Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse

Arginine vasotocin (AVT) and its mammalian homologoue arginine vasopressin (AVP) influence male sexual and aggressive behaviors in many species. We tested the effects of AVT and an AVP-V(1a) receptor antagonist on the display of alternative male tactics in a tropical coral reef fish, the bluehead wrasse Thalassoma bifasciatum. We gave AVT injections to territorial and nonterritorial males of the large and colorful phenotype (terminal phase) and an AVP-V(1a) receptor antagonist, Manning compound, to territorial males in the field. AVT increased courtship independent of status, while its effects on territoriality and aggression were dependent upon male status. In territorial males, AVT increased courtship and tended to decrease the number of chases toward initial phase individuals. In nonterritorial males, AVT increased courtship, chases toward initial phase individuals, and territorial behavior while decreasing feeding. These are all behaviors rarely seen in nonterritorial males, so AVT made these males act like territorial TP males. The AVP-V(1a) receptor antagonist had opposite effects. It decreased courtship and territorial defense, making these males act more like nonterritorial males. Manipulations of the AVT system shifted males within a single phenotype from the nonterritorial social status to the territorial social status and vice versa. Since the entire suite of behaviors related to territoriality was affected by AVT system manipulations, our results suggest that the AVT system may play a key role in motivation of behaviors related to mating.     

Courtship behavior of male white perch, Morone americana: evidence for control by androgens

Courtship behaviors are androgen-dependent in many vertebrates and castration often decreases courtship. We examined the effectiveness of castration in reducing courtship behaviors and 11-ketotestosterone (KT) and testosterone (T) in restoring them in male white perch. Castrates were given implants containing KT, T or no hormone. Sham-operated males received implants without hormone. Three weeks later, males were exposed to an ovulated female for 1 h and two courtship behaviors were quantified. Attending behavior involves close and continuous following of a female with occasional contact. Circling involves rapid transits around the female in a circular pattern or back and forth in front of her. In plasma samples taken immediately after observations, KT and T were below detectable levels in castrated males but at high physiological levels in males implanted with KT or T. Castrated males given KT attended females more than castrated males given T implants or implants containing no hormone, but not more than sham-operated males. Circling was eliminated by castration but restored by implantation with T or 11-KT to values exhibited by sham-operated males. This is one of the few demonstrations that KT can regulate courtship behavior in a non-territorial and economically important fish species.     

Social context influences aggressive and courtship behavior in a cichlid fish

Social interactions require knowledge of the environment and status of others, which can be acquired indirectly by observing the behavior of others. When being observed, animals can also alter their signals based on who is watching. Here we observed how male cichlid fish (Astatotilapia burtoni) behave when being watched in two different contexts. In the first, we show that aggressive and courtship behaviors displayed by subordinate males depends critically on whether dominant males can see them, and in the second, we manipulated who was watching aggressive interactions and showed that dominant males will change their behavior depending on audience composition. In both cases, when a more dominant individual is out of view and the audience consists of more subordinate individuals, those males signal key social information to females by displaying courtship and dominant behaviors. In contrast, when a dominant male is present, males cease both aggression and courtship. These data suggest that males are keenly aware of their social environment and modulate their aggressive and courtship behaviors strategically for reproductive and social advantage.     

Vasotocin stimulates appetitive responses to the visual and pheromonal stimuli used by male roughskin newts during courtship

