Transgenerational epigenetic imprints on mate preference

Abstract

Environmental contamination by endocrine-disrupting chemicals (EDC) can have epigenetic effects (by DNA methylation) on the germ line and promote disease across subsequent generations. In natural populations, both sexes may encounter affected as well as unaffected individuals during the breeding season, and any diminution in attractiveness could compromise reproductive success. Here we examine mate preference in male and female rats whose progenitors had been treated with the antiandrogenic fungicide vinclozolin. This effect is sex-specific, and we demonstrate that females three generations removed from the exposure discriminate and prefer males who do not have a history of exposure, whereas similarly epigenetically imprinted males do not exhibit such a preference. The observations suggest that the consequences of EDCs are not just transgenerational but can be ''transpopulational'', because in many mammalian species, males are the dispersing sex. This result indicates that epigenetic transgenerational inheritance of EDC action represents an unappreciated force in sexual selection. Our observations provide direct experimental evidence for a role of epigenetics as a determinant factor in evolution.endocrine disruption ͉ vinclozolin ͉ sexual selection ͉ odor salience

Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems

“…showed that reproductive behaviors such as partner preference, and attractiveness of individuals to a conspecific mate, were modified in the third generation of descendants of animals exposed fetally to endocrine disruptors [36]. This is strong evidence that neonatal imprinting may epigenetically modify neuroendocrine genes that control reproduction.…”

“…4) Exposures may be acute (e.g., toxic spills or contamination; [47]) but more often they are chronic. 5) Transgenerational, epigenetic effects may be exerted by endocrine disruptors [5,6,36]. 6) Mechanisms of endocrine disruption are complex and include not only direct actions on nuclear hormone receptors, but also membrane steroid receptors, non-steroid receptors (e.g., neurotransmitter receptors), enzymes involved in synthesis/degradation of hormones, and other mechanisms that control levels or activity of hormones (reviewed in [63,1]).…”

“…Such observations raise concerns about permanent effects of exposures to environmental toxicants, not just to exposed individuals but also to future generations. Despite our best efforts to clean up contaminated sites, or to avoid the use of known or suspected EDCs, it may be too late if the epigenome has been affected in a manner that can be transmitted to offspring (e.g., see [36]). By understanding the neuroendocrine consequences of early EDC exposures, and whether effects are passed on by a transgenerational, epigenetic mechanism, we will be able to determine when, and how, we may be able to intervene.…”

The social environment and the epigenome

“…These observations put forward the thought-provoking notion that environmental exposures in one generation could have an impact on phenotype and disease susceptibility on generations to come. Interestingly, exposure to endocrine disruptors affect female mate preference in rodents three generation removed from the exposure, raising the possibility that epigenetics is a yet unappreciated force in evolution [Crews et al, 2007]. If environmental exposures could alter the epigenetic information in a heritable fashion then it could serve as a mechanism for environmental directed evolution.…”

Epigenetic reprogramming and imprinting in origins of disease

“…Indeed, our data [84] showed an increased incidence of precancerous lesions in the prostates of mice neonatally treated with estrogen/BPA. Anway, Skinner, and co-workers [17,85,86] have provided the first evidence that in utero exposure of male mice to vinclozolin, a pesticide and an antiandrogen, induced epigenetic changes that could be transmitted across four generations. The epigenetic modification in specific DNA sequences is associated with adult phenotypes such as decreased spermatogenic capacity and increased incidence of infertility [17]; abnormalities in the prostate, breast, kidney, testis, and immune system [85]; and aberrant mating behavior [86].…”