Molecular mechanisms and evolutionary implications of social plasticity

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Publications

Dear enemies elicit lower androgen responses to territorial challenges than unfamiliar intruders in a cichlid fish

Publication . Aires, Rui F.; Oliveira, Gonçalo A.; Oliveira, Tânia Sofia Ferreira de; Ros, Albert F. H.; Oliveira, Rui Filipe

In many territorial species androgen hormones are known to increase in response to territorial intrusions as a way to adjust the expression of androgen-dependent behaviour to social challenges. The dear enemy effect has also been described in territorial species and posits that resident individuals show a more aggressive response to intrusions by strangers than by other territorial neighbours. Therefore, we hypothesized that the dear enemy effect may also modulate the androgen response to a territorial intrusion. Here we tested this hypothesis in male cichlid fish (Mozambique tilapia, Oreochromis mossambicus) using a paradigm of four repeated territorial intrusions, either by the same neighbour or by four different unfamiliar intruders. Neighbour intruders elicited lower aggression and a weaker androgen response than strangers on the first intrusion of the experiment. With repeated intrusions, the agonistic behaviour of the resident males against familiar intruders was similar to that displayed towards strangers. By the fourth intrusion the androgen response was significantly reduced and there was no longer a difference between the responses to the two types of intruders. These results suggest that the dear enemy effect modulates the androgen response to territorial intrusions and that repeated intrusions lead to a habituation of the androgen response.

2015Journal article

Open access

Brain transcriptomic response to social eavesdropping in zebrafish (Danio rerio)

Publication . Lopes, Joao Sollari; Abril-de-Abreu, Rodrigo; Oliveira, Rui Filipe

Public information is widely available at low cost to animals living in social groups. For instance, bystanders may eavesdrop on signaling interactions between conspecifics and use it to adapt their subsequent behavior towards the observed individuals. This social eavesdropping ability is expected to require specialized mechanisms such as social attention, which selects social information available for learning. To begin exploring the genetic basis of social eavesdropping, we used a previously established attention paradigm in the lab to study the brain gene expression profile of male zebrafish (Danio rerio) in relation to the attention they paid towards conspecifics involved or not involved in agonistic interactions. Microarray gene chips were used to characterize their brain transcriptomes based on differential expression of single genes and gene sets. These analyses were complemented by promoter regionbased techniques. Using data from both approaches, we further drafted protein interaction networks. Our results suggest that attentiveness towards conspecifics, whether interacting or not, activates pathways linked to neuronal plasticity and memory formation. The network analyses suggested that fos and jun are key players on this response, and that npas4a, nr4a1 and egr4 may also play an important role. Furthermore, specifically observing fighting interactions further triggered pathways associated to a change in the alertness status (dnajb5) and to other genes related to memory formation (btg2, npas4b), which suggests that the acquisition of eavesdropped information about social relationships activates specific processes on top of those already activated just by observing conspecifics.

2015Journal article

Open access

Quantifying aggressive behavior in zebrafish

Publication . Teles, Magda; Oliveira, Rui Filipe

Aggression is a complex behavior that influences social relationships and can be seen as adaptive or maladaptive depending on the context and intensity of expression. A model organism suitable for genetic dissection of the underlying neural mechanisms of aggressive behavior is still needed. Zebrafish has already proven to be a powerful vertebrate model organism for the study of normal and pathological brain function. Despite the fact that zebrafish is a gregarious species that forms shoals, when allowed to interact in pairs, both males and females express aggressive behavior and establish dominance hierarchies. Here, we describe two protocols that can be used to quantify aggressive behavior in zebrafish, using two different paradigms: (1) staged fights between real opponents and (2) mirror-elicited fights. We also discuss the methodology for the behavior analysis, the expected results for both paradigms, and the advantages and disadvantages of each paradigm in face of the specific goals of the study.

2016Book part

Restricted access

Social network predicts loss of fertilizations in nesting males of a fish with alternative reproductive tactics

Publication . Cardoso, Sara D.; Faustino, Ana Isabel Soares; Costa, Silvia S.; Valério, Fábio; Gonçalves, David; Oliveira, Rui Filipe

Alternative reproductive tactics (ARTs) evolve when there is strong intra-sexual competition between conspecifics for access to mates. Typically, larger Bbourgeois^ males reproduce by securing the access to reproductive resources while smaller Bparasitic^ males reproduce by stealing fertilizations from larger males. A number of factors can influence the reproductive success of each tactic, including intrinsic (e.g. size) and extrinsic (e.g. tactic relative frequency) variables. An example where plastic ARTs occur is the peacock blenny Salaria pavo, with large males reproducing by defending nests and attracting females (bourgeois tactic) and small males reproducing by achieving sneaked fertilizations (parasitic tactic). In this study, we conducted field observations on individually tagged animals to determine their social network and collected eggs from 11 nests to determine the fertilization success of each male tactic. Paternity estimates for 550 offspring indicated an average fertilization success for nest-holder males of 95%. Nest-holder male morphological traits and social network parameters were tested as predictors of fertilization success, but only the number of sneakers present in the nest-holder’s social networks was found to be a predictor of paternity loss. Although male morphological traits had been previously found to be strongly correlated with reproductive success of nest-holder males, as measured by the number of eggs collected in the male’s nest, no correlation was found between any of the measured morphological traits and fertilization success for these males. The results suggest a stronger influence of the social environment than of morphological variables in the proportion of lost fertilizations by nest-holder males of this species.

2016Journal article

Restricted access

Androgen modulation of social decision-making mechanisms in the brain : An integrative and embodied perspective

Publication . Oliveira, Gonçalo A.; Oliveira, Rui Filipe

Apart from their role in reproduction androgens also respond to social challenges and this response has been seen as a way to regulate the expression of behavior according to the perceived social environment (Challenge hypothesis, Wingfield et al., 1990). This hypothesis implies that social decision-making mechanisms localized in the central nervous system (CNS) are open to the influence of peripheral hormones that ultimately are under the control of the CNS through the hypothalamic-pituitary-gonadal axis. Therefore, two puzzling questions emerge at two different levels of biological analysis: (1) Why does the brain, which perceives the social environment and regulates androgen production in the gonad, need feedback information from the gonad to adjust its social decision-making processes? (2) How does the brain regulate gonadal androgen responses to social challenges and how do these feedback into the brain? In this paper, we will address these two questions using the integrative approach proposed by Niko Tinbergen, who proposed that a full understanding of behavior requires its analysis at both proximate (physiology, ontogeny) and ultimate (ecology, evolution) levels.

2014Journal article

Open access