Warming and pollution interact to alter energy transfer efficiency, performance and fitness across generations in zebrafish (Danio rerio)

Sci Total Environ. 2024 Feb 20:912:168942. doi: 10.1016/j.scitotenv.2023.168942. Epub 2023 Dec 2.

Abstract

Energy transfer efficiency across different trophic levels, from food to new biomass, can determine population dynamics and food-web function. Here we show that the energy needed to produce a unit of new biomass increases with warming and exposure to bisphenol A (BPA), an endocrine disrupting compound. These environmental effects are at least partially transmitted across generations via DNA methylation. We raised parental (F0) and their offspring (F1) zebrafish (Danio rerio) of two genotypes (DNA methyltransferase 3a knock-out [DNMT3a-/-] and wild type [DNMT3a+/+]) at different temperatures (24 and 30 °C), with and without BPA (0 and 10 μg l-1) to test whether the effects of BPA are i) temperature specific, ii) mediated by DNA methylation, and iii) transmitted across generations even if offspring are not exposed. All experimental factors interacted to influence growth in length and mass, and metabolic rates with the result that wild-type F0 and F1 fish experienced the greatest energetic cost of growth under warm conditions in the presence of BPA. However, this response was not observed in DNMT3a-/- fish, indicating that DNA methylation is at least partly responsible for mediating these effects. Under the same conditions (warm + BPA) wild-type parents had reduced swimming performance, and reduced fecundity, and offspring embryonic survival was reduced significantly; genotype affected these responses significantly. Our results indicate that the conditions that are becoming increasingly common globally - warming and endocrine disrupting compounds from plastic pollution and production - can have detrimental effects on energy transfer efficiency and thereby potentially on food-web structure. These effects can be transmitted across generations even if offspring are not exposed to the pollutant, and are likely to have ramifications for conservation and fisheries.

Keywords: Bisphenol A; Climate change; DNA methylation; Endocrine disruption; Epigenetics; Global heating.

MeSH terms

  • Animals
  • Benzhydryl Compounds / metabolism
  • Benzhydryl Compounds / toxicity
  • DNA Methylation*
  • Swimming
  • Zebrafish* / physiology

Substances

  • Benzhydryl Compounds