The aquatic environment is considered as the ultimate receptacle for anthropogenic compounds that frequently exhibit a genotoxic potential towards organisms. The reproductive process could influence the recruitment rate and hence the population dynamics. The link between the loss of DNA integrity in spermatozoa following paternal exposure to genotoxicant and reproduction impairment has been recently investigated in two fish species. These results have demonstrated a decrease in the progeny survival when sperm DNA was damaged and so, possible long term effects of environmental genotoxicant in aquatic systems. Such results needed to be confirmed through studies carried out in other fish species and the contribution of oocytes to further progeny defects had to be highlighted, as recently done in aquatic invertebrates. The aim of the present study was to investigate the link between DNA damage and reproductive impairment after in vivo exposure of stickleback to the genotoxic compound methyl methane sulfonate (MMS) during the breeding season, paying special attention to the contribution of genetic load brought by each sex to the observed progeny defects. Adult fish were acclimated and were then exposed or not through water to different MMS concentrations (0 / 0.05 uM / 0.5 uM / 5 uM). In vitro fertilization were realized with mature fish and DNA damage in spermatozoa and erythrocytes (as a biomarker of exposure for both sex) were assessed by the comet assay. The morphological abnormalities of larvae due to parental MMS exposure were studied and the progeny survival at embryogenesis and larval development key stages was evaluated. Parental exposure of three-spined stickleback to the genotoxicant MMS induced a significant decrease in early life stage survival which was less important when only females were exposed. When males or both genders were exposed, DNA damage level measured in spermatozoa (p<0.01) and exposure duration (p<0.01) were shown to be significant factors associated with progeny mortality. Whatever the gender, parental exposure to MMS resulted in a 60 fold increase in progeny abnormality frequency. This study underlines that male genotoxic message transmitted to progeny could predominate on the female one. Hence, this work confirms that spermatozoa are susceptible to accumulate DNA damage under chronic and low-dose exposure to genotoxic compounds, leading to drastic offspring defects in stickelback, as recently shown in other aquatic species.