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Journal ArticleDOI

Rapid behavioral and genomic responses to social opportunity.

18 Oct 2005-PLOS Biology (Public Library of Science)-Vol. 3, Iss: 11, pp 1996-2004
TL;DR: It is shown for the first time that subordinate males can become dominant within minutes of an opportunity to do so, displaying dramatic changes in body coloration and behavior and induction of egr-1 in the anterior preoptic area by social opportunity could be an early trigger in the molecular cascade that culminates in enhanced fertility and other long-term physiological changes associated with dominance.
Abstract: From primates to bees, social status regulates reproduction. In the cichlid fish Astatotilapia (Haplochromis) burtoni, subordinate males have reduced fertility and must become dominant to reproduce. This increase in sexual capacity is orchestrated by neurons in the preoptic area, which enlarge in response to dominance and increase expression of gonadotropin-releasing hormone 1 (GnRH1), a peptide critical for reproduction. Using a novel behavioral paradigm, we show for the first time that subordinate males can become dominant within minutes of an opportunity to do so, displaying dramatic changes in body coloration and behavior. We also found that social opportunity induced expression of the immediate-early gene egr-1 in the anterior preoptic area, peaking in regions with high densities of GnRH1 neurons, and not in brain regions that express the related peptides GnRH2 and GnRH3. This genomic response did not occur in stable subordinate or stable dominant males even though stable dominants, like ascending males, displayed dominance behaviors. Moreover, egr-1 in the optic tectum and the cerebellum was similarly induced in all experimental groups, showing that egr-1 induction in the anterior preoptic area of ascending males was specific to this brain region. Because egr-1 codes for a transcription factor important in neural plasticity, induction of egr-1 in the anterior preoptic area by social opportunity could be an early trigger in the molecular cascade that culminates in enhanced fertility and other long-term physiological changes associated with dominance.

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Journal ArticleDOI
07 Nov 2008-Science
TL;DR: Progress has been made in identifying and understanding two key “vectors of influence” that link genes, the brain, and social behavior: social information alters gene expression in the brain to influence behavior, and genetic variation influences brain function and socialbehavior.
Abstract: What specific genes and regulatory sequences contribute to the organization and functioning of brain circuits that support social behavior? How does social experience interact with information in the genome to modulate these brain circuits? Here we address these questions by highlighting progress that has been made in identifying and understanding two key “vectors of influence” that link genes, brain, and social behavior: 1) social information alters gene readout in the brain to influence behavior; and 2) genetic variation influences brain function and social behavior. We also briefly discuss how evolutionary changes in genomic elements influence social behavior and outline prospects for a systems biology of social behavior.

508 citations

Journal ArticleDOI
TL;DR: It is proposed that the study of social competence requires an integrative approach that aims to understand how the brain translates social information into flexible behavioural responses, how flexibility might be constrained by the developmental history of an individual or by trade-offs with other competences, and how social plasticity feeds back on fitness.
Abstract: ‘Social competence’ refers to the ability of an individual to optimise its social behaviour depending on available social information. Although such ability will enhance social interactions and thus raise Darwinian fitness, its evolutionary and ecological significance has been largely ignored. Social competence is based on behavioural flexibility. We propose that the study of social competence requires an integrative approach that aims to understand how the brain translates social information into flexible behavioural responses, how flexibility might be constrained by the developmental history of an individual or by trade-offs with other (ecological) competences, and how social plasticity feeds back on fitness. Finally we propose a hypothesis of how social competence can become a driver of social evolution. Behavioural flexibility as phenotypic plasticity Adaptation to the environment is a universal characteristic of living systems. According to classic evolutionary theory, adaptation by natural selection relies 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 [1]. In this scenario, the evolution of phenotypic plasticity is favoured, that is, a certain genotype produces different phenotypes depending on environmental conditions [2]. Among animals, behavioural traits exhibit a greater plasticity than morphological and physiological traits and plastic changes are reversible within an individual’s lifetime (‘behavioural flexibility’). This makes behavioural flexibility a powerful, immediate mechanism allowing organisms to adapt to changing environmental conditions, which may or may not be followed by other flexible adjustments of physiology or morphology. Many of these responses are simple reflexes and fixed action patterns elicited by a stimulus in the environment, when it deterministically predicts an appropriate response. However, when environmental complexity and variability increase, the capacity to adaptively modify behaviour as a function of experience and context is needed. Although some degree of context-dependent behavioural flexibility may be achieved with genetically determined rules, behavioural flexibility will often depend on cognitive abilities (understood as the acquisition, retention, and use of information; [3]) that allow individuals to adapt behavioural output to specific situations in a complex and variable world (e.g., see [4]). Interestingly, the evolutionary study of behavioural flexibility has rarely been framed within the scope of phenotypic plasticity, but rather in terms of cognitive evolution and ecology [3,5]. This is most probably due to the fact that in contrast to morphological and life history traits (which have been the main focus of phenotypic plasticity studies, and whose plasticity results from processes during development and is usually non-reversible) behavioural flexibility involves rapid changes, is labile, and is present during the whole life of the animal [6,7].

342 citations

Journal ArticleDOI
TL;DR: This review presents examples of integrative studies that illustrate the molecular and cellular mechanisms underlying plastic traits, and shows how new techniques will grow in importance in the study of these plastic molecular processes.
Abstract: Phenotypic plasticity is the development of different phenotypes from a single genotype, depending on the environment. Such plasticity is a pervasive feature of life, is observed for various traits and is often argued to be the result of natural selection. A thorough study of phenotypic plasticity should thus include an ecological and an evolutionary perspective. Recent advances in large-scale gene expression technology make it possible to also study plasticity from a molecular perspective, and the addition of these data will help answer long-standing questions about this widespread phenomenon. In this review, we present examples of integrative studies that illustrate the molecular and cellular mechanisms underlying plastic traits, and show how new techniques will grow in importance in the study of these plastic molecular processes. These techniques include: (i) heterologous hybridization to DNA microarrays; (ii) next generation sequencing technologies applied to transcriptomics; (iii) techniques for studying the function of noncoding small RNAs; and (iv) proteomic tools. We also present recent studies on genetic model systems that uncover how environmental cues triggering different plastic responses are sensed and integrated by the organism. Finally, we describe recent work on changes in gene expression in response to an environmental cue that persist after the cue is removed. Such long-term responses are made possible by epigenetic molecular mechanisms, including DNA methylation. The results of these current studies help us outline future avenues for the study of plasticity.

320 citations


Cites background from "Rapid behavioral and genomic respon..."

  • ...Solid green curve: dominance behaviour (White et al. 2002; Burmeister et al. 2005); solid blue curve: gonad development (White et al....

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  • ...…specifically in the neurons that trigger the hormonal reproductive axis, thus pointing to a link between the perceived change in the environment (the male is freed of challenges from the dominant opponents) and the development of the dominant and reproductive phenotype (Burmeister et al. 2005)....

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  • ...development of the dominant and reproductive phenotype (Burmeister et al. 2005)....

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Journal ArticleDOI
22 May 2020-Science
TL;DR: These findings suggest that some aspects of the social determinants of health—especially those that can be modeled through studies of direct social interaction in nonhuman animals—have deep evolutionary roots and present new opportunities for studying the emergence of social disparities in health and mortality risk.
Abstract: The social environment, both in early life and adulthood, is one of the strongest predictors of morbidity and mortality risk in humans. Evidence from long-term studies of other social mammals indicates that this relationship is similar across many species. In addition, experimental studies show that social interactions can causally alter animal physiology, disease risk, and life span itself. These findings highlight the importance of the social environment to health and mortality as well as Darwinian fitness-outcomes of interest to social scientists and biologists alike. They thus emphasize the utility of cross-species analysis for understanding the predictors of, and mechanisms underlying, social gradients in health.

305 citations

Journal ArticleDOI
TL;DR: The results illuminate the importance of the molecular response to social conditions, particularly in the immune system, and demonstrate a key role for gene regulation in linking the social environment to individual physiology.
Abstract: Variation in the social environment is a fundamental component of many vertebrate societies. In humans and other primates, adverse social environments often translate into lasting physiological costs. The biological mechanisms associated with these effects are therefore of great interest, both for understanding the evolutionary impacts of social behavior and in the context of human health. However, large gaps remain in our understanding of the mechanisms that mediate these effects at the molecular level. Here we addressed these questions by leveraging the power of an experimental system that consisted of 10 social groups of female macaques, in which each individual's social status (i.e., dominance rank) could be experimentally controlled. Using this paradigm, we show that dominance rank results in a widespread, yet plastic, imprint on gene regulation, such that peripheral blood mononuclear cell gene expression data alone predict social status with 80% accuracy. We investigated the mechanistic basis of these effects using cell type-specific gene expression profiling and glucocorticoid resistance assays, which together contributed to rank effects on gene expression levels for 694 (70%) of the 987 rank-related genes. We also explored the possible contribution of DNA methylation levels to these effects, and identified global associations between dominance rank and methylation profiles that suggest epigenetic flexibility in response to status-related behavioral cues. Together, these results illuminate the importance of the molecular response to social conditions, particularly in the immune system, and demonstrate a key role for gene regulation in linking the social environment to individual physiology.

261 citations

References
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Journal ArticleDOI
TL;DR: The meta-analysis identified two variables that significantly predictedrelative cortisol levels: subordinates exhibited higher relative cortisol levels when they were subjected to higher rates of stressors and experienced decreased opportunities for social (including close kin) support.

655 citations


Additional excerpts

  • ...growth rate [5], and stress physiology [6,7]....

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Journal ArticleDOI
01 Oct 1998-Neuron
TL;DR: It is shown that the anterior forebrain vocal pathway contains medial and lateral "cortical-basal ganglia" subdivisions that have differential ZENK gene activation depending on whether the bird sings female-directed or undirected song.

448 citations


"Rapid behavioral and genomic respon..." refers background in this paper

  • ...Indeed, there is precedence for social context causing large differences in motor-driven egr-1 expression [24,33], suggesting that the stimulus context itself, or subtle behavioral motor differences between the two contexts, are able to cause large differences in egr-1 expression....

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Journal ArticleDOI
TL;DR: Recent systems-based studies underscore the remarkable sensitivity and specificity of the induction of the expression of genes encoding EGR-family members in naturally occurring plasticity paradigms, but they also challenge conventional views of the role of this family in plasticity.

439 citations

Journal ArticleDOI
TL;DR: The PTEN tumour suppressor and pro-apoptotic gene is frequently mutated in human cancers and loss of Egr-1 expression could deregulate the PTEN gene and contribute to the radiation resistance of some cancer cells.
Abstract: The PTEN tumour suppressor and pro-apoptotic gene is frequently mutated in human cancers. We show that PTEN transcription is upregulated by Egr-1 after irradiation in wild-type, but not egr-1-/-, mice in vivo. We found that Egr-1 specifically binds to the PTEN 5' untranslated region, which contains a functional GCGGCGGCG Egr-1-binding site. Inducing Egr-1 by exposing cells to ultraviolet light upregulates expression of PTEN messenger RNA and protein, and leads to apoptosis. egr-1-/- cells, which cannot upregulate PTEN expression after irradiation, are resistant to ultraviolet-light-induced apoptosis. Therefore, Egr-1 can directly regulate PTEN, triggering the initial step in this apoptotic pathway. Loss of Egr-1 expression, which often occurs in human cancers, could deregulate the PTEN gene and contribute to the radiation resistance of some cancer cells.

391 citations


"Rapid behavioral and genomic respon..." refers background in this paper

  • ...burtoni GnRH1 gene is a candidate target of the egr-1 transcription factor by localizing an egr-1 binding site (GCGGCGGCG [27]) 1,311 nucleotides upstream of the transcription start site [28]....

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Journal ArticleDOI
TL;DR: Critical review of the large literature describing the "immediate early gene" response leads to an alternative model of IEG function in the brain, which sets the overall gain or efficiency of memory formation and directs it to circuits engaged by behaviorally significant contexts.

379 citations