It is now well established that vasotocin (AVT) and its mammalian homologue vasopressin influence various social behaviors in vertebrates, but less is known about the mechanisms through which these peptides modulate behavior. In male roughskin newts, Taricha granulosa, AVT stimulates a courtship behavior, amplectic clasping. Three general explanations for how AVT affects male courtship behavior have been considered: by enhancing a central state of sexual motivation, by affecting sensorimotor integration mechanisms in individual sensory modalities, or by influencing a nonspecific state of attention, arousal, or anxiety. AVT administration enhanced appetitive responses to visual and olfactory sexual stimuli, as would be expected if AVT affects a state of sexual motivation that affects behavioral responses to sexual stimuli regardless of the sensory modality in which they are processed. However, AVT selectively enhanced responses to female olfactory stimuli (sex pheromones), but similarly enhanced responses to female and food-related visual stimuli (worms), thus questioning the utility of such a motivational mechanism, as responses to female stimuli were not selectively enhanced in all sensory modalities. We therefore propose that exogenous AVT independently influences olfactory processes associated with orientation/attraction toward a female sex pheromone and visual processes associated with orientation/attraction toward a visual feature common to females and worms. In further experiments AVT administration failed to stimulate feeding behavior but did decrease locomotor activity. Thus, AVT does not stimulate courtship behavior in this species by enhancing the animals' general state of attention or by decreasing general anxiety, as responses to nonsexual, attractive stimuli were not uniformly enhanced, nor by stimulating general arousal, as activity levels did not increase. Rather, the data support the conclusion that AVT affects courtship by influencing specific sensorimotor processes associated with behavioral responses to individual releasing stimuli, which suggests a mechanistic framework for understanding socially motivated behavior is this species.     

The effects of sex steroids and vasotocin on behavioral responses to visual and olfactory sexual stimuli in ovariectomized female roughskin newts

Previous studies have found that vasotocin (AVT) administration to male roughskin newts (Taricha granulosa) enhances courtship clasping as well as appetitive responses to specific sexual stimuli and that treating female newts with androgens plus AVT induces the expression of male-typical courtship clasping (the selective clasping of females). However, the unique and/or interactive effects of sex steroids and AVT on appetitive responses to specific sexual stimuli have not yet been determined. To first identify male-typical, sexually dimorphic appetitive responses to female sexual stimuli, we tested intact newts during the breeding season and found that males, but not females, are attracted to female visual and pheromonal sexual stimuli. We then used ovariectomized (ovx) females implanted with empty silastic capsules (Blk) or with capsules containing testosterone (T), dihydrotestosterone (DHT), or estradiol (E2) and then injected with either saline or AVT to determine the effects of steroids and AVT, alone or in combination with each other, on male-typical behavioral responses to those stimuli. E2 treatment depressed responses toward female visual stimuli independently of AVT. On the other hand, only T-implanted, AVT-injected females displayed male-typical behavioral responses toward female olfactory stimuli, preferring to spend more time in proximity to female-scented than unscented newt models and selectively clasping the female-scented models. Together, these results support the conclusion that sex steroids and AVT influence behavioral responses to sexual stimuli via sensory-specific mechanisms. Furthermore, they suggest that T and AVT interact within the brain to influence sensorimotor processing in the pathways that integrate olfactory sexual stimuli into male-typical courtship behaviors.     

Androgen and behavior in the male three-spined stickleback,Gasterosteus aculeatus I.--changes in 11-ketotestosterone levels during the nesting cycle

Circulating 11-ketotestosterone (11KT) levels are higher during the courtship phase than during the later parental phase in a number of male teleosts. The present study describes the temporal changes in 11KT levels and their relationships to changes in courtship behavior, after different number of spawnings, over the nesting cycle of the male three-spined stickleback, Gasterosteus aculeatus, a small teleost showing pronounced paternal behavior. Plasma 11KT levels, measured by radioimmunoassay, were approximately 34 times higher during the initial courtship phase than at the end of the following parental phase in spawned males. In addition, males that spawned with three or more females on a single day showed an earlier decline in 11KT levels and in courtship behavior compared to males that were only allowed to spawn with a single female. Plasma 11KT levels remained high in males not allowed to spawn.     

Courtship behavior of male white perch, Morone americana: evidence for control by androgens.

