Project/scholarship details


According to classic evolutionary theory nonheritable phenotypic variation would seem to be irrelevant to evolutionary change, since adaptation by natural selection rather depends on heritable phenotypic variation produced by genetic variation. However, when the rate of genetic evolutionary change is outpaced by changes in the environment the need for adaptive change without genetic mutation emerges. In this scenario, the evolution of phenotypic plasticity is favored according to which environmental cues sensed by the organism lead the same genotype to produce different phenotypes depending on environmental conditions (i.e. reaction norm). Thus, despite the fact that the contribution of nonheritable phenotypic variation to evolutionary change appears to be a paradox, the evolution of mechanisms that generate it can be a common evolutionary phenomenon. Different traits show different evolutionary changes in plasticity, both in terms of the time lag to respond to the environmental cue and of the magnitude of the response. Among animals, behavioral traits exhibit both more rapid and stronger plasticity than morphological traits, which makes behavioral plasticity a key adaptive response to changing environmental conditions. At the proximate level behavioral plasticity depends on the development of a central nervous system which allows for rapid and integrated organismal responses in order to maintain homeostasis (or allostasis). Many of these responses are simple reflexes and fixed action patterns elicited by a stimulus in the environment, when it determinately predicts an appropriate response. However, when environmental complexity and ambiguity increases, the capacity to adaptively modify behavior, as a function of experience (learning) and context, is needed. One of the most ambiguous components of the environment is the social domain, since it is made of other behavioral agents with an inherent level of unpredictability of their actions, with whom the individual needs to interact. Hence, the ability of animals to regulate the expression of social behavior, as to adapt their behavioral output to specific situations in a complex and variable social world, is expected to depend on the evolution of plastic responses. These allow the same genotype to produce different behavioral phenotypes (social plasticity), rather than to genetically determine rules controlling fixed responses. Thus, social plasticity should be viewed as a key ecological performance trait that impacts Darwinian fitness. Here we propose an integrative framework for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behavior in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different neurogenomic states correspond to different behavioral responses and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. At the evolutionary scale social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. However, when social plasticity is too costly or incomplete, behavioral consistency (behavioral syndromes) can emerge by directional selection which recruits gene modules corresponding to favored behavioral states in that environment. In this project we will address the following questions (Q): Q1. What are the mechanisms animals use for sensing and responding adaptively to specific environmental cues that trigger plastic responses? Q2. How can the same genome produce different social phenotypes in response to cues provided by the ecological and social environment? Q3. Is plasticity itself subject to selection and might therefore evolve? Q4. Have the mechanisms underlying plasticity in social behavior been co-opted to regulate plasticity in inter-specific interactions, among species with complex inter-specific relationships (e.g. mutualisms)? The choice of fish as study models is justified by the fact that teleosts are the most diverse and plastic taxa among vertebrates. Following Krogh’s principle, we have chosen what we considered to be the species of choice to most conveniently study each of these questions (Q1: zebrafish, tilapia; Q2: peacock blenny; Q3: zebrafish; Q4: cleaner wrasse). As a result of this project we expect to show how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences, therefore highlighting the fact that proximate mechanisms of nonheritable phenotypic variation contribute to the dynamics of selection.

  • Funder

    FCT - Fundação para a Ciência e a Tecnologia, I.P.

  • Funder's country

    Portugal

  • Funding program

    3599-PPCDT

  • Funding amount

    310,000.00 €

  • Start date

    Sat Jun 01 00:00:00 WEST 2013

  • End date

    Tue May 31 00:00:00 WEST 2016

  • Date awarded

    Tue Mar 12 00:00:00 WET 2013

Documents


Androgen response to social competition in a shoaling fish

Teles, Magda; Oliveira, Rui Filipe

Androgens respond to social challenges and this response has been interpreted as a way for males to adjust androgen-dependent behavior to social context. However, the androgen responsiveness to social challenges varies across species and a conceptual framework has been developed to explain this variation according to differences in the mating system and parental care type, which determines the regimen of challe...


Assessment of fight outcome is needed to activate socially driven transcription...

Oliveira, Rui Filipe; Simões, José Miguel; Teles, Magda; Oliveira, Catarina R.; Becker, Jorg D.; Lopes, João Sollari

Group living animals must be able to express different behavior profiles depending on their social status. Therefore, the same genotype may translate into different behavioral phenotypes through socially driven differential gene expression. However, how social information is translated into a neurogenomic response and what are the specific cues in a social interaction that signal a change in social status are q...


Agonistic interactions elicit rapid changes in brain nonapeptide levels in zebr...

Teles, Magda; Gozdowska, Magdalena; Kalamarz-Kubiak, Hanna; Kulczykowska, Ewa; Oliveira, Rui Filipe

The teleost fish nonapeptides, arginine vasotocin (AVT) and isotocin (IT), have been implicated in the regulation of social behavior. These peptides are expected to be involved in acute and transient changes in social context, in order to be efficient in modulating the expression of social behavior according to changes in the social environment. Here we tested the hypothesis that short-term social interactions ...


Social buffering of fear in zebrafish

Faustino, Ana Isabel Soares

A ubiquidade da formação de grupos em animais tem sido explicada, entre outros aspectos, pelos seus benefícios na proteção contra predadores, nomeadamente devido ao aumento global do estado de vigilância, diluição do risco e capacidade de confundir o predador. Assim, os grupos sociais proporcionam um ambiente mais seguro na presença de ameaças, onde a presença de conspecíficos diminui o medo desencadeado por ev...


Quantifying aggressive behavior in zebrafish

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 fun...


Social network predicts loss of fertilizations in nesting males of a fish with ...

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 (...


Social Plasticity Relies on Different Neuroplasticity Mechanisms across the Bra...

Teles, Magda C.; Cardoso, Sara D.; Oliveira, Rui F.

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 ci...


Mechanisms of social buffering of fear in zebrafish

Faustino, Ana Isabel Soares; Tacão-Monteiro, André; Oliveira, Rui Filipe

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 expo...


Audience effects in territorial defense of male cichlid fish are associated wit...

Roleira, António; Oliveira, Gonçalo A.; Lopes, João Sollari; Oliveira, Rui Filipe

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 pr...


Temporal variation in brain transcriptome is associated with the expression of ...

Cardoso, Sara D.; Gonçalves, David; Goesmann, Alexander; Canário, Adelino V. M.; Oliveira, Rui Filipe

Distinct patterns of gene expression often underlie intra- and inter-sexual differences, and the study of this set of co-regulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behav...

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