Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.

Many organisms, including the fathead minnow (Pimephales promelas), a toxicological model organism, establish social hierarchies. The social rank of each male in a population is under the control of the hypothalamic-pituitary-gonadal (HPG) axis mainly through regulation of circulating androgen conce...

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Main Authors: Jelena Ivanova, Shiju Zhang, Rong-Lin Wang, Heiko L Schoenfuss
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5648243?pdf=render
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spelling doaj-da1a749e96f547be88b9b13a598fc1212020-11-24T21:48:15ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-011210e018680710.1371/journal.pone.0186807Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.Jelena IvanovaShiju ZhangRong-Lin WangHeiko L SchoenfussMany organisms, including the fathead minnow (Pimephales promelas), a toxicological model organism, establish social hierarchies. The social rank of each male in a population is under the control of the hypothalamic-pituitary-gonadal (HPG) axis mainly through regulation of circulating androgen concentrations, which in turn drive the expression of secondary sex characteristics (SSCs). As dominant and subordinate males in an exposure study are initially under different physiological conditions (i.e., differing plasma androgen concentrations), we proposed that they belong to different subpopulations in the context of exposure to compounds that may interact with the HPG axis. Using a meta-analysis of our data from several previously published studies, we corroborated the hypothesis that social status, as indicated by SSCs, results in distinct clusters (eigenvalues >0.8 explaining >80% of variability) with differential expression of plasma vitellogenin, a commonly used biomarker of exposure to contaminants of emerging concern (CEC). Furthermore, we confirmed our predictions that exposure to estrogenic CECs would homogenize plasma vitellogenin response (E1: cluster mean SSC values decreased to 4.33 and 4.86 relative to those of control; E2: decreased to 4.8 and 5.37) across the social hierarchy. In contrast, serotonin-specific reuptake inhibitors expand this response range (cluster mean SSC increased to 5.21 and 6.5 relative to those of control). Our results demonstrated that social hierarchies in male fathead minnows result in heterogeneous responses to chemical exposure. These results represent a cautionary note for the experimental design of single-sex exposure studies. We anticipate our study to be a starting point for the re-evaluation of toxicological data analyses in single sex exposure experiments.http://europepmc.org/articles/PMC5648243?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Jelena Ivanova
Shiju Zhang
Rong-Lin Wang
Heiko L Schoenfuss
spellingShingle Jelena Ivanova
Shiju Zhang
Rong-Lin Wang
Heiko L Schoenfuss
Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
PLoS ONE
author_facet Jelena Ivanova
Shiju Zhang
Rong-Lin Wang
Heiko L Schoenfuss
author_sort Jelena Ivanova
title Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
title_short Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
title_full Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
title_fullStr Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
title_full_unstemmed Social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
title_sort social hierarchy modulates responses of fish exposed to contaminants of emerging concern.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2017-01-01
description Many organisms, including the fathead minnow (Pimephales promelas), a toxicological model organism, establish social hierarchies. The social rank of each male in a population is under the control of the hypothalamic-pituitary-gonadal (HPG) axis mainly through regulation of circulating androgen concentrations, which in turn drive the expression of secondary sex characteristics (SSCs). As dominant and subordinate males in an exposure study are initially under different physiological conditions (i.e., differing plasma androgen concentrations), we proposed that they belong to different subpopulations in the context of exposure to compounds that may interact with the HPG axis. Using a meta-analysis of our data from several previously published studies, we corroborated the hypothesis that social status, as indicated by SSCs, results in distinct clusters (eigenvalues >0.8 explaining >80% of variability) with differential expression of plasma vitellogenin, a commonly used biomarker of exposure to contaminants of emerging concern (CEC). Furthermore, we confirmed our predictions that exposure to estrogenic CECs would homogenize plasma vitellogenin response (E1: cluster mean SSC values decreased to 4.33 and 4.86 relative to those of control; E2: decreased to 4.8 and 5.37) across the social hierarchy. In contrast, serotonin-specific reuptake inhibitors expand this response range (cluster mean SSC increased to 5.21 and 6.5 relative to those of control). Our results demonstrated that social hierarchies in male fathead minnows result in heterogeneous responses to chemical exposure. These results represent a cautionary note for the experimental design of single-sex exposure studies. We anticipate our study to be a starting point for the re-evaluation of toxicological data analyses in single sex exposure experiments.
url http://europepmc.org/articles/PMC5648243?pdf=render
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