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.     

Arginine vasotocin and androgen pathways are associated with mating system variation in North American cichlid fishes

Neuroendocrine pathways that regulate social behavior are remarkably conserved across divergent taxa. The neuropeptides arginine vasotocin/vasopressin (AVT/AVP) and their receptor V1a mediate aggression, space use, and mating behavior in male vertebrates. The hormone prolactin (PRL) also regulates social behavior across species, most notably paternal behavior. Both hormone systems may be involved in the evolution of monogamous mating systems. We compared AVT, AVT receptor V1a2, PRL, and PRL receptor PRLR1 gene expression in the brains as well as circulating androgen concentrations of free-living reproductively active males of two closely related North American cichlid species, the monogamous Herichthys cyanoguttatus and the polygynous Herichthys minckleyi. We found that H. cyanoguttatus males bond with a single female and together they cooperatively defend a small territory in which they reproduce. In H. minckleyi, a small number of large males defend large territories in which they mate with several females. Levels of V1a2 mRNA were higher in the hypothalamus of H. minckleyi, and PRLR1 expression was higher in the hypothalamus and telencephalon of H. minckleyi. 11-ketotestosterone levels were higher in H. minckleyi, while testosterone levels were higher in H. cyanoguttatus. Our results indicate that a highly active AVT/V1a2 circuit(s) in the brain is associated with space use and social dominance and that pair bonding is mediated either by a different, less active AVT/V1a2 circuit or by another neuroendocrine system.     

Arginine vasotocin activates advertisement calling and movement in the territorial Puerto Rican frog, Eleutherodactylus coqui

Arginine vasotocin (AVT) is a neuropeptide that modulates social behavior in amphibians and activates calling in frogs. The Puerto Rican coqui frog, Eleutherodactylus coqui, is a terrestrial anuran that exhibits complex social behaviors, including territoriality and paternal care. Males have a distinctive social hierarchy and can be any of the following: satellite (non-calling), territorial (calling), or paternal (guards and broods embryos). Field experiments were conducted to determine the effects of AVT on satellite behavior and the male social hierarchy of E. coqui. Satellite males were captured within the territory held by a resident male, given injections (i.p.) of AVT or saline (control) and placed back in their original location. To determine if AVT affects all males, not merely satellite males, territorial (calling) males were injected with AVT. Significantly more satellite males commenced advertisement calling following AVT injections than did control males injected with saline. AVT-activated satellites did not challenge the resident territorial male for possession of the territory but instead moved into a new area before commencing to call. In fact, AVT-activated satellite males were significantly more likely to move into a new territory following AVT injections than AVT-injected territorial males. The effect of AVT was short lived, lasting only one night in all but two cases. It is concluded that AVT stimulates advertisement calling and AVT-activated males displayed territorial characteristics of E. coqui.     

Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals

The neuropeptide arginine vasopressin (AVP) influences many social behaviors through its action in the forebrain of mammals. However, the function of the homologous arginine vasotocin (AVT) in the forebrain of fishes, specifically the telencephalon remains unresolved. We tested whether the density of AVT-immunoreactive (-ir) fiber varicosities, somata size or number of AVT-ir neuronal phenotypes within the forebrain were predictive of social behavior in reproductive males of seven species of butterflyfishes (family Chaetodontidae) in four phylogenetic clades. Similar to other fishes, the aggressive (often territorial) species in most cases had larger AVT-ir cells within the gigantocellular preoptic cell group. Linear discriminant function analyses demonstrated that the density of AVT-ir varicosities within homologous telencephalic nuclei to those important for social behavior in mammals and birds were predictive of aggressive behavior, social affiliations, and mating system. Of note, the density of AVT-ir varicosities within the ventral nucleus of the ventral telencephalon, thought to be homologous to the septum of other vertebrates, was the strongest predictor of aggressive behavior, social affiliation, and mating system. These results are consistent with the postulate that AVT within the telencephalon of fishes plays an important role in social behavior and may function in a similar manner to that of AVT / AVP in birds and mammals despite having cell populations solely within the preoptic area.     

