Transcriptional regulation of brain gene expression in response to a territorial intrusion

Sanogo, Yibayiri O.; Band, Mark; Blatti, Charles; Sinha, Saurabh; Bell, Alison M.

doi:10.1098/rspb.2012.2087

Cited by 57 publications

(77 citation statements)

References 57 publications

(77 reference statements)

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“…One motif, predicted to bind the nuclear receptor protein NR2E1 (a toolkit TF), was enriched in all three species. Several others were enriched in two species, including motifs for TFs involved in neuroendocrine signaling [NR2A1, which was also associated with territorial intrusion in a previous stickleback study (8); LEF1 (34); and DLX1 (35)]. Results also implicated the transcriptional repressor HIC1, which is believed to act via chromatin remodeling (36), and the IEG ZNF354C.…”

Section: Cross-species Core Processes In the Response To Territory Inmentioning

confidence: 76%

“…Several of these have been associated with metabolism or social behavior in previous studies. Nr4a3 (a nuclear receptor protein), Nr5a1, and Irx3 (a homeobox transcription factor) play key roles in energy homeostasis (44)(45)(46)(47); Nr5a1, Emx1, and Foxg1 have been associated with behavior and mood disorders (48)(49)(50); Nr4a3 is up-regulated in response to novel song in birds (51); and Nr5a1 is linked to social aggression in sticklebacks and mice (8,48).…”

Section: Discussionmentioning

confidence: 99%

“…We sequenced different brain regions across the three species: honey bee whole brain [which shows a robust transcriptomic signature across multiple aggressive contexts (7)], stickleback diencephalon [which shows intense neural activation in response to intrusion (8)], and mouse ventral hypothalamus (VH) (9). We validated strong involvement of the VH, using brain regional quantitative PCR (qPCR) analysis of several immediate early genes (IEGs) [Fos, Fosl2, Arc, and Egr1 (early growth response protein 1); Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Animals were killed after an additional 15 min (mouse) or 25 min (honey bee and stickleback). These slight variations in timelines were required to keep mouse and stickleback experiments consistent with previously published protocols (8,43,67,68). The protocol for honey bee was novel, so we followed the stickleback timeline because expression differences for IEGs and other socially responsive genes are generally best detected 30 min poststimulus (69,70).…”

Section: Methodsmentioning

confidence: 99%

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Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Rittschof

Bukhari

Sloofman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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141

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Certain complex phenotypes appear repeatedly across diverse species due to processes of evolutionary conservation and convergence. In some contexts like developmental body patterning, there is increased appreciation that common molecular mechanisms underlie common phenotypes; these molecular mechanisms include highly conserved genes and networks that may be modified by lineage-specific mutations. However, the existence of deeply conserved mechanisms for social behaviors has not yet been demonstrated. We used a comparative genomics approach to determine whether shared neuromolecular mechanisms could underlie behavioral response to territory intrusion across species spanning a broad phylogenetic range: house mouse (Mus musculus), stickleback fish (Gasterosteus aculeatus), and honey bee (Apis mellifera). Territory intrusion modulated similar brain functional processes in each species, including those associated with hormone-mediated signal transduction and neurodevelopment. Changes in chromosome organization and energy metabolism appear to be core, conserved processes involved in the response to territory intrusion. We also found that several homologous transcription factors that are typically associated with neural development were modulated across all three species, suggesting that shared neuronal effects may involve transcriptional cascades of evolutionarily conserved genes. Furthermore, immunohistochemical analyses of a subset of these transcription factors in mouse again implicated modulation of energy metabolism in the behavioral response. These results provide support for conserved genetic "toolkits" that are used in independent evolutions of the response to social challenge in diverse taxa.genetic hotspot | NF-κB signaling | brain metabolism | aggression S imilar phenotypes can have a shared molecular basis, even among distantly related species (1-3). This phenomenon has been observed for an array of traits, including morphological adaptations like coat color or wing patterning, rapid adaptations like drug resistance, and artificially selected phenological traits like flowering time (reviewed in ref. 2). Shared molecular mechanisms can arise convergently as a result of de novo mutations at genetic hotspots (2) or as a result of conservation. Both of these processes result in "genetic toolkits" or genes that are repeatedly used over evolutionary time to give rise to similar phenotypes (3). The phenomenon of genetic toolkits challenges fundamental notions about evolutionary convergence, conservation, and the origins of biodiversity.The role of genetic toolkits in shaping behavioral phenotypes is unclear (4, 5). Behaviors are typically polygenic (6) and they show great nuance and plasticity within a species, raising the possibility that cross-species similarities in behavior are superficial. Social behaviors in particular present a challenge to the genetic toolkit concept: these behaviors are critical to survival and reproductive success, but across species there is significant variation in the contexts for an...

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Section: Cross-species Core Processes In the Response To Territory Inmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Rittschof

Bukhari

Sloofman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

141

189

View full text Add to dashboard Cite

show abstract

“…Hence, the same genotype must accommodate the expression of multiple social phenotypes, and this should be accomplished, at least partially, by socially driven changes in gene expression in the brain that would lead to distinct transcriptome profiles across the social behavior neural network (aka neurogenomic states) (3,9,10) corresponding to status-specific behavioral states. Previous studies have established this mapping of socially dependent behavioral states onto neurogenomic states (11)(12)(13)(14), and rapid responses to social interactions have also been described (15)(16)(17)(18). However, the specific cue that signals changes in social status and triggers the switch between neurogenomic states has remained elusive.…”

mentioning

confidence: 99%

Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain

Oliveira

Simões

Teles

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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 questions that have remained unanswered. Here, we show for the first time, to our knowledge, that the switch between status-specific neurogenomic states relies on the assessment of fight outcome rather than just on self- or opponent-only assessment of fighting ability. For this purpose, we manipulated the perception of fight outcome in male zebrafish and measured its impact on the brain transcriptome using a zebrafish whole genome gene chip. Males fought either a real opponent, and a winner and a loser were identified, or their own image on a mirror, in which case, despite expressing aggressive behavior, males did not experience either a victory or a defeat. Massive changes in the brain transcriptome were observed in real opponent fighters, with losers displaying both a higher number of differentially expressed genes and of coexpressed gene modules than winners. In contrast, mirror fighters expressed a neurogenomic state similar to that of noninteracting fish. The genes that responded to fight outcome included immediate early genes and genes involved in neuroplasticity and epigenetic modifications. These results indicate that, even in cognitively simple organisms such as zebrafish, neurogenomic responses underlying changes in social status rely on mutual assessment of fighting ability.

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Neurogenomics of Behavioural Plasticity in Socioecological Contexts

Baker

Hofmann

Wong

2017

Encyclopedia of Life Sciences

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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.

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Transcriptional regulation of brain gene expression in response to a territorial intrusion

Cited by 57 publications

References 57 publications

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee

Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain

Neurogenomics of Behavioural Plasticity in Socioecological Contexts

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