Courtship behaviors are androgen-dependent in many vertebrates and castration often decreases courtship. We examined the effectiveness of castration in reducing courtship behaviors and 11-ketotestosterone (KT) and testosterone (T) in restoring them in male white perch. Castrates were given implants containing KT, T or no hormone. Sham-operated males received implants without hormone. Three weeks later, males were exposed to an ovulated female for 1 h and two courtship behaviors were quantified. Attending behavior involves close and continuous following of a female with occasional contact. Circling involves rapid transits around the female in a circular pattern or back and forth in front of her. In plasma samples taken immediately after observations, KT and T were below detectable levels in castrated males but at high physiological levels in males implanted with KT or T. Castrated males given KT attended females more than castrated males given T implants or implants containing no hormone, but not more than sham-operated males. Circling was eliminated by castration but restored by implantation with T or 11-KT to values exhibited by sham-operated males. This is one of the few demonstrations that KT can regulate courtship behavior in a non-territorial and economically important fish species.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Involvement of arginine vasotocin in reproductive events in the male newt Cynops pyrrhogaster

Effects of arginine vasotocin (AVT) on reproductive events such as courtship behavior, pheromone release, and spermatophore discharge were investigated in the male newt Cynops pyrrhogaster. AVT enhanced the incidence and frequency of androgen-induced courtship behavior. In this case, AVT was likely to act centrally because the behavior was evoked with a much smaller amount of AVT when the hormone was administered intracerebroventricularly than when given intraperitoneally. Involvement of endogenous AVT in spontaneously occurring courtship behavior was also evidenced by the fact that administration of a V1 (vasopressor) receptor antagonist, [d(CH2)5(1), Tyr(Me)2, Arg8-vasopressin] suppressed the expression of the courtship behavior. The water in which AVT-treated males had been kept showed considerable female-attracting activity as compared with the water in which saline-injected males had been kept. Moreover, the content of sodefrin, a female-attracting pheromone in the abdominal gland, was decreased by the intraperitoneal injection of AVT, suggesting that the neurohypophyseal hormone stimulated the release of sodefrin from the abdominal gland into the water. AVT induced contraction of the excised abdominal gland concentration-dependently, and, again, the V1 receptor antagonist suppressed the AVT-induced contraction. Thus, we concluded that AVT induces the pheromone discharge, acting peripherally on a contractile structure of the abdominal gland. AVT was also found to induce spermatophore deposition in the male kept in the absence of the female. Administration of the V1 receptor blocker to the sexually developed males suppressed the spermatophore deposition. All these results indicate the involvement of AVT in reproductive events acting centrally and peripherally.     

Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae)

Pupfishes in the Death Valley region have rapidly differentiated in social behaviors since their isolation in a series of desert streams, springs, and marshes less than 20,000 years ago. These habitats can show dramatic fluctuations in ecological conditions, and pupfish must cope with the changes by plastic physiological and behavioral responses. Recently, we showed differences among some Death Valley populations in brain expression of arginine vasotocin (AVT). As AVT regulates both hydromineral balance and social behaviors in other taxa, these population differences may indicate adaptive changes in osmoregulatory and/or behavioral processes. To test whether AVT is relevant for behavioral shifts in these fish, here we examined how manipulations to the AVT system affect agonistic and reproductive behaviors in Amargosa River pupfish (Cyprinodon nevadensis amargosae). We administered exogenous AVT (0.1, 1, and 10 microg/g body weight) and an AVP V1 receptor antagonist (Manning compound, 2.5 microg/g body weight) intraperitoneally to males in mixed-sex groups in the laboratory. We found that AVT reduced the initiation of aggressive social interactions with other pupfish but had no effect on courtship. The effects of AVT were confirmed in males in the wild where AVT (1 microg/g body weight) reduced the aggressive initiation of social interactions and decreased aggressive responses to the behavior of other males. Combined, these results show that AVT can modulate agonistic behaviors in male pupfish and support the idea that variation in AVT activity may underlie differences in aggression among Death Valley populations.     

