Neurogenomics of Behavioural Plasticity in Socioecological Contexts

Abstract

Social and ecological challenges often elicit behavioural and physiological responses that are adaptive and subject to selection. The varying behavioural states and traits of animals are a direct output of the nervous system and underlying molecular substrates. Changes in gene expression in response to a variety of contexts such as mate choice, aggression and developmental experience can alter a number of cellular and neural pathways that lead to changes in behaviour. A common framework has emerged to understand the role of the transcriptome in animal behaviour. Behavioural plasticity describes both an individual's ability to modify behavioural states and correlated suites of behaviour in populations, which may constrain variance across contexts. By integrating the study of behavioural plasticity with genome scale, bioinformatics and candidate gene analyses, we are rapidly expanding our understanding of this kind of organismal flexibility, its relationship with the genome and its evolutionary implications. Key Concepts To understand animal behaviour fully, both the proximate (causation and ontogeny) and the ultimate (function and evolution) mechanisms of behaviour must be considered and integrated. Utilising both forward and reverse genetics, candidate genes underlying a behaviour can be better identified and characterised. The genome is plastic and flexible in response to social or environmental cues, which can lead to changes in behaviour. Comparative transcriptomics across species can help identify and characterise conserved mechanisms of animal behaviour. The relationship between behavioural evolution and the processes that generate structural variation in the genome is not well understood and needs to be considered. The proposed framework will streamline future studies to uncover not only the genetic and neural mechanisms of complex animal behaviours but also its adaptive function and evolution.

Brain transcriptomics of agonistic behaviour in the weakly electric fish Gymnotus omarorum, a wild teleost model of non-breeding aggression

“…The search for both the neuromolecular basis of aggression and a conserved transcriptomic signature of dominance across species are matters of current research 1,2 . Social behaviour in vertebrates arises from a network of brain nuclei named the Social Decision-Making Network (SDMN), which includes a highly interconnected group of conserved brain regions [3][4][5][6] .…”

“…The strong behavioural asymmetry between contenders during agonistic encounters has provided a solid base for the search of phenotype-dependent gene expression profiles in the brain of vertebrates 17 . In particular, in fish, multiple reports have shown an association between social status and the variation of a few candidate genes 6,18,19 , as well as changes in gene expression at a genome-wide scale 1,2,6,[20][21][22][23][24][25][26][27][28] . A common result of measuring dynamic responses in gene expression is that there are hundreds to thousands of genes that are differentially expressed as a function of dominance, many of which have unrelated functions 28,29 .…”

Differential effects of ethanol on behavior and GABAA receptor expression in adult zebrafish (Danio rerio) with alternative stress coping styles

“…An individual’s behavioral and physiological stress responses are often correlated and are consistent across contexts. Throughout many taxa there exists two alternative correlated suites of behavioral and physiological responses to stressors known as the proactive and reactive stress coping styles 2 , 3 , 5 – 7 . In response to novelty, proactive individuals actively engage stressors and characteristically exhibit a lower whole-body cortisol response compared to reactive individuals 2 , 3 , 5 , 8 – 11 .…”

Differential effects of ethanol on behavior and GABAAreceptor subunit expression in zebrafish (Danio rerio) with alternative stress coping styles

“…While an organism’s stress response is essential to its survival, not all conspecifics exhibit similar responses and often differ both behaviorally and physiologically 1–5 . Across many taxa there exists two alternative correlated suites of behavioral and physiological responses to stressors known as the proactive and reactive stress coping styles 2,3,5–7 . Proactive individuals actively engage stressors and characteristically exhibit a lower whole-body cortisol response compared to reactive individuals in response to novelty 2,3,5,8–10 .…”

“…These coping styles in zebrafish display differences in genetic backgrounds, behavior and neuroendocrine responses to stressors that are consistent with what has been documented in birds and mammals 42–44 . Only recently are studies beginning to demonstrate the roles of synaptic plasticity and neurotransmitter system regulation in facilitating the display of alternative stress coping styles in zebrafish 5,7,12,45–47 . Hence zebrafish can serve as a useful system to study the neuromolecular variations between stress coping styles through the use of GABA-acting drugs.…”