Ancestral lineages of dietary exposure to an endocrine disrupting chemical drive distinct forms of transgenerational subfertility in an insect model

• Published in: Scientific reports Vol. 14; no. 1; pp. 18153 - 16
• Main Authors: Pool, Kelsey R., Gajanayakage, Raveena Hewa, Connolly, Callum, Blache, Dominique
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 05.08.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/158; 631/158/1745; 631/1647/767; 631/443/494; 631/443/494/2732; Animals; Anthropogenic factors; Dietary Exposure - adverse effects; Drosophila melanogaster - drug effects; Endocrine disrupting chemicals; Endocrine disruptors; Endocrine Disruptors - toxicity; Epigenesis, Genetic - drug effects; Epigenetics; Exposure; Female; Females; Fertility; Fertility - drug effects; Flow cytometry; Humanities and Social Sciences; Infertility - chemically induced; Insect decline; Insects; Male; multidisciplinary; Offspring; Population decline; Population dynamics; Reproduction; Reproduction - drug effects; Science; Science (multidisciplinary); Sex Ratio; Sperm; Spermatozoa - drug effects; Transgenic plants; Reproduction; Population dynamics; Insect decline; Endocrine disrupting chemicals
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-024-67921-x

Across the globe, many species of insects are facing population decline. This is largely driven by anthropogenic changes to the environment, including the widespread exposure of invertebrates to endocrine disrupting chemicals (EDCs), which impair fertility. To test whether generations of Drosophila melanogaster born from parents exposed to a common dietary EDC, equol, could recover reproductive function, we quantified the reproductive capacity of the two subsequent generations. Using a novel suite of flow cytometry assays to assess sperm functionality in real time, we find that sperm function is compromised across three generations, even after non-exposed in individuals contribute to the breeding population. Though the sex ratio alters in response to EDC exposure, favouring the survival of female offspring, most lineages with ancestral EDC exposure exhibit persistent subfertility in both the male and female. Male offspring with ancestral EDC exposure present with reduced fertility and dysfunctional spermatozoa, whereby spermatozoa are metabolically stressed, lack DNA integrity and present with permanent epigenetic alterations. Across generations, male and female offspring demonstrate distinct patterns of reproductive characteristics, depending upon the specific lineage of EDC exposure. Our results illustrate how dietary EDCs present in agricultural plants could promote transgenerational subfertility and contribute to declining insect populations.