Visual sex discrimination in goldfish: seasonal, sexual, and androgenic influences

The olfactory signals used by goldfish for sexual and aggressive communication have been studied extensively, but little work has addressed the role of other sensory modalities in social communication in this species. We therefore investigated the role that visual stimuli play in sex discrimination and the ability of androgens, which masculinize courtship behavior, to affect behavioral responses toward female visual stimuli. We found that males selectively orient toward female visual stimuli during the breeding season but not outside it, whereas prostaglandin F2-alpha (PGF2alpha)-injected females do not differentially approach male and female visual stimuli, even during the breeding season. Implanting adult females with testosterone (T) and 11-ketotestosterone (KT), however, induced orientation responses toward female visual stimuli similar to those observed in males. These results indicate that visual sexual stimuli are likely important for reproductive signaling in goldfish, potentially helping males identify ovulating females from a distance in a shoal of fish, and that androgens can influence mechanisms associated with orientation responses toward such stimuli.     

Analysis of tufted capuchin (Cebus apella) courtship and sexual behavior repertoire: changes throughout the female cycle and female interindividual differences

Sexual solicitations and initiative (proceptivity, sensu Beach [1976] Horm Behav 7:105-138) are important components of the sexuality of females of many primate species. In the tufted capuchin (Cebus apella), female proceptivity characterizes the species' mating system. In study 1, we defined and discussed 20 behavioral patterns based on the observation of 6 females and 5 males living in two social groups. In study 2, each behavior, including mounting activity, was quantitatively assessed during the periovulatory and nonperiovulatory cycle phases of 4 females, detected on the basis of urinary progestin levels (N = 20 ovulatory cycles, 5 for each female); moreover, we monitored changes in females' social interactions (agonism, grooming activity, and play). Nine of the behaviors typically used by the female during courtship and in sexual interactions showed a dramatic increase during the periovulatory phase. Though males mounted females at an apparently higher rate during the periovulatory than the nonperiovulatory phase, the difference was not significant. However, when adult male mounting is separated into those which occur within play and nonplay contexts, there is a significant periovulatory phase effect for mounts not associated with play. Females groomed adult males at the same rate throughout the cycle. Agonism and play did not show any phase effect; however, females' avoidance of adult males significantly increased during the periovulatory phase. Finally, each female made a statistically different use of the behavioral repertoire by performing some behaviors more than others. This variability among females during courtship calls for further research into whether it affects mating success.     

Getting that female glance: Patterns and consequences of male nonverbal behavior in courtship contexts

Females apparently are the choosier sex in courtship contexts, but there still is limited information about female selection criteria in real courtship settings. Given that a female knows little about a heretofore unacquainted male, upon what dimensions can (and do) females base their initial courtship decisions? Here, we report findings from observational studies that investigated male nonverbal behavior in a bar context. Study 1 documented the body movements of males prior to making contact with a female. It was found that males who successfully made “contact” courtship initiation with females exhibited different body language in this precontact phase than did males who did not make contact with females, including significantly more glancing behaviors, space-maximization movements, intrasexual touching, and less closed-body movements. The findings from a second within-subject study comparing the behavior of men in a bar when women were present or not present supported the initial study's findings and showed that males' emphasis on these behaviors increases in a mate-relevant context. We suggest that certain aspects of male nonverbal behavior in courtship contexts can serve as self-presentation and mate-value signals.     

Courtship Roles of Male and Female European Earwigs, Forficula auricularia L. (Dermaptera: Forficulidae), and Sexual Use of Forceps

Detailed observations of the courtship and mating of the European earwig Forficula auricularia revealed a complex of sexual behaviors for both males and females. A sequential analysis of the transition frequencies between male preceding-following behaviors showed that courtship is intricate and nonstereotyped. The significance of the male forceps was demonstrated by their use in early courtship with displays and later use as a tactile stimulus for the female. A study of males from which the forceps had been removed showed no mating by altered males. Male forcep length was bimodally distributed and positively allometric, while female forcep length was normally distributed. Males with longer forceps did not have a mating advantage. Receptive females were behaviorally active during courtship. The possible evolutionary development of the sexual dimorphism of the earwig is discussed.     

