Wildlife is chronically exposed to various sources of ionizing radiations, both environmental or anthropic, due to nuclear energy use, which can induce several defects in organisms. In invertebrates, reproduction, which directly impacts population dynamics, has been found to be the most radiosensitive endpoint. Understanding the underlying molecular pathways inducing this reproduction decrease can help in predicting the effects at larger scales (i.e., population). In this study, we used a life stage dependent approach in order to better understand the molecular determinants of reproduction decrease in the roundworm C. elegans. Worms were chronically exposed to 50 mGy·h−1 external gamma ionizing radiations throughout different developmental periods (namely embryogenesis, gametogenesis, and full development). Then, in addition to reproduction parameters, we performed a wide analysis of lipids (different class and fatty acid via FAMES), which are both important signaling molecules for reproduction and molecular targets of oxidative stress. Our results showed that reproductive defects are life stage dependent, that lipids are differently misregulated according to the considered exposure (e.g., upon embryogenesis and full development) and do not fully explain radiation induced reproductive defects. Finally, our results enable us to propose a conceptual model of lipid signaling after radiation stress in which both the soma and the germline participate.

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Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may, therefore, switch their reproductive mode from inbreeding to outcrossing when under environmental stress. This switch may have consequences on the demographic dynamics and evolutionary trajectory of populations. For example, it may directly influence the sex ratio of a population. However, much remains to be discovered about the mechanisms and evolutionary implications of sex ratio changes in a population in response to environmental stress. Populations of the androdioecious nematode Caenorhabditis elegans, are composed of selfing hermaphrodites and rare males. Here, we investigate the changes in the sex ratio of C. elegans populations exposed to radioactive pollution for 60 days or around 20 generations. We experimentally exposed populations to three levels of ionizing radiation (i.e., 0, 1.4, and 50 mGy.h −1 ). We then performed reciprocal transplant experiments to evaluate genetic divergence between populations submitted to different treatments. Finally, we used a mathematical model to examine the evolutionary mechanisms that could be responsible for the change in sex ratio. Our results showed an increase in male frequency in irradiated populations, and this effect increased with the dose rate. The model showed that an increase in male fertilization success or a decrease in hermaphrodite self-fertilization could explain this increase in the frequency of males. Moreover, males persisted in populations after transplant back into the control conditions. These results suggested selection favoring outcrossing under irradiation conditions. This study shows that ionizing radiation can sustainably alter the reproductive strategy of a population, likely impacting its long-term evolutionary history. This study highlights the need to evaluate the impact of pollutants on the reproductive strategies of populations when assessing the ecological risks.

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Wildlife is subject to various sources of pollution, including ionizing radiation. Adverse effects can impact organisms survival, growth, or reproduction, later affecting population dynamics. In invertebrates, reproduction, which directly impacts population dynamics, has been found to be the most radiosensitive endpoint. Understanding the underlying molecular pathways inducing this reproduction decrease can help to comprehend species-specific differences in radiosensitivity. In line with previous studies, we used a life stage dependent approach to better understand the molecular determinants of reproduction decrease, especially of gamete decrease, in the hermaphrodite roundworm Caenorhabditis elegans. Worms were chronically exposed to 50 mG-h external gamma ionizing radiations throughout different developmental periods (namely embryogenesis, gametogenesis, and full development).Conserved molecular pathways across invertebrates and vertebrates involved in reproduction processes and stress response were analyzed: apoptosis and MAP kinase Ras/ERK (MPK-1). Our results showed that these pathways are life-stage dependant, resulting from an accumulation of damages upon chronic exposure to IR throughout the whole development. The Ras/ERK pathway was found to be activated in our conditions in the pachytene region of the gonad where it induces the apoptotic pathway, but not in the ovulation zone, showing no incidence on oocyte maturation and ovulation. Additionally, no effect on germ cell proliferation was found, meaning that Ras/ERK pathway is probably not involved in this process in our conditions. Finally, a functional analysis of apoptosis revealed that the decrease of ovulation rate is due to DNA-damaged induced apoptosis which does not occur in spermatocytes. Thus, sperm decrease seem to be mediated via another mechanism, probably a decrease in germ cells proliferation speed that needs further investigation to better characterize sex-specific responses to IR exposure.