Multigenerational and Transgenerational Effects of Environmentally Relevant Concentrations of Endocrine Disruptors in an Estuarine Fish Model

Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational...

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Published inEnvironmental science & technology Vol. 54; no. 21; pp. 13849 - 13860
Main Authors DeCourten, Bethany M, Forbes, Joshua P, Roark, Hunter K, Burns, Nathan P, Major, Kaley M, White, J. Wilson, Li, Jie, Mehinto, Alvine C, Connon, Richard E, Brander, Susanne M
Format Journal Article
LanguageEnglish
Published United States American Chemical Society 03.11.2020
Subjects
abnormal development
Animals
Aquatic organisms
bifenthrin
Contaminants
Deoxyribonucleic acid
DNA
DNA methylation
Ecotoxicology and Public Health
Egg production
Endocrine disruptors
Endocrine Disruptors - toxicity
Environmental effects
Epigenetics
Estuaries
estuarine fish
Estuarine pollution
Ethinyl Estradiol - toxicity
Ethinylestradiol
Exposure
Fishes
Gene expression
Immune response
Immune system
Insecticides
larvae
Larval development
Menidia beryllina
Pollutants
Reproduction
technology
toxic substances
Toxicants
Trenbolone
Water Pollutants, Chemical - toxicity
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Abstract Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational and transgenerational effects, respectively), particularly in estuarine fishes. To investigate this possibility, we exposed inland silversides (Menidia beryllina) to environmentally relevant (low ng/L) concentrations of ethinylestradiol, bifenthrin, trenbolone, and levonorgestrel from 8 hpf to 21 dph. We then measured development, immune response, reproduction, gene expression, and DNA methylation for two subsequent generations following the exposure. Larval exposure (F0) to each compound resulted in negative effects in the F0 and F1 generations, and for ethinylestradiol and levonorgestrel, the F2 also. The specific endpoints that were responsive to exposure in each generation varied, but included increased incidence of larval deformities, reduced larval growth and survival, impaired immune function, skewed sex ratios, ovarian atresia, reduced egg production, and altered gene expression. Additionally, exposed fish exhibited differences in DNA methylation in selected genes, across all three generations, indicating epigenetic transfer of effects. These findings suggest that assessments across multiple generations are key to determining the full magnitude of adverse effects from contaminant exposure in early life.
AbstractList Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational and transgenerational effects, respectively), particularly in estuarine fishes. To investigate this possibility, we exposed inland silversides (Menidia beryllina) to environmentally relevant (low ng/L) concentrations of ethinylestradiol, bifenthrin, trenbolone, and levonorgestrel from 8 hpf to 21 dph. We then measured development, immune response, reproduction, gene expression, and DNA methylation for two subsequent generations following the exposure. Larval exposure (F0) to each compound resulted in negative effects in the F0 and F1 generations, and for ethinylestradiol and levonorgestrel, the F2 also. The specific endpoints that were responsive to exposure in each generation varied, but included increased incidence of larval deformities, reduced larval growth and survival, impaired immune function, skewed sex ratios, ovarian atresia, reduced egg production, and altered gene expression. Additionally, exposed fish exhibited differences in DNA methylation in selected genes, across all three generations, indicating epigenetic transfer of effects. These findings suggest that assessments across multiple generations are key to determining the full magnitude of adverse effects from contaminant exposure in early life.Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational and transgenerational effects, respectively), particularly in estuarine fishes. To investigate this possibility, we exposed inland silversides (Menidia beryllina) to environmentally relevant (low ng/L) concentrations of ethinylestradiol, bifenthrin, trenbolone, and levonorgestrel from 8 hpf to 21 dph. We then measured development, immune response, reproduction, gene expression, and DNA methylation for two subsequent generations following the exposure. Larval exposure (F0) to each compound resulted in negative effects in the F0 and F1 generations, and for ethinylestradiol and levonorgestrel, the F2 also. The specific endpoints that were responsive to exposure in each generation varied, but included increased incidence of larval deformities, reduced larval growth and survival, impaired immune function, skewed sex ratios, ovarian atresia, reduced egg production, and altered gene expression. Additionally, exposed fish exhibited differences in DNA methylation in selected genes, across all three generations, indicating epigenetic transfer of effects. These findings suggest that assessments across multiple generations are key to determining the full magnitude of adverse effects from contaminant exposure in early life.
Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational and transgenerational effects, respectively), particularly in estuarine fishes. To investigate this possibility, we exposed inland silversides (Menidia beryllina) to environmentally relevant (low ng/L) concentrations of ethinylestradiol, bifenthrin, trenbolone, and levonorgestrel from 8 hpf to 21 dph. We then measured development, immune response, reproduction, gene expression, and DNA methylation for two subsequent generations following the exposure. Larval exposure (F0) to each compound resulted in negative effects in the F0 and F1 generations, and for ethinylestradiol and levonorgestrel, the F2 also. The specific endpoints that were responsive to exposure in each generation varied, but included increased incidence of larval deformities, reduced larval growth and survival, impaired immune function, skewed sex ratios, ovarian atresia, reduced egg production, and altered gene expression. Additionally, exposed fish exhibited differences in DNA methylation in selected genes, across all three generations, indicating epigenetic transfer of effects. These findings suggest that assessments across multiple generations are key to determining the full magnitude of adverse effects from contaminant exposure in early life.
Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little is known about the potential for toxicant exposures in a parental (F0) generation to affect unexposed F1 or F2 generations (multigenerational and transgenerational effects, respectively), particularly in estuarine fishes. To investigate this possibility, we exposed inland silversides ( ) to environmentally relevant (low ng/L) concentrations of ethinylestradiol, bifenthrin, trenbolone, and levonorgestrel from 8 hpf to 21 dph. We then measured development, immune response, reproduction, gene expression, and DNA methylation for two subsequent generations following the exposure. Larval exposure (F0) to each compound resulted in negative effects in the F0 and F1 generations, and for ethinylestradiol and levonorgestrel, the F2 also. The specific endpoints that were responsive to exposure in each generation varied, but included increased incidence of larval deformities, reduced larval growth and survival, impaired immune function, skewed sex ratios, ovarian atresia, reduced egg production, and altered gene expression. Additionally, exposed fish exhibited differences in DNA methylation in selected genes, across all three generations, indicating epigenetic transfer of effects. These findings suggest that assessments across multiple generations are key to determining the full magnitude of adverse effects from contaminant exposure in early life.
Author Roark, Hunter K
Major, Kaley M
Brander, Susanne M
White, J. Wilson
Connon, Richard E
DeCourten, Bethany M
Li, Jie
Mehinto, Alvine C
Forbes, Joshua P
Burns, Nathan P
AuthorAffiliation Department of Environmental and Molecular Toxicology
Department of Fisheries and Wildlife, Coastal Oregon Marine Experiment Station
Bioinformatics Core, Genome Center
Department of Biology and Marine Biology
University of California, Davis
Department of Anatomy, Physiology & Cell Biology, School of Veterinary Medicine
AuthorAffiliation_xml – name: Department of Anatomy, Physiology & Cell Biology, School of Veterinary Medicine
– name: Bioinformatics Core, Genome Center
– name: Department of Fisheries and Wildlife, Coastal Oregon Marine Experiment Station
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  givenname: Bethany M
  orcidid: 0000-0002-1880-6809
  surname: DeCourten
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  organization: Department of Anatomy, Physiology & Cell Biology, School of Veterinary Medicine
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  givenname: Joshua P
  surname: Forbes
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  organization: Department of Biology and Marine Biology
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  organization: Department of Fisheries and Wildlife, Coastal Oregon Marine Experiment Station
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32989987$$D View this record in MEDLINE/PubMed
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Snippet Many pollutants cause endocrine disruption in aquatic organisms. While studies of the direct effects of toxicants on exposed organisms are commonplace, little...
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StartPage 13849
SubjectTerms abnormal development
Animals
Aquatic organisms
bifenthrin
Contaminants
Deoxyribonucleic acid
DNA
DNA methylation
Ecotoxicology and Public Health
Egg production
Endocrine disruptors
Endocrine Disruptors - toxicity
Environmental effects
Epigenetics
Estuaries
estuarine fish
Estuarine pollution
Ethinyl Estradiol - toxicity
Ethinylestradiol
Exposure
Fishes
Gene expression
Immune response
Immune system
Insecticides
larvae
Larval development
Menidia beryllina
Pollutants
Reproduction
technology
toxic substances
Toxicants
Trenbolone
Water Pollutants, Chemical - toxicity
Title Multigenerational and Transgenerational Effects of Environmentally Relevant Concentrations of Endocrine Disruptors in an Estuarine Fish Model
URI http://dx.doi.org/10.1021/acs.est.0c02892
https://www.ncbi.nlm.nih.gov/pubmed/32989987
https://www.proquest.com/docview/2466059724
https://www.proquest.com/docview/2447308267
https://www.proquest.com/docview/2574339011
Volume 54
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