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

Competition for mates is a wide-spread phenomenon affecting individual reproductive success. The ability of animals to adjust their behaviors in response to changing social environment is important and well documented. Drosophila melanogaster males compete with one another for matings with females and modify their reproductive behaviors based on prior social interactions. However, it remains to be determined how male social experience that culminates in mating with a female impacts subsequent male reproductive behaviors and mating success. Here we show that sexual experience enhances future mating success. Previously mated D. melanogaster males adjust their courtship behaviors and out-compete sexually inexperienced males for copulations. Interestingly, courtship experience alone is not sufficient in providing this competitive advantage, indicating that copulation plays a role in reinforcing this social learning. We also show that females use their sense of hearing to preferentially mate with experienced males when given a choice. Our results demonstrate the ability of previously mated males to learn from their positive sexual experiences and adjust their behaviors to gain a mating advantage. These experienced-based changes in behavior reveal strategies that animals likely use to increase their fecundity in natural competitive environments.     

Nonapeptides and social behavior in fishes

The nonapeptide hormones arginine vasotocin and isotocin play important roles in mediating social behaviors in fishes. Studies in a diverse range of species demonstrate variation in vasotocin neuronal phenotypes across within and between sexes and species as well as effects of hormone administration on aggressive and sexual behaviors. However, patterns vary considerably across species and a general explanatory model for the role of vasotocin in teleost sociosexual behaviors has proven elusive. We review these findings, examine potential explanations for the lack of agreement across studies, and propose a model based on the parvocellular AVT neurons primarily mediating social approach and subordinance functions while the magnocellular and gigantocellular AVT neurons mediate courtship and aggressive behaviors. Isotocin neuronal phenotypes and effects on behavior are relatively unstudied, but research to date suggests this will be a fruitful line of inquiry. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

The nutritional contribution of males affects the feeding behavior and spatial distribution of females in a bruchid beetle,<Emphasis Type="Italic"> Bruchidius dorsalis</Emphasis>

The relationship between the quality/quantity of male investment and the feeding behavior of females was investigated in a bruchid weevil, Bruchidius dorsalis (Fahraeus), whose males donate nutrition via seminal fluid to females. Experiments on the effect of feeding regimes of both sexes on the mating frequency of females showed that females mated at a higher frequency if given low-quality food or poor male investment. On the other hand, the experiment that examined the effect of male investment quality on female feeding behavior showed that females receiving the high-quality investment exhibited feeding behavior less often. These results suggest that male investment and feeding behavior play the same role for B. dorsalis females. These experiments also showed that there are sex-related asymmetries in mating and feeding behaviors: females mated more often but males fed more often. Moreover, a field census suggested that only males visited non-host flowers to feed on the pollen and nectar during the non-flowering period of the host plants; females always stayed on the host plants irrespective of the flowering phenology. These results suggest that in B. dorsalis courtship role reversal and sex-specific feeding modes are fairly fixed and obligatory, and that male investment, derived from sexual selection, could affect the feeding behavior and spatial distribution of both sexes, which may have far-reaching impact in various ecological contexts.     

Differential effects of 11-ketotestosterone on dimorphic traits in a teleost with alternative male reproductive morphs

Species with dimorphic males typically have one morph (type I) associated with territoriality and courtship, and another morph (type II) associated with cuckoldry. In teleost fishes, type I males generally have higher levels of the androgen 11-ketotestosterone (KT) than type II males. Is KT causal to phenotypic differences between morphs? We investigated this question in the midshipman fish (Porichthys notatus) in which type I males have detectable levels of KT during the breeding season, whereas levels in type II males are usually undetectable. Type I midshipman will either cuckold or hold territories and court females, whereas type II males are only known to cuckold. Acoustic courtship by type I's is supported by the sonic motor nucleus, which innervates a sound-producing sonic muscle. Type I males have larger sonic motor nuclei and larger sonic muscles than type II males, consistent with the more dynamic vocal repertoire of type I's. Here, we tested whether intraperitoneal KT implants in adult type II males would induce type I male-like traits in brain, sonic muscle, and behavior. Type II's treated with KT did not differ from blank-implanted type II's in sonic motor nucleus volume. Sonic muscle mass increased in KT-implanted type II's, but did not reach the relative mass naturally observed in type I's. While neither territoriality nor courtship were induced, cuckoldry behavior intensified in KT-implanted type II's. Thus, for some but not all characters, KT exaggerated the expression of already existing type II male traits rather than inducing the type I male-like traits of territoriality, courtship, and an expansive vocal motor system.     

