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

PLoS One. 2017 Oct 19;12(10):e0186807. doi: 10.1371/journal.pone.0186807. eCollection 2017.

Abstract

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.

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Estrogens / toxicity*
  • Fishes*
  • Male
  • Selective Serotonin Reuptake Inhibitors / toxicity*
  • Vitellogenins / blood
  • Water Pollutants, Chemical / toxicity*

Substances

  • Biomarkers
  • Estrogens
  • Serotonin Uptake Inhibitors
  • Vitellogenins
  • Water Pollutants, Chemical

Grants and funding

HLS (St Cloud State University) received funding from the US Fish & Wildlife Service for this project (628737). Additional support was provided to HLS by a National Science Foundation grant (CBET 1336062). Travel grants and award funds by SETAC (to JL) are acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.