Consequences of directly- and indirectly-experienced heat stress in a mutagenic environment

Abstract

Climate change increases the frequency and duration of heat events. Negative effects of heat stress may be exacerbated through the action of social metabolites between aquatic animals. Whilst early life stages are vulnerable to stress-induced damage, they deploy cellular mechanisms to protect cells against mutagens such as ultraviolet rays (UV). Little is known about the fate of fish embryos which have experienced heat stress in a mutagenic environment. The present study exposed zebrafish embryos to one of three stress history treatments consisting of direct heat stress (TS+UV), the social context of heat stress via social metabolites (SM+UV), and their combination in TS+SM+UV before a UVB/UVA damage/repair assay. We measured phenotypic and transcriptomic responses to these treatments, and estimated mutational damage through DNA mutation frequencies and RNA integrity values. Compared to UV-treated controls (C+UV), the social context of heat stress history preceding the UV assay altered keratin and cell structuring-related pathways, associated with longer embryos with over-developed pericardia displaying behavioural hypoactivity. Relative to C+UV, direct heat stress history preceding UV exposure had a hormetic effect by stimulating the cellular stress response and facilitating DNA repair, which rescued embryos from subsequent UV damage and improved their apparent fitness. However, heat stress combined with social metabolites overwhelmed embryos in the UV assay, which annihilated the hormetic effect, introduced mutations, and lowered their apparent fitness. Whilst generated in the laboratory, these findings provide an important baseline for understanding the consequences of heat stress history in natural environments, where heat stress occurs within a social context.HighlightsHeat stress had a hormetic effect against UV damage, by stimulating the heat shock response, antioxidants, and DNA repair.The heat hormetic effect protected and/or rescued embryos from UV damage by reducing single nucleotide variants observed in RNA, lowering malformations, and accelerating development.Heat-stressed embryos released social metabolites that initiated keratin, immune, and cellular structuring responses in receivers, in turn increasing body sizes but without reducing UV-induced malformations.Heat combined with social metabolites overwhelmed embryos in response to UV, reducing fitness-relevant performance.Heat stress during early embryogenesis led to differential fitness-relevant outcomes showing a nonlinear relationship with stress intensity.Summary statementSublethal heat stress protects zebrafish embryos in a mutagenic environment, but this protective effect is lost when zebrafish embryos additionally stress each other via chemical cues.Graphical abstract