The influence of environmental quality on sexual selection in Nauphoeta cinerea (Dictyoptera: Blaberidae)

We examined the impact of environmental conditions on the sexpheromone and mating behavior of the cockroach, Nauphoeta cinerea.Previous research on this species has shown that female behaviorduring courtship reflects female mate choice, male behaviorcorrelates with male social status, and the male sex pheromoneis the character used by females to assess males. In the presentstudy, males and females were allowed to develop from adultemergence to sexual maturity in either a high- or low-qualityenvironment. The environment affected the quantities of sexpheromone components. We found significantly less 3-hydroxy-2-butanoneand 4-ethyl-2-methoxyphenol, but not 2-methylthiazolidine, inthe pheromone glands of males from a poor environment. Pheromonequality was also affected; the ratios involving 2-methylthiazolidinewere altered, while the ratio 3-hydroxy-2-butanone to 4-ethyl-2-methoxyphenoldid not change. Development to sexual maturity under these environmentalconditions also influenced male and female sexual behavior.Male courtship activity reflected environmental influences;males from the low-quality environment took longer to initiatecourtship and spent more time copulating with females from allenvironments. Male quality, as assessed by females, was alsoaffected by their environment. Females were slower to respondto the courtship of males from the poor environment, regardlessof the females' own rearing environments. However, females fromthe low-quality environment also took longer to respond to thecourtship, and required more courtship, regardless of the males'rearing environments. Thus, poor environments also increasefemale choosiness. However, there was only one significant interactionterm, suggesting that the environmental effects are generaland that females do not show adaptive plasticity in mate choice.Studies of sexual selection that consider the effects of variableenvironments on behavior as well as the sexually selected morphologyin other systems are likely to provide new insights into thisevolutionary process     

Androgen and behavior in the male three-spined stickleback,Gasterosteus aculeatus. II. Castration and 11-ketoandrostenedione effects on courtship and parental care during the nesting cycle

Courtship declines and ceases while parental care increases in the presence of developing eggs during the nesting cycle of the male three-spined stickleback, Gasterosteus aculeatus. Furthermore, circulating 11-ketotestosterone (11KT) levels are higher during the initial "courtship phase" than during the later "parental phase," similar to that found in other paternal fishes. This study aimed to investigate a possible functional relationship between changes in 11KT levels and changes in reproductive behavior during the nesting cycle. To this end, groups of nonspawned and spawned male sticklebacks were sham-operated, castrated, or castrated and treated with 11-ketoandrostenedione (11KA), and the effects of the treatments on courtship and parental care were studied. Castration removed circulating 11KT, while 11KA replacement prevented the natural decline in 11KT during the parental phase (11KA converts to 11KT extratesticularly), as assessed by radioimmunoassay. Regardless of treatment, parental care remained low and courtship was present in all nonspawned males, even at the end of the experiment. However, courtship did eventually decline in castrated nonspawned males compared to the other two nonspawned groups. In all treatments of spawned males there was a drastic decline in courtship and an increase in parental care. In castrated spawned males, however, the decline in courtship came earlier than in the other two spawned groups. 11KA treatment did not prevent the natural decline in courtship/increase in parental care in spawned males, indicating that the natural decline in 11KT is not responsible for the main portion of the rapid changes in these behaviors over the stickleback's nesting cycle. The limited effects of castration also exclude other gonadal hormones from being responsible for most of these changes.