Periodic Reporting for period 1 - PEARL (Novel biomarkers of pollution in avian models: Paternally-transmitted Epigenetic Alterations in Response to heavy metaL exposure)
Reporting period: 2023-04-03 to 2025-04-02
Non-genetic inheritance encompasses the many ways in which changes in parental environment affect the next generations (so-called parental effects), as well as the parent-to offspring transmission of epigenetic marks. While paternal effects have sparked an interest in medical research over the past decade, the field is still in its infancy in evolutionary ecology research. Yet, paternal non-genetic inheritance can have strong evolutionary applications, particularly regarding a species’ capacity to respond to environmental changes. Heavy metal pollution is among the major environmental pressures currently affecting not only terrestrial biodiversity but also human health. As such, heavy metal pollution presents an increasingly important concern worldwide.
PEARL’s central hypothesis postulates that metal pollution, even at low doses, can alter the sperm quality of male birds, as example at the epigenetic level (DNA methylation), which would then result in observable phenotypic alterations in the offspring. The objectives of this project were trifold: 1) to quantify the effects of heavy metal pollution exposure on physiology and behavior, 2) to quantify the effects of heavy metal pollution on sperm morphology, 3) to determine whether paternal effects of pollution are detectable in offspring of contaminated fathers.
To do so, we combined an experimental approach with a captive Japanese quail population, and experiments in a wild population of songbirds breeding along a metal pollution gradient in Harjavalta, Southwestern Finland. Our primary finding is that ecologically realistic concentrations of a ubiquitous and persistent metal, lead, can induce effects on the offspring of exposed males, with important consequences for their survival. Our now work calls for future research evaluating the extent to which paternal effects contribute to global parental effects and how this can affect the offspring’s ability to respond not only to contaminants but also other anthropogenic pressures.
PEARL’s central hypothesis postulates that metal pollution, even at low doses, can alter the sperm quality of male birds, as example at the epigenetic level (DNA methylation), which would then result in observable phenotypic alterations in the offspring. The objectives of this project were trifold: 1) to quantify the effects of heavy metal pollution exposure on physiology and behavior, 2) to quantify the effects of heavy metal pollution on sperm morphology, 3) to determine whether paternal effects of pollution are detectable in offspring of contaminated fathers.
To do so, we combined an experimental approach with a captive Japanese quail population, and experiments in a wild population of songbirds breeding along a metal pollution gradient in Harjavalta, Southwestern Finland. Our primary finding is that ecologically realistic concentrations of a ubiquitous and persistent metal, lead, can induce effects on the offspring of exposed males, with important consequences for their survival. Our now work calls for future research evaluating the extent to which paternal effects contribute to global parental effects and how this can affect the offspring’s ability to respond not only to contaminants but also other anthropogenic pressures.
Our primary objective was to assess the existence of paternal effects of pollution in birds. We combined two approaches: 1) a two-generation experiment of lead exposure in control conditions in captive Japanese quails, and 2) in-situ data collected from songbirds breeding along a metal pollution gradient in Southwestern Finland. We exposed quail males to an environmentally relevant dose of lead (reflecting levels measured in European ground-feeding birds) and monitored the consequences of this exposure on their fertility and their behavior, as well as on the body condition, physiology and behavior of the offspring. We found no difference in corticosterone levels in blood but found that sperm morphology was altered in exposed quails. In addition, our results revealed that lead exposure can decrease fearfulness in birds, making them more vulnerable to new threats, and this effect persisted in the non-exposed offspring of contaminated fathers, that exhibited altered growth, fear behavior and cognitive abilities. In addition, we monitored great tit (Parus major) and pied flycatcher (Ficedula hypoleuca) populations breeding in the Harjavalta smelter area in South Western Finland (which constitutes a natural gradient of metal pollution exposure). We found evidence of species-specific changes in sperm morphology - potentially explaining the historically low reproductive success observed in polluted areas. In addition, we quantified parental care in flycatchers but found no evidence of an effect of heavy metals on this behavior.
We found that exposure to an ecologically relevant concentration of lead induced adverse effects on fitness-relevant behaviors, such as a reduction in fearfulness towards predators, which can have critical consequences on individual survival. However, these behavioral changes did not seem to be mediated by typical ‘stress’ hormones (i.e. corticosterone). Most importantly, our results highlighted that paternal lead exposure causes detectable alterations in offspring behavior and cognition. Our ongoing analyses will now follow up on these results to connect sperm molecular markers with these observed changes. In wild conditions, we identified modifications in the sperm cell morphology of male songbirds breeding in polluted areas that could affect their fertility negatively, explaining the low breeding success historically observed in polluted areas, and constitute a pathway of transmission of paternal effects.
Overall, PEARL has been one of the first initiatives to have thoroughly investigated the male’s role in transmitting environmental effects in non-mammalian animals. By combining a wild and a captive approach, we provided novel insights into the potential of lead contamination to cause adverse effects on wildlife health over generations. Ultimately, the project sheds light on biomarkers of lead exposure that have potential to be passed on over generations, highlighting possible targets for population monitoring. In this context, PEARL has a strong potential to interest the scientific community as well as policy makers.
Overall, PEARL has been one of the first initiatives to have thoroughly investigated the male’s role in transmitting environmental effects in non-mammalian animals. By combining a wild and a captive approach, we provided novel insights into the potential of lead contamination to cause adverse effects on wildlife health over generations. Ultimately, the project sheds light on biomarkers of lead exposure that have potential to be passed on over generations, highlighting possible targets for population monitoring. In this context, PEARL has a strong potential to interest the scientific community as well as policy makers.