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.

• Project/scholarship ID

  129982

• Reference

  EXCL/BIA-ANM/0549/2012

• FundRef URI

  http://www.fct.pt/apoios/projectos/consulta/vglobal_projecto.phtml.en?idProjecto=129982&idElemConcurso=7286

• 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

  2013-06-01

• End date

  2016-08-31