Persistent maternal memory, transient offspring effects: the temporal and sex-specific architecture of heritable heat-stress responses in zebrafish

Maternal memory and offspring effects of environmental experiences, particularly heat stress, form a complex architecture in zebrafish populations. In a study examining the transmission of environmental information through egg provisioning, researchers followed the effects of a two-week heat wave across successive matings and two unexposed generations, tracking gonad responses, