Effects of monoamine manipulations on the personality and gene expression of three-spined sticklebacks

Abstract

Among-individual behavioral differences (i.e. animal personality) are commonly observed across taxa, although the underlying, causal mechanisms of such differences are poorly understood. Animal personality has been correlated with physiological functions as well as fitness-related traits. Variation in many aspects of monoamine systems, such as metabolite levels and gene polymorphisms, has been linked to behavioral variation. Therefore, here we experimentally investigated the potential role of monoamines in explaining individual variation in personality, using two common pharmaceuticals that respectively alter the levels of serotonin and dopamine in the brain: fluoxetine and ropinirole. We exposed threespined sticklebacks, a species that shows animal personality, to either chemical alone or to a combination of the two chemicals, for 18 days. During the experiment, fish were assayed at four time points for the following personality traits: exploration, boldness, aggression and sociability. To quantify brain gene expression on short-and longer-term scales, fish were sampled at two time points. Our results show that monoamine manipulations influence fish behavior. Specifically, fish exposed to either fluoxetine or ropinirole were significantly bolder, and fish exposed to the two chemicals together tended to be bolder than control fish. Our monoamine manipulations did not alter the gene expression of monoamine or stress-associated neurotransmitter genes, but control, untreated fish showed covariation between gene expression and behavior. Specifically, exploration and boldness were predicted by genes in the dopaminergic, serotonergic and stress pathways, and sociability was predicted by genes in the dopaminergic and stress pathways. These results add further support to the links between monoaminergic systems and personality, and show that exposure to monoamines can causally alter animal personality.

Sociability as a personality trait in animals: methods, causes and consequences

“…Oxytocin receptor genes are important in explaining consistent differences in sociability in dogs (Kis et al ., 2014) and mice (Sala et al ., 2013), but not in chimpanzees Pan troglodytes , where variation in sociability is instead associated with the vasopressin receptor gene (Staes et al ., 2015). Sociability has also been shown to be linked to variation in the expression of genes involved in stress hormones such as cortisol, and monoamine neurotransmitters such as serotonin and dopamine (Shou et al ., 2019; Abbey‐Lee et al ., 2019; Bond et al ., 2020). In the bee Lasioglossum albipes , several candidate genes associated with social variation and linked to neurotransmission were identified (Kocher et al ., 2018).…”

Exploring the Relationship Between Boldness, Activity, Exploration and Monoaminergic Gene Expression in Red Junglefowl Chicks

“…Both methods have been used to demonstrate a link between the monoaminergic systems and the behaviors we measured here. Studies on variation in gene expression have manipulated circulating levels of monoamines and/or looked at links between natural levels and behavior (Abbey-Lee, Uhrig, Garnham, et al, 2018;Abbey-Lee et al, 2019). Gene polymorphism studies involve knocking down a specific gene (e.g., Kalueff et al, 2006;Malleret et al, 1999), or looking at gene polymorphisms in either producing, transporting or receptor genes (e.g., Fidler et al, 2007;Holtmann et al, 2016;Korsten et al, 2010;Suomi, 2006).…”

“…However, the current literature is biased towards a focus on mammals for studies on SERT (Gordon & Hen, 2004;Monafo et al, 2009;Reif & Lesch, 2003), and great tits for studies focusing on DRD4 (Fidler et al, 2007;Korsten et al, 2010;Mueller et al, 2014;Riyahi et al, 2015), which limits our general understanding of these links. Further, very few studies have simultaneously investigated how several genes from the serotonergic and dopaminergic systems may link to variation in a range of behavior ; but see e.g., Abbey-Lee, Uhrig, Garnham, et al 2018;Abbey-Lee et al, 2019;Edward et al, 2015;Holtmann et al, 2016;Riyahi et al, 2015;Lundgren et al, 2021).…”

“…Additionally, both methods give similar general information on whether there is evidence for a relationship between a specific behavior and gene. The genes 5HT1B, 5HT2C, and DRD2 were chosen because earlier studies in other species suggest an association between these genes and variation in exploration, activity, or boldness, respectively (Abbey- Lee et al, 2019;Heisler & Tecott, 2000;Malleret et al, 1999;van Oers et al, 2005). Based on this, we predicted that exploration and activity would be negatively correlated with gene expression of 5HT1A and 5HT1B, whilst exploration and boldness would be positively correlated with DRD2.…”

Functional convergence of genomic and transcriptomic genetic architecture underlying sociability in a live-bearing fish

“…Studies in non-human organisms likewise point towards a major role of genes involved in the regulation of these neurochemical systems. For instance, sociability is affected in mouse knock-out mutants for genes involved in dopaminergic signalling in the mouse nervous system 19 , and changes in sociability in three-spined sticklebacks, Gasterosteus aculeatus are predicted by natural variation in the expression of genes within the dopaminergic and stress pathways 20 . While specific groups of genes have been identified for a range of affiliative behaviors, we lack a deeper understanding of their role in inter-individual variation and evolutionary processes underlying social systems.…”