The Influence of Rearing on Behavior, Brain Monoamines, and Gene Expression in Three-Spined Sticklebacks

Abbey-Lee, Robin N.; Uhrig, Emily J.; Zidar, Josefina; Favati, Anna; Almberg, Johan; Dahlbom, Josefin; Winberg, Svante; Løvlie, Hanne

doi:10.1159/000489942

Cited by 14 publications

(6 citation statements)

References 65 publications

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“…We also found that carnivore‐biased genes were associated with nervous system development, synaptic signaling, and behavior (Table 4). Such changes in brain gene expression are common in organisms encountering a dynamic or enriched environment (Abbey‐Lee et al, 2018; Chesler & Williams 2004; Rampon et al, 2000) and are generally consistent with previous work on brain gene expression between spadefoot morphs (Ledón‐Rettig, 2021). Our results suggest that the individuals that have more to gain from effectively navigating such a dynamic environment—carnivores—may do so by expanding their nervous system (presumably the brain) and increasing their activity to facilitate changes in behavior accompanying a predatory lifestyle (Ledón‐Rettig, 2021; Pfennig, 1999; Pfennig & Murphy, 2000).…”

Section: Discussionsupporting

confidence: 81%

Transcriptomic bases of a polyphenism

et al. 2021

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Polyphenism—in which multiple distinct phenotypes are produced from a single genotype owing to differing environmental conditions—is commonplace, but its molecular bases are poorly understood. Here, we examine the transcriptomic bases of a polyphenism in Mexican spadefoot toads (Spea multiplicata). Depending on their environment, their tadpoles develop into either a default “omnivore” morph or a novel “carnivore” morph. We compared patterns of gene expression among sibships that exhibited high versus low production of carnivores when reared in conditions that induce the carnivore morph versus those that do not. We found that production of the novel carnivore morph actually involved changes in fewer genes than did the maintenance of the default omnivore morph in the inducing environment. However, only body samples showed this pattern; head samples showed the opposite pattern. We also found that changes to lipid metabolism (especially cholesterol biosynthesis) and peroxisome contents and function might be crucial for establishing and maintaining differences between the morphs. Thus, our findings suggest that carnivore phenotype might have originally evolved following the breakdown of robustness mechanisms that maintain the default omnivore phenotype, and that the carnivore morph is developmentally regulated by lipid metabolism and peroxisomal form, function, and/or signaling. This study also serves as a springboard for further exploration into the nature and causes of plasticity in an emerging model system.

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Section: Discussionsupporting

confidence: 81%

Transcriptomic bases of a polyphenism

et al. 2021

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“…Taken together, our results show a clear link between monoamines and behavior, but also highlight that gene expression, at least of our measured genes in whole brain tissue, may not be influenced by exposure to our tested pharmaceuticals. Work in other populations of sticklebacks has had similar results, confirming correlations between behavior and monoamine systems, but not finding monoamines as underlying mechanisms (Abbey-Lee et al, 2018b). Potentially, earlier steps of the HPI axis or other unmeasured aspects of physiology may be responsible for the observed behavioral differences, and therefore our manipulations of serotonin and dopamine levels were ineffectual.…”

Section: Discussionsupporting

confidence: 68%

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

Abbey-Lee

Kreshchenko

Sala

et al. 2019

Journal of Experimental Biology

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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.

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“…After the novel arena test, fish were exposed to a 10-min mirror test to measure aggression and sociability towards a same-size conspecific (Scherer et al 2016 ; Abbey-Lee et al 2018 ). A mirror was placed in the tank to contain the fish in a 1/3 of the tank farthest from the sheltered area.…”

Section: Methodsmentioning

confidence: 99%

Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social

Petkova

Abbey-Lee

Løvlie

2018

Behav Ecol Sociobiol

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The existence of animal personality is now well-documented, although the causes and consequences of this phenomenon are still largely unclear. Parasite infection can have pervasive effects on hosts, including altering host behaviour, and may thus contribute to differences in host personality. We investigated the relationship between the three-spined stickleback and its common parasite Glugea anomala, with focus on differences in host personality. Naturally infected and uninfected individuals were assayed for the five personality traits activity, exploration, boldness, sociability, and aggression. If infected fish behaved differently from uninfected, to benefit this parasite with horizontal transmission, we predicted behaviour increasing interactions with other sticklebacks to increase. Infection status explained differences in host personality. Specifically, Glugea-infected individuals were more social than uninfected fish. This confirms a link between parasite infection and host behaviour, and a relationship which may improve the horizontal transmission of Glugea. However, future studies need to establish the consequences of this for the parasite, and the causality of the parasite-host personality relationship.Significance statementParasite infection that alters host behaviour could be a possible avenue of research into the causes of animal personality. We studied the link between infection and personality using the three-spined stickleback and its parasite Glugea anomala. We predicted that infected individuals would be more prone to interact with other sticklebacks, since this would improve transmission of this parasite. The personality of uninfected and naturally infected fish was measured and we observed that Glugea-infected sticklebacks were more social. Our results confirm a link between parasitism and variation in host personality.Electronic supplementary materialThe online version of this article (10.1007/s00265-018-2586-3) contains supplementary material, which is available to authorized users.

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The Influence of Rearing on Behavior, Brain Monoamines, and Gene Expression in Three-Spined Sticklebacks

Cited by 14 publications

References 65 publications

Transcriptomic bases of a polyphenism

Transcriptomic bases of a polyphenism

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

Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social

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