulating steroid hormone levels, in encoding information from the social environment and in shaping adaptive behavior. In addition, they provide further evidence for a role of D2R in context‐dependent behavior.     

The influence of age and experience with conspecifics on territorial behavior inDrosophila melanogaster

Drosophila melanogastermales initiated aggressive behavior toward other males and defended territories several hours after they were able to court and mate females. Males that were 3 days or more posteclosion were more successful at holding territories than younger males. Three-day-old males established territories more readily and escalated more often against territory residents than males that were 1 day old. Residents did not usually force young males from territories until they were a few hours posteclosion. The development of territorial behavior was not affected by familiarity or prior exposure to females. Males held in isolation established territories more quickly and behaved more aggressively than males held in groups. Males that previously held territories were more likely to reestablish them after a disturbance.     

Low-ranking individuals present high and unstable fecal cortisol levels in provisioned free-ranging adult male rhesus macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) during the birth season in a mountain area of northern China

Social hierarchy commonly exists in animal societies, affecting both the endocrine functioning and the behavior of animals. In nonhuman primates, the relationship between social rank and cortisol levels varies across species and even within species. Here, we assessed the relationships between social rank and fecal cortisol levels in adult male Taihangshan macaques (rhesus macaques, Macaca mulatta tcheliensis) from the provisioned, free-ranging Wulongkou-2 (WLK-2) group inhabiting Wulongkou Scenic Area, Jiyuan, China. From March to May 2014, we recorded 195 agonistic behaviors and collected 54 fresh fecal samples from eight adult male Taihangshan macaques. Males were assigned a social rank according to an agonistic behavior matrix, and enzyme-linked immunosorbent assay was then used to measure the cortisol concentration in the fecal samples. We found that social rank among the eight male Taihangshan macaques in WLK-2 group followed a strict linear hierarchy, and that fecal cortisol levels were significantly higher and more variable in low-ranking males than in more dominant individuals. Age was not significantly associated with social rank or fecal cortisol levels. Our results suggest that social rank and maintenance of the social hierarchy within the WLK-2 group is a chronic stressor, with low-ranking males maintaining heightened stress levels and enlarged reactive scope relative to dominant males. This provides new support for the theory that social environment can influence endocrine functioning.     

The effect of social isolation on androgen and corticosteroid levels in a cichlid fish (Haplochromis burtoni) and in swordtails (Xiphophorus helleri)

The blood androgen and glucocorticoid levels of male Haplochromis burtoni and Xiphophorus helleri were measured in socially isolated individuals (8 and 4 weeks, respectively) and nonisolated controls. In both species social isolation leads to significant reductions of mean concentrations and variances, both for androgens and corticosteroids. It is known for H. burtoni—and new evidence for X. helleri is presented—that social isolation reduces aggressivity in nonescalating situations. It is proposed that social stimuli in both species stimulate the testes to produce more androgenic hormones, and that this can lead to higher levels of aggression. At least in tropical fish species the androgenic optimum for defending a territory or a social status may be much more controlled by social stimuli than previously realized.     

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.     

Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena)

Concentration of the hormone cortisol is often used as an indicator of stress, and chronically high cortisol levels are often associated with poor health. Among group living animals that compete for resources, agonistic social interactions can be expected to contribute to variation in cortisol levels within and among individuals over time. Reproductive tactics of males can change with individual quality, relatedness, and social structure, and affect cortisol levels. In gray-cheeked mangabey (Lophocebus albigena) groups, male rank is an important factor in social interactions, and males also move between groups while actively competing for females or sneaking copulations. During a 20-month study we observed the social behavior and collected 461 fecal samples from 24 adult male gray-cheeked mangabeys from five groups in Kibale National Park, Uganda. Aggressive interactions and the presence of females at the peak of sexual swelling were associated with elevated cortisol concentrations in all males. Independently, dominant (i.e., highest-ranking) males within groups had higher cortisol concentrations than subordinate males, and immigrant males had higher cortisol concentrations than dominant males.     

Responses to song playback vary with the vocal performance of both signal senders and receivers

Mating signals of many animal species are difficult to produce and thus should indicate signaler quality. Growing evidence suggests that receivers modulate their behaviour in response to signals with varying performance levels, although little is known about if and how responses are affected by receiver attributes. To explore this topic we conducted two experiments with swamp sparrows, Melospiza georgiana, in which we challenged territorial males with playback of songs with trill rates that were natural, digitally reduced, or digitally elevated (control-, low- and high-performance stimuli, respectively). In our first experiment, we found that males responded more aggressively to control songs than to low-performance stimuli, that low-performance stimuli with the most severe trill-rate reductions elicited the weakest aggressive responses, and that the subjects'' own trill rates predicted aggressive responses. In our second experiment, we found that male responses to high-performance stimuli varied significantly, in ways predicted by two factors: the degree to which we had elevated stimulus performance levels of high-performance stimuli, and subjects'' own vocal performance levels. Specifically, males were less aggressive towards stimuli for which we had elevated performance levels to higher degrees, and subject males with higher vocal performances themselves responded more aggressively. These findings together offer a novel illustration of how responses to aggressive signals may rely not just on signal attributes, but also on attributes of responding animals themselves.