Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks

Bell, Alison M.; Bukhari, Syed; Sanogo, Yibayiri O.

doi:10.1163/1568539x-00003393

Cited by 63 publications

(29 citation statements)

References 70 publications

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“…; Bell et al. ) and honey bees (Alaux et al. ), and have ascribed a strong and multigenic transcriptional basis to behavioral variation.…”

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confidence: 99%

“…), though one study has found transcriptional overlap between behavioral transitions and behavioral variation in sticklebacks (Bell et al. ).…”

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confidence: 99%

“…For example, in honeybees, differential expression is associated with the transition between nursing behavior and foraging behavior (Ben-Shahar et al 2002;Whitfield et al 2003;Grozinger et al 2007;Ament et al 2008). Other studies investigate how transcription relates to quantitative variation in behavior (QTT) or behavioral type in Drosophila (Dierick and Greenspan 2006;Edwards et al 2006), fish (Cummings et al 2008;Sanogo et al 2012;Rey et al 2013;Fraser et al 2014;Wong et al 2015;Bell et al 2016) and honey bees (Alaux et al 2009), and have ascribed a strong and multigenic transcriptional basis to behavioral variation.…”

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confidence: 99%

“…If, on the other hand, there is little or no overlap between these mechanisms, it instead suggests that two distinct processes are needed to produce a specific behavioral phenotype; one tightly controlled process to produce a transition, and a separately regulated process producing the quantitative phenotype. It has been predicted that regulatory mechanisms for different types of behavioral change will be different (Cardoso et al 2015), though one study has found transcriptional overlap between behavioral transitions and behavioral variation in sticklebacks (Bell et al 2016).…”

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Relating quantitative variation within a behavior to variation in transcription

et al. 2017

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Many studies have shown that variation in transcription is associated with changes in behavioral state, or with variation within a state, but little has been done to address if the same genes are involved in both. Here we investigate the transcriptional basis of variation in parental provisioning using two species of burying beetle, Nicrophorus orbicollis and Nicrophorus vespilloides. We used RNA-seq to compare transcription in parents that provided high amounts of provisioning behavior versus low amounts in males and females of each species. We found no overarching transcriptional patterns distinguishing high from low caring parents, and no informative transcripts that displayed particularly large expression differences in either sex. However, we did find subtler gene expression differences between high and low provisioning parents that are consistent across both sexes and species. Furthermore, we show that transcripts previously implicated in transitioning into parental care in N. vespilloides had high variance in the levels of transcription and were unusually likely to display differential expression between high and low provisioning parents. Thus, quantitative behavioral variation appears to reflect many transcriptional differences of small effect. Furthermore, the same transcripts required for the transition between behavioral states are also related to variation within a behavioral state.

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“…; Bell et al. ) and honey bees (Alaux et al. ), and have ascribed a strong and multigenic transcriptional basis to behavioral variation.…”

mentioning

confidence: 99%

“…), though one study has found transcriptional overlap between behavioral transitions and behavioral variation in sticklebacks (Bell et al. ).…”

mentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Relating quantitative variation within a behavior to variation in transcription

et al. 2017

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“…In addition to having a fully sequenced genome, they have been used in comparative cross-taxa studies looking for a conservation in the molecular underpinnings of social behavior (Rittschof et al 2014; Saul et al 2019) with both emerging and classic model systems. Indeed, there are already hundreds of previously identified candidate genes for social behavior waiting to be characterized (Sanogo et al 2011; Laine et al 2012; Greenwood et al 2013; Mommer & Bell 2014; Greenwood & Peichel 2015; Bell et al 2016; Bukhari et al 2017) and well-established behavioral assays (van Iersel 1953; Rowland 1982) that are amenable to automation (Ardekani et al 2013; Norton & Gutiérrez 2019).…”

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Minimally invasive brain injections for viral-mediated transgenesis: New tools for behavioral genetics in sticklebacks

James

Bell

2020

Preprint

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24Major Findings 25 Forced expression of MAOA or AVP resulted in more attacks, showing a causal link between genes and 26 behavior.Abstract 35 Establishing a causal relationship between genes and social behavior is challenging. To enable 36 direct manipulation of candidate genes and thereby examine how their expression contributes to 37 behavior, we developed a neurosurgical method to deliver pharmacological agents or transgenic 38 elements directly into the threespine stickleback (Gasterosteus aculeatus) brain. Threespine sticklebacks 39 are a classic system for the study of behavior, ecology, and evolution. Male sticklebacks defending 40 nesting territories are highly aggressive toward intruders. Previous studies in stickleback have shown 41 that aggression is heritable, and that hundreds of genes are differentially expressed in the brain following 42 territorial intrusion. 43 We use viral-mediated transgenesis to test the effects on territorial aggression of overexpression 44 of candidate genes, monoamine oxidase (MAOA) and arginine vasopressin (AVP), in the stickleback 45 brain. Male sticklebacks received transcranial injections of mammalian homolog cDNA packaged in a 46 replication-deficient Herpes Simplex Virus 1 carrier. Animals transfected with either AVP or MAOA 47 constructs were more aggressive in response to a territorial intruder, unlike control animals transfected 48 with a fluorescent protein. 49 Viral-mediated transgenesis is a promising method to examine genetic underpinnings of 50 behaviors. Our success demonstrates that widely available mammalian plasmids work with this method, 51 lowering the barrier of entry to the technique. This method is flexible, fast, and amenable to statistically 52 powerful within-subject experimental designs, making it practical for use in natural populations. It 53 further enhances the growing molecular toolkit in threespine stickleback, a classic ethological system, 54 and is the first step toward using chemogenetics and optogenetics.55 56 57 Complex behaviors have been repeatedly shown to be heritable (reviewed in Dochtermann et al., 58 2019), yet establishing a causal relationship between genes and social behavior remains challenging. 59Partially, this difficulty arises from limitations of the primarily correlative methods for examining the 60 interplay between genes and behavior (Charney 2017), such as QTL, GWAS, and RNAseq studies. 61These types of studies are certainly a necessary step generating many candidate genes. However, to fully 62 characterize how a gene contributes to behavior, it is necessary to consider not just sequence differences, 63 but also regulatory and epigenetic influences. Therefore, to demonstrate and fully characterize a causal 64 relationship between a gene and behavior, it is crucial to have a method for manipulating gene 65 expression at a specific time and location. We developed one such method, viral-mediated transgenesis, 66 for the classic ethological system of threespined stickleback (Gasterosteus aculeatus).

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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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Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks

Cited by 63 publications

References 70 publications

Relating quantitative variation within a behavior to variation in transcription

Relating quantitative variation within a behavior to variation in transcription

Minimally invasive brain injections for viral-mediated transgenesis: New tools for behavioral genetics in sticklebacks

Neurogenomics of Behavioural Plasticity in Socioecological Contexts

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