Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes

We argue that phenotypic plasticity should be broadly construed to encompass a diversity of phenomena spanning several hierarchical levels of organization. Despite seemingly disparate outcomes among different groups of organisms (e.g., the opening/closing of stomata in leaves, adjustments of allocation to growth/reproduction, or the production of different castes in social insects), there are underlying shared processes that initiate these responses. At the most fundamental level, all plastic responses originate at the level of individual cells, which receive and process signals from their environment. The broad variations in physiology, morphology, behavior, etc., that can be produced by a single genotype, can be accounted for by processes regulating gene expression in response to environmental variation. Although evolution of adaptive plasticity may not be possible for some types of environmental signals, in many cases selection has molded responses to environmental variation that generate precise and repeatable patterns of gene expression. We highlight the example of responses of plants to variation in light quality and quantity, mediated via the phytochrome genes. Responses to changes in light at particular stages of plants' life cycles (e.g., seed germination, competition, reproduction) are controlled by different members of this gene family. The mechanistic details of the cell and molecular biology of phytochrome gene action (e.g., their effects on expression of other genes) is outlined. Plasticity of cells and organisms to internal and external environmental signals is pervasive, and represents not just an outcome of evolutionary processes, but also a potentially important molder of them. Phenotypes originally initiated via a plastic response, can be fixed through genetic assimilation as alternate regulatory pathways are shut off. Evolution of mechanisms of plasticity and canalization can both reduce genetic variation, as well as shield it. When the organism encounters novel environmental conditions, this shielded variation may be expressed, revealing hidden reaction norms that represent the raw material for subsequent evolution.     

Plasticity of the mate choice mind: courtship evokes choice‐like brain responses in females from a coercive mating system

Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole‐brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species‐level differences in female behavioral and brain molecular responses represent ‘canalized’ or ‘plastic’ traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole‐brain gene expression analyses of neuroserpin, egr‐1 and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning‐based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion‐driven mating systems.     

细菌群体感应信号网络及其应用

群体感应（Quorum sensing,QS）是一种细菌细胞与细胞间的通讯系统,即细菌通过分泌扩散性小分子信号感知细菌群体的密度,从而引起一组特定基因在转录水平协调表达。大量研究已表明,群体感应系统控制细菌多种生理行为和过程,以及与真核宿主（寄主）的互作。参与群体感应调控的信号分子多种多样,QS系统所调控的功能也具有多样性,甚至菌株专化性。通过聚焦同一细菌中由多个QS系统组成的信号网络,综合评述了不同QS系统之间如何相互作用全局调控基因表达,以及QS系统如何通过与其它全局调控系统整合精细调节细菌的社会行为以及环境适应性及其应用前景。     

Manipulation of colony environment modulates honey bee aggression and brain gene expression

The social environment plays an essential role in shaping behavior for most animals. Social effects on behavior are often linked to changes in brain gene expression. In the honey bee (Apis mellifera L.), social modulation of individual aggression allows colonies to adjust the intensity with which they defend their hive in response to predation threat. Previous research has showed social effects on both aggression and aggression‐related brain gene expression in honey bees, caused by alarm pheromone and unknown factors related to colony genotype. For example, some bees from less aggressive genetic stock reared in colonies with genetic predispositions toward increased aggression show both increased aggression and more aggressive‐like brain gene expression profiles. We tested the hypothesis that exposure to a colony environment influenced by high levels of predation threat results in increased aggression and aggressive‐like gene expression patterns in individual bees. We assessed gene expression using four marker genes. Experimentally induced predation threats modified behavior, but the effect was opposite of our predictions: disturbed colonies showed decreased aggression. Disturbed colonies also decreased foraging activity, suggesting that they did not habituate to threats; other explanations for this finding are discussed. Bees in disturbed colonies also showed changes in brain gene expression, some of which paralleled behavioral findings. These results show that bee aggression and associated molecular processes are subject to complex social influences .     