The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network

Neuropeptides in the arginine vasotocin/arginine vasopressin (AVT/AVP) family play a major role in the regulation of social behavior by their actions in the brain. In mammals, AVP is found within a circuit of recriprocally connected limbic structures that form the social behavior neural network. This review examines the role played by AVP within this network in controlling social processes that are critical for the formation and maintenance of social relationships: social recognition, social communication and aggression. Studies in a number of mammalian species indicate that AVP and AVP V1a receptors are ideally suited to regulate the expression of social processes because of their plasticity in response to factors that influence social behavior. The pattern of AVP innervation and V1a receptors across the social behavior neural network may determine the potential range and intensity of social responses that individuals display in different social situations. Although fundamental information on how social behavior is wired in the brain is still lacking, it is clear that different social behaviors can be influenced by the actions of AVP in the same region of the network and that AVP can act within multiple regions of this network to regulate the expression of individual social behaviors. The existing data suggest that AVP can influence social behavior by modulating the interpretation of sensory information, by influencing decision making and by triggering complex motor outputs. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Do Feeding Resources Induce the Adoption of Resource Defence Polygyny in a Lekking Butterfly?

Among polygynous species, males often compete for the possession of mating sites to increase their reproductive success. Weaker individuals frequently adopt alternative non‐territorial mate‐locating tactics, but the adoption of alternative territorial tactics may also occur. Although alternative tactics with territory defence are less common in arthropods, factors that drive its adoption may provide information to understand the organization of different territorial mating systems in the group. Here we investigate the adoption of resource‐based territoriality as an alternative to a non‐resource‐based one by males of the butterfly Paryphthimoides phronius. Male P. phronius commonly defend sunny clearings lacking feeding resources in the forest edge (non‐resource‐based territoriality). However, after experimentally offering fermenting fruit in previously undefended sites, we showed that males also adopt a resource defence tactic. Males in territories with fermenting fruits apparently feed on this resource when they are not defending the territory. However, males in sites without resources did not migrate to territories with resources when given the opportunity. To our knowledge, this is the first experimental investigation to show a non‐resource‐ and an alternative resource‐based mate‐locating tactic in a butterfly. We suggest that this behavioural flexibility may represent an important step to understand the ecological factors responsible for the organization and evolution of different territorial mating systems in insects.     

The Haremic Mating System and Mate Choice in the Wide-Eyed Flounder, Bothus podas

The social structure and reproductive behaviour of the wide-eyed flounder, Bothus podas, was studied in the coastal waters around the Azorean Islands. Both sexes are territorial throughout the year. Adult males defend large territories, which include several smaller female territories. Intraspecific agonistic behaviour was frequent and differed between sexes: males were more aggressive towards other males, while females were only aggressive towards each other and juveniles. During the reproductive season and only at dawn, territorial males court and mate successively with females in their territories, and females seem to show mating fidelity to their dominant male. Such territoriality and mating patterns indicate a haremic social system in the wide-eyed flounder. In order to identify potential factors influencing female mate choice acting on this haremic system, we examined male mating success and some of its potential correlates. We found no evidence for female preference for any of the males' physical or territory characteristics. However, courtship effort was strongly correlated with the total number of attempted and successful spawnings, indicating that females seem to mate preferentially with males that court them more vigorously. Thus, our data suggest that courtship plays an important role in determining male mating success in the wide-eyed flounder and, that it may possibly serve as an honest indicator of male `quality' for female choice.     

Territory defence in male European roe deer (Capreolus capreolus)—a sexual ornament?

The function of male territoriality in roe deer has been debated for decades. There now seems to be consensus that it is a mating tactic. As such, it is highly untypical though. The reasons being, first, males neither conform to the typical ‘resource defence’ territoriality model nor to the ‘mate defence’ territoriality model; second, territory defence commences several months in advance of the breeding season; and third, the territorial system seems to be very rigid, as practically all studies that have described the social organisation of the species have reported adult males to be territorial. In spite of the general agreement that territoriality is a mating tactic, conclusive evidence on which selective forces are responsible for the prevalent pattern is still lacking. In the present paper, it is suggested that territorial defence serves as a sexual ornament, i.e. ‘cleanness’ of other males on the territory, in combination with size of the ‘clean’ area, and tenure length are parameters used by females to estimate male phenotypic quality. The hypothesis generates at least four predictions, and available data provide support. It is concluded that although a firm test of the hypothesis remains to be undertaken, existing data support this, just as well as any other, explanatory model and therefore it should be taken into consideration.     

Butterflyfish social behaviour,with special reference to the incidence of territoriality: a review

Synopsis Butterflyfishes (Chaetodontidae) are among the best studied of coral reef fishes. Feeding ecology and some aspects of behaviour have been firmly established. However, spacing behaviour remains controversial. Two major studies made in the 1970s concluded that the majority of species were not territorial. We suggest that these and other studies which have concluded that territories are not held have generally suffered from short observation periods, and have not mapped the ranges occupied by individuals. Further, low frequencies of agonistic behaviour have been interpreted as evidence of non-territoriality. By contrast, studies which have proven territoriality have had long observation periods and have mapped ranges. These have shown that territories are usually maintained with very little overt aggression. Spacing behaviour and feeding behaviour are clearly linked, with territoriality common among benthic-feeding species, especially obligate corallivores. Species with broad dietary flexibility tend to have flexible social systems, while plankton feeders are usually gregarious. The widespread occurrence of monogamy in butterflyfishes appears linked to territoriality, the majority of territorial species identified to date occurring predominantly as pairs. Data currently available suggest that this is because pair defence of the territory is more efficient than by individuals. However, several alternative hypotheses for the evolution of monogamy based on spawning constraints and predation risk cannot yet be ruled out.     

Differences in size and energy content affect the territorial status and mating success of a neotropical dragonfly

In male odonates, both size and fat content are related to territory defence and mating success. Males that are larger and have higher energy reserves win relatively more disputes for territory and attract more females. Wing colour has also been regarded as a mechanism that influences agonistic behaviour between males, as wing pigmentation might be regarded as a sign of male quality. In this study, we analysed whether a set of male physical (body size and wing colour), physiological (body fat content) and behavioural (disputes between males) characteristics were involved in the territory defence and mating behaviour of the neotropical dragonfly Zenithoptera lanei Santos, 1941 (Anisoptera: Libellulidae). Males were characterised as territorial whenever they warded‐off other males and remained in the same place within the pond for two consecutive days. In general, these territorial males were larger and had more abdominal and thoracic fat, engaged in pursuits more frequently, spent more time on sexual behaviour and female guarding, and mated more in comparison to subordinate males. By evaluating whether the percentage of wing area covered by black ink influenced male behaviour, we found that territorial males tended to act aggressively towards other males whose wings were partially painted, and sexually towards females irrespective of wing area painted. In Z. lanei, both body size and fat content play a role in defining territoriality. By subduing competitors and dominating preferred locations within high‐quality sites, these males are likely to be visited by females and engage in mating.     

Why are Male Columbian Ground Squirrels Territorial?

Male territorial defence is a component of many vertebrate mating systems and is often regarded as a tactic for acquiring mates. Traditionally considered within the context of overt site‐specific defence, territoriality actually may have several components which encompass a variety of behavioural tactics (e.g. post‐copulatory mate‐guarding, defence of resources that females need, defence of area around females) that underlie a mating system. The purpose of our study was to evaluate such influences on the territorial behaviour of male Columbian ground squirrels in southwestern Alberta, Canada. Males were dominant and territorial if they defended a minimum convex polygon activity range by chasing other males more within the activity range than they were chased. Subordinate males had no territory and were chased throughout their ranges, but they competed for mates by increasing chases in their activity range when nearby females were oestrous. Dominant males exhibited conditional breeding tactics, tending to chase other dominant males from their territory when nearby females were oestrous, but travelling outside their activity ranges to chase subordinate males when females were not oestrous. Although females mated first with a dominant male on whose territory they resided (and in order from oldest to youngest if several territories overlapped), mating pairs were not exclusive, as females usually mated with additional males. Males also guarded females after copulation and defended females directly just before oestrus, rather than defending territory per se during those times. Thus, males possess a repertoire of behaviours that complement site‐specific territoriality, and territory ownership serves to facilitate a first mating with females that live on the territory.     

BEHAVIORAL CONVERGENCE AND ADAPTIVE RADIATION: EFFECTS OF HABITAT USE ON TERRITORIAL BEHAVIOR IN ANOLIS LIZARDS

Most studies of adaptive radiations focus on morphological aspects of differentiation, yet behavior is also an important component of evolutionary diversification, often mediating the relationship between animal ecology and morphology. In species within radiations that are convergent in ecology and morphology, we then also expect convergence in behavior. Here, we examined 13 Anolis lizard species to determine whether territorial strategies have evolved convergently with morphology and habitat use. We evaluated two aspects of territoriality: behavioral defense of space via territorial displays, and territory overlap within and between sexes. Controlling for the phylogenetic relationships of the taxa in our study, we found that species similar in perch height and diameter convergently evolved patterns of territory overlap, whereas species similar in habitat visibility (the proportion of space that can be seen from a perch) convergently evolved display behavior. We also found that species with greater display time have more extensive male–male territory overlap. This study provides strong evidence for the role of habitat in the evolution of territoriality and suggests that the social structure of a species ultimately evolves in concert with habitat use and morphology.     

Arginine vasotocin regulation of interspecific cooperative behaviour in a cleaner fish

In an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.     

Group size correlates with territory size in European badgers: implications for the resource dispersion hypothesis?

The resource dispersion hypothesis (RDH) predicts that resource heterogeneity can act as a passive cause of group‐living in social carnivores and potentially many other species. One central prediction of the RDH is that territory size and group size are not related, as they are determined by resource dispersion and quality, respectively. In this study we investigated the relationship between territory size, group size and group composition in the European badger, a non‐cooperative social mustelid whose behavioural ecology was central to the development of the RDH. Using data from a long‐term study in the UK, we found that territory size and group size were positively related, contradicting a core prediction of the RDH. Furthermore, territory size was more strongly correlated with the number of adult males in the group than to the number of females or total group size. This result suggests that male badgers may have a more important role in territoriality and receive greater benefits from territory enlargement. These findings are consistent with the predictions of the anti‐kleptogamy hypothesis, and suggest that badger territorial and social behaviour is not purely driven by resource dispersion, but may also be associated with breeding behaviour, as in other mustelids.     

Multiple mechanisms of phenotype development in the bluehead wrasse

Despite having detailed information on mechanisms mediating sex-typical behavior in many species, we have little understanding of whether the same mechanisms regulate these behaviors when they are performed in the same species under different social contexts. In the five field experiments of this study of bluehead wrasses (Thalassoma bifasciatum), a sex-changing fish, we examined the roles of arginine vasotocin (AVT) and the potent teleost androgen 11-ketotestosterone (11KT) in mediating sexual and aggressive behaviors typical of dominant males. We demonstrated that AVT appears necessary for the assumption of dominant territorial status in males and females, but is sufficient only in the socially dominant terminal phase (TP) male phenotype. Specifically, an AVP V(1) receptor antagonist prevented both TP males and females from gaining dominance over recently vacated territories. However, unlike TP males in a previous study, neither females nor initial phase males responded to AVT treatment with increases in display of TP male typical behaviors when under social conditions that inhibit sex change. Treating females with 11KT did not alter responsiveness to AVT, but did induce male coloration and courtship behavior that was not observed in oil-treated females. Combined with the results of a previous study, these results indicate that the ability of AVT to induce male-typical behavior differs among sexual phenotypes and that this differential responsiveness appears to be dependent on social context and not directly on exposure to 11KT. Furthermore, since 11KT can induce courtship behavior in females that is not affected by AVT, there may be different hormonal mechanisms mediating courtship behavior under different social contexts.     

Impact of season and social challenge on testosterone and corticosterone levels in a year-round territorial bird

Plasma testosterone increases during breeding in many male vertebrates and has long been implicated in the promotion of aggressive behaviors relating to territory and mate defense. Males of some species also defend territories outside of the breeding period. For example, the European nuthatch (Sitta europaea) defends an all-purpose territory throughout the year. To contribute to the growing literature regarding the hormonal correlates of non-breeding territoriality, we investigated the seasonal testosterone and corticosterone profile of male (and female) nuthatches and determined how observed hormone patterns relate to expression of territorial aggression. Given that non-breeding territoriality in the nuthatch relates to the reproductive context (i.e., defense of a future breeding site), we predicted that males would exhibit surges in plasma testosterone throughout the year. However, we found that males showed elevated testosterone levels only during breeding. Thus, testosterone of gonadal origin does not appear to be involved in the expression of non-breeding territoriality. Interestingly, territorial behaviors of male nuthatches were stronger in spring than in autumn, suggesting that in year-round territorial species, breeding-related testosterone elevations may upregulate male-male aggression above non-breeding levels. In females, plasma testosterone was largely undetectable. We also examined effects of simulated territorial intrusions (STIs) on testosterone and corticosterone levels of breeding males. We found that STIs did not elicit a testosterone response, but caused a dramatic increase in plasma corticosterone. These data support the hypothesis that corticosterone rather than testosterone may play a role in the support of behavior and/or physiology during acute territorial encounters in single-brooded species.     

Multiple routes to interspecific territoriality in sister species of North American perching birds

Behavioral interference between species can influence a wide range of ecological and evolutionary processes. Here, we test foundational hypotheses regarding the origins and maintenance of interspecific territoriality, and evaluate the role of interspecific territoriality and hybridization in shaping species distributions and transitions from parapatry to sympatry in sister species of North American perching birds (Passeriformes). We find that interspecific territoriality is pervasive among sympatric sister species pairs, and that interspecifically territorial species pairs have diverged more recently than sympatric noninterspecifically territorial pairs. None of the foundational hypotheses alone explains the observed patterns of interspecific territoriality, but our results support the idea that some cases of interspecific territoriality arise from misdirected intraspecific aggression while others are evolved responses to resource competition. The combination of interspecific territoriality and hybridization appears to be an unstable state associated with parapatry, whereas species that are interspecifically territorial and do not hybridize are able to achieve extensive fine- and coarse-scale breeding range overlap. In sum, these results suggest that interspecific territoriality has multiple origins and impacts coexistence at multiple spatial scales.     

Influences on variation in territorial tenures of male white-faced dragonflies (Leucorrhinia intacta) (Odonata: Libellulidae)

Some individuals in species with extended periods of territorial occupancy may change territory locations within a single bout of territorial activity. Length of occupancy of mating territories among males in a local population of white-faced dragonflies (Leucorrhinia intacta) varied from more than 6 h to 15 min or less. Males with short tenures often established territories in several locations on the pond during a day. Several hypotheses have been proposed to explain shifting territorial sites rather than remaining in a single site during one bout of territoriality. We attempted to test the hypothesis that males shift to leave low-quality sites. Site quality may be affected by costs of defense in relation to intruder rate and the mating benefits of holding the territory. To test whether variation in these possible effects of benefits and costs of territoriality influenced tenure, we manipulated local quality of oviposition substrate and perch density. The quality of oviposition substrate, but not perch density, influenced both potential benefits and costs of territoriality. Female density was higher in areas with good substrate, but so were rates of males intruding into the territories, rates of chasing by territorial males, and local density of territorial males. More matings occurred in areas with good substrate, but among males with tenures of 15 min or more, mating success per male and tenure lengths did not differ statistically among treatments. Defense costs were low for all treatments and perhaps were not an important influence on tenure duration. Territorial males in this population probably adjusted local density to expected mating success by initial choice of site rather than by varying tenure length. Variation in tenure length at a site resulted, in part, from stochastic external factors, such as predation attempts.