Pesticide-induced multigenerational effects on amphibian reproduction and metabolism

Abstract

Underlying drivers of species extinctions need to be better understood for effective conservation of biodiversity. Nearly half of all amphibian species are at risk of extinction, and pollution may be a significant threat as seasonal high-level agrochemical use overlaps with critical windows of larval development. The potential of environmental chemicals to reduce the fitness of future generations may have profound ecological and evolutionary implications. This study characterized effects of male developmental exposure to environmentally relevant concentrations of the anti-androgenic pesticide linuron over two generations of offspring in Xenopus tropicalis frogs. The adult male offspring of pesticide-exposed fathers (F1) showed reduced body size, decreased fertility, and signs of endocrine system disruption. Impacts were further propagated to the grand-offspring (F2), providing evidence of transgenerational effects in amphibians. The adult F2 males demonstrated increased weight and fat body palmitoleic-to-palmitic acid ratio, and decreased plasma glucose levels. The study provides important cross-species evidence of paternal epigenetic inheritance and pollutant-induced transgenerational toxicity, supporting a causal and complex role of environmental contamination in the ongoing species extinctions, particularly of amphibians.

Keywords: Anti-androgenic; Frog; Linuron; Paternal epigenetic inheritance; SCD-1; Transgenerational; Xenopus tropicalis.

Graphical Abstract

Fig. 1. The overall study design and main findings.

Fig. 2. Histomicrographs showing seminiferous tubules (– – –) from 24-month-old Xenopus tropicalis

A-B) F1 control male with all different germ cell stages and clearly structured, organized and distinguished seminiferous tubules with a thin layer of interstitial connective tissue and C) F1 male in the linuron group containing an elevated number of spermatogonia. D) F1 male in the linuron group with disorganized germinal epithelium in the seminiferous tubules, germ cells at different developmental stages scattered across the tubule, and thickened interstitial connective tissue. Arrows indicate interstitial connective tissue. Magnification 40× (A-B) and 20× (C-D). Spg = spermatogonia, Spc = spermatocytes, Spt = spermatids, Spz = spermatozoa.