Expanding the concept of social behavior to interspecific interactions

In pretty much any species, an individual's survival and reproduction depends crucially on the outcome of interactions with other individuals. Key interactions may take place between individuals of the same species but also between individuals belonging to different species. However, the most accepted definition of social behavior only considers interactions between conspecifics. Here, we argue that the distinction between intra- and interspecific interactions is largely artificial and hinders the integration of the historically separately developed concepts. At the ultimate level, given that the ecological landscape of organisms is composed both by interactions with conspecifics and with heterospecifics, and both types of interactions may have evolutionary consequences. Although intraspecific interactions usually have a higher impact in fitness because in most species interactions relevant for reproduction (mating, parenting) exclusively involve conspecifics, and interactions relevant for survival are more probable between conspecifics because they share the same ecological niche, hence competing for the same resources (e.g., food, shelter), there are notable exceptions in both fitness components (e.g., heterospecific mating in parthenogenic all-female species; heterospecific brood parasitism; heterospecific aggression in sympatric species that compete for shared resources). At the proximate level, behaviors and cognitive decision-making rules used to interact with other organisms may be shared between intra- and interspecific interactions, and the mechanistic differences between conspecific social behaviors used in distinct functional domains, such as mating, aggression, or parenting, can be more expressive than those found within the same functional domain between conspecific and heterospecific behavior. Therefore, there are neither fundamental conceptual (ultimate) reasons, nor key differences in mechanisms underlying behaviors involved in conspecific vs. heterospecific interactions that support the exclusion of interspecific interactions from the conceptual framework of social behaviorFundação para a Ciência e Tecnologia - FCTinfo:eu-repo/semantics/publishedVersio

Linking appraisal to behavioral flexibility in animals: implications for stress research

In fluctuating environments, organisms require mechanisms enabling the rapid expression of context-dependent behaviors. Here, we approach behavioral flexibility from a perspective rooted in appraisal theory, aiming to provide a better understanding on how animals adjust their internal state to environmental context. Appraisal has been defined as a multi-component and interactive process between the individual and the environment, in which the individual must evaluate the significance of a stimulus to generate an adaptive response. Within this framework, we review and reframe the existing evidence for the appraisal components in animal literature, in an attempt to reveal the common ground of appraisal mechanisms between species. Furthermore, cognitive biases may occur in the appraisal of ambiguous stimuli. These biases may be interpreted either as states open to environmental modulation or as long-lasting phenotypic traits. Finally, we discuss the implications of cognitive bias for stress research.FCT Ph.D. fellowships: (SFRH/BD/79087/2011, SFRH/BD/68528/2010), FCT strategic grant: (PEst-OE/MAR/UI0331/2011)

Nemo through the looking-glass: a commentary on Desjardins & Fernald

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Interaction between vasotocin and gonadal hormones in the regulation of reproductive behavior in a cichlid fish

Vasotocin (VT) has been associated with the regulation of diferent aspects of social behavior (e.g., mating and aggression). Given the fact that androgens are also known to regulate reproductive behavior, we hypothesized that VT and androgens could be interacting, rather than acting independently, in the regulation of reproductive behavior. In the present study, we aimed to understand the efect of VT and its interaction with gonadal hormones (putatively androgens) on diferent aspects of reproductive behavior of a polygynous and territorial cichlid fsh, the Mozambique tilapia (Oreochromis mossambicus). Using a within-subject design, we treated territorial males, that were previously castrated or sham-operated, with diferent dosages of VT as well as with a V1A receptor antagonist (Manning compound) and subsequently analyzed their behavior towards females and towards an intruder male. Our results showed that VT afected the behavior of territorial males towards females but not towards males. Specifcally, VT-treated males interacted less with females (i.e., spent less time touching the transparent partition that allowed visual contact with females) and were less aggressive towards females than salinetreated males. Moreover, in sham-operated males, blocking V1A receptors increased the frequency of bites towards females in comparison to saline-treated males, but not in castrated males. This result suggests that VT down-regulates aggressiveness towards females through the action of V1A receptors in the gonads (putatively decreasing androgen secretion), and that androgens up-regulate this behavior. In summary, our results suggest that VT may modulate social behavior, through an interaction with gonadal hormones.Fundação para a Ciência e Tecnologia - FCTinfo:eu-repo/semantics/publishedVersio

Audience Effects in Territorial Defense of Male Cichlid Fish Are Associated with Differential Patterns of Activation of the Brain Social Decision-Making Network

Animals communicate by exchanging signals frequently in the proximity of other conspecifics that may detect and intercept signals not directed to them. There is evidence that the presence of these bystanders modulates the signaling behavior of interacting individuals, a phenomenon that has been named audience effect. Research on the audience effect has predominantly focused on its function rather than on its proximate mechanisms. Here, we have investigated the physiological and neuromolecular correlates of the audience effect in a cichlid fish (Mozambique tilapia, Oreochromis mossambicus). A male was exposed to a territorial intrusion in the presence or absence of a female audience. Results showed that the presence of the female audience increased territorial defense, but elicited a lower androgen and cortisol response to the territorial intrusion. Furthermore, analysis of the expression of immediate early genes, used as markers of neuronal activity, in brain areas belonging to the social decision-making network (SDMN) revealed different patterns of network activity and connectivity across the different social contexts (i.e., audience × intrusion). Overall, these results suggest that socially driven plasticity in the expression of territorial behavior is accommodated in the central nervous system by rapid changes in functional connectivity between nodes of relevant networks (SDMN) rather than by localized changes of activity in specific brain nuclei

Social Plasticity Relies on Different Neuroplasticity Mechanisms across the Brain Social Decision-Making Network in Zebrafish

Social living animals need to adjust the expression of their behavior to their status within the group and to changes in social context and this ability (social plasticity) has an impact on their Darwinian fitness. At the proximate level social plasticity must rely on neuroplasticity in the brain social decision-making network (SDMN) that underlies the expression of social behavior, such that the same neural circuit may underlie the expression of different behaviors depending on social context. Here we tested this hypothesis in zebrafish by characterizing the gene expression response in the SDMN to changes in social status of a set of genes involved in different types of neural plasticity: bdnf, involved in changes in synaptic strength; npas4, involved in contextual learning and dependent establishment of GABAergic synapses; neuroligins (nlgn1 and nlgn2) as synaptogenesis markers; and genes involved in adult neurogenesis (wnt3 and neurod). Four social phenotypes were experimentally induced: Winners and Losers of a real-opponent interaction; Mirror-fighters, that fight their own image in a mirror and thus do not experience a change in social status despite the expression of aggressive behavior; and non-interacting fish, which were used as a reference group. Our results show that each social phenotype (i.e., Winners, Losers, and Mirror-fighters) present specific patterns of gene expression across the SDMN, and that different neuroplasticity genes are differentially expressed in different nodes of the network (e.g., BDNF in the dorsolateral telencephalon, which is a putative teleost homolog of the mammalian hippocampus). Winners expressed unique patterns of gene co-expression across the SDMN, whereas in Losers and Mirror-fighters the co-expression patterns were similar in the dorsal regions of the telencephalon and in the supracommissural nucleus of the ventral telencephalic area, but differents in the remaining regions of the ventral telencephalon. These results indicate that social plasticity relies on multiple neuroplasticity mechanisms across the SDMN, and that there is not a single neuromolecular module underlying this type of behavioral flexibility.FCT fellowships: (SFRH/BD/44848/2008, SFRH/BD/89072/2012)

Threat perception and familiarity moderate the androgen response to competition in women

Social interactions elicit androgen responses whose function has been posited to be the adjustment of androgen-dependent behaviors to social context. The activation of this androgen response is known to be mediated and moderated by psychological factors. In this study we tested the hypothesis that the testosterone (T) changes after a competition are not simply related to its outcome, but rather to the way the subject evaluates the event. In particular we tested two evaluative dimensions of a social interaction: familiarity with the opponent and the subjective evaluation of the outcome as threat or challenge. Challenge/threat occurs in goal relevant situations and represent different motivational states arising from the individuals' subjective evaluation of the interplay between the task demands and coping resources possessed. For challenge the coping resources exceed the task demands, while threat represents a state where coping resources are insufficient to meet the task demands. In this experiment women competed in pairs, against a same sex opponent using the number tracking test as a competitive task. Losers appraised the competition outcome as more threatening than winners, and displayed higher post-competition T levels than winners. No differences were found either for cortisol (C) or for dehydroepiandrosterone. Threat, familiarity with the opponent and T response were associated only in the loser condition. Moderation analysis suggests that for the women that lost the competition the effect of threat on T is moderated by familiarity with the opponent.FCT grant: (RG-LVT-331-2352), FCT PhD fellowship (SFRH/BD/68528/2010)

Social Eavesdropping in Zebrafish: Tuning of Attention to Social Interactions

Group living animals may eavesdrop on signalling interactions between conspecifics in order to collect adaptively relevant information obtained from others, without incurring in the costs of first-hand information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment. These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning. Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics. Our results show that zebrafish are more attentive towards interacting (i.e. fighting) than towards non-interacting pairs of conspecifics, with the exposure to fighting not increasing activity or stress levels. Moreover, using video playbacks to manipulate form features of the fighting fish, we show that during the assessment phase of the fight, bystanders' attention is more driven by form features of the interacting opponents; whereas during the post-resolution phase, it is driven by biological movement features of the dominant fish chasing the subordinate fish.FCT fellowship: (SFRH/BD/33280/2007), Champalimaud Neuroscience Programme

Mechanisms of social buffering of fear in zebrafish

The supplementary materials such the videos, are not present in the deposit due to incompatibilty of the extension of the files with the repository.Some humans thrive whereas others resign when exposed to threatening situations throughout life. Social support has been identified as an important modulator of these discrepancies in human behaviour, and other social animals also exhibit phenomena in which individuals recover better from aversive events when conspecifics are present - aka social buffering. Here we studied social buffering in zebrafish, by exposing focal fish to an aversive stimulus (alarm substance - AS) either in the absence or presence of conspecific cues. When exposed to AS in the presence of both olfactory (shoal water) and visual (sight of shoal) conspecific cues, focal fish exhibited a lower fear response than when tested alone, demonstrating social buffering in zebrafish. When separately testing each cue's effectiveness, we verified that the visual cue was more effective than the olfactory in reducing freezing in a persistent threat scenario. Finally, we verified that social buffering was independent of shoal size and coincided with a distinct pattern of co-activation of brain regions known to be involved in mammalian social buffering. Thus, this study suggests a shared evolutionary origin for social buffering in vertebrates, bringing new evidence on the behavioural, sensory and neural mechanisms underlying this phenomenon.info:eu-repo/semantics/publishedVersio