Interaction of rearing environment and reproductive tactic on gene expression profiles in Atlantic salmon

Organisms that share the same genotype can develop into divergent phenotypes, depending on environmental conditions. In Atlantic salmon, young males of the same age can be found either as sneakers or immature males that are future anadromous fish. Just as the organism-level phenotype varies between divergent male developmental trajectories, brain gene expression is expected to vary as well. We hypothesized that rearing environment can also have an important effect on gene expression in the brain and possibly interact with the reproductive tactic adopted. We tested this hypothesis by comparing brain gene expression profiles of the two male tactics in fish from the same population that were reared in either a natural stream or under laboratory conditions. We found that expression of certain genes was affected by rearing environment only, while others varied between male reproductive tactics independent of rearing environment. Finally, more than half of all genes that showed variable expression varied between the two male tactics only in one environment. Thus, in these fish, very different molecular pathways can give rise to similar macro-phenotypes depending on rearing environment. This result gives important insights into the molecular underpinnings of developmental plasticity in relationship to the environment.     

Behavioral plasticity and G × E of reproductive tactics in Nicrophorus vespilloides burying beetles

Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals’ signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.     

Neurogenomic evidence for a shared mechanism of the antidepressant effects of exercise and chronic fluoxetine in mice

Several different interventions improve depressed mood, including medication and environmental factors such as regular physical exercise. The molecular pathways underlying these effects are still not fully understood. In this study, we sought to identify shared mechanisms underlying antidepressant interventions. We studied three groups of mice: mice treated with a widely used antidepressant drug--fluoxetine, mice engaged in voluntary exercise, and mice living in an enriched environment. The hippocampi of treated mice were investigated at the molecular and cellular levels. Mice treated with fluoxetine and mice who exercised daily showed, not only similar antidepressant behavior, but also similar changes in gene expression and hippocampal neurons. These changes were not observed in mice with environmental enrichment. An increase in neurogenesis and dendritic spine density was observed following four weeks of fluoxetine treatment and voluntary exercise. A weighted gene co-expression network analysis revealed four different modules of co-expressed genes that were correlated with the antidepressant effect. This network analysis enabled us to identify genes involved in the molecular pathways underlying the effects of fluoxetine and exercise. The existence of both neuronal and gene expression changes common to antidepressant drug and exercise suggests a shared mechanism underlying their effect. Further studies of these findings may be used to uncover the molecular mechanisms of depression, and to identify new avenues of therapy.     

Epigenetic mechanisms in drug addiction

Changes in gene expression in brain reward regions are thought to contribute to the pathogenesis and persistence of drug addiction. Recent studies have begun to focus on the molecular mechanisms by which drugs of abuse and related environmental stimuli, such as drug-associated cues or stress, converge on the genome to alter specific gene programs. Increasing evidence suggests that these stable gene expression changes in neurons are mediated in part by epigenetic mechanisms that alter chromatin structure on specific gene promoters. This review discusses recent findings from behavioral, molecular and bioinformatic approaches being used to understand the complex epigenetic regulation of gene expression by drugs of abuse. This novel mechanistic insight might open new avenues for improved treatments of drug addiction.     

社会性昆虫级型和行为分化机制研究进展

社会性的出现是生物演化过程中的重要革新, 理解社会性的演化和调控机制具有重要的理论和实际意义。社会性昆虫的个体间有着明显的级型分化和劳动分工, 这有利于它们适应复杂的环境变化。理解社会性昆虫如何产生不同的形态、行为和生活史特性, 一直是进化和发育生物学的重要目标。随着测序技术的不断更新及生物信息学的快速发展, 已经有众多关于社会性昆虫级型和行为分化机制的研究报道。本文通过整理社会性昆虫研究的已有成果, 从环境因素、生理调控和分子机制等方面对社会性昆虫级型和行为分化机制相关研究进展进行了综述, 并对未来的研究方向做出了展望。根据现有证据, 社会性昆虫所生活的生物环境(食物营养、信息素、表皮碳氢化合物)和非生物环境(温度、气候等)均能直接或间接影响社会性昆虫级型和行为的分化; 保幼激素、蜕皮激素、类胰岛素及生物胺等内分泌激素和神经激素对社会性昆虫的级型和行为分化也有重要的调控作用; 此外, 遗传因素、新基因等DNA序列或基因组结构上的变化以及表观遗传修饰、基因的差异表达等基因调控机制均能不同程度地影响社会性昆虫的行为分化。本文建议加强昆虫纲其他社会性类群如半翅目蚜虫和缨翅目蓟马等的社会性行为及其演化机制的研究, 以加深对社会性昆虫起源及其行为演化的理解和认识。     

Social behavior in context: Hormonal modulation of behavioral plasticity and social competence

In social species animals should fine-tune the expression of their social behavior to social environments in order to avoid the costs of engaging in costly social interactions. Therefore, social competence, defined as the ability of an animal to optimize the expression of its social behavior as a function of the available social information, should be considered as a performance trait that impacts on the Darwinian fitness of the animal. Social competence is based on behavioral plasticity which, in turn, can be achieved by different neural mechanisms of plasticity, namely by rewiring or by biochemically switching nodes of a putative neural network underlying social behavior. Since steroid hormones respond to social interactions and have receptors extensively expressed in the social behavioral neural network, it is proposed that steroids play a key role in the hormonal modulation of social plasticity. Here, we propose a reciprocal model for the action of androgens on short-term behavioral plasticity and review a set of studies conducted in our laboratory using an African cichlid fish (Oreochromis mossambicus) that provide support for it. Androgens are shown to be implicated as physiological mediators in a wide range of social phenomena that promote social competence, namely by adjusting the behavioral response to the nature of the intruder and the presence of third parties (dear enemy and audience effects), by anticipating territorial intrusions (bystander effect and conditioning of the territorial response), and by modifying future behavior according to prior experience of winning (winner effect). The rapid behavioral actions of socially induced short-term transient changes in androgens indicate that these effects are most likely mediated by nongenomic mechanisms. The fact that the modulation of rapid changes in behavior is open to the influence of circulating levels of androgens, and is not exclusively achieved by changes in central neuromodulators, suggests functional relevance of integrating body parameters in the behavioral response. Thus, the traditional view of seeing neural circuits as unique causal agents of behavior should be updated to a brain-body-environment perspective, in which these neural circuits are embodied and the behavioral performance (and outcomes as fitness) depends on a dynamic relationship between the different levels. In this view hormones play a major role as behavioral modulators.     

How does Behavior Change the Brain? Multiple Methods to Answer Old Questions

Clearly the brain controls behavior but can behavior also "control" the brain? On an evolutionary time scale, selective ecological pressures shape the sensory and motor capacities as well as the body and behavior. Correspondingly, in development, behavior acts in concert with the environment to cause structural changes in the brain lasting a lifetime. Surprisingly, in "real time" social behavior can also cause changes, typically reversible, in the brain in adult animals. Changes caused by behavioral interactions can be dramatic, and in many instances, these interactions are directly related to reproductive behavior. Understanding how behavior sculpts the brain in the course of behavioral interactions is a major challenge. Analyzing such changes requires a model system allowing control of the biological and behavioral environment of many animals simultaneously yet allowing access to physiological, cellular and molecular processes being regulated. The mouthbrooding cichlid Haplochromis (Astatotilapia) burtoni (Günther) from Lake Tanganyika lends itself to the study of social influences on the brain. It has complex, though easily observable individual and social behaviors regulated by two distinct classes of males, those with territories and those without. Many features of the animals are shaped by social encounters including the maturation of juveniles, the hypothalamic-pituitary-gonadal axis, the growth rate, the basal stress level among others. How does social information effect change in the brain and body? Animals must attend to the social scene to identify their chances. Learning how social information is transduced into cellular changes in this species should help understand how this happens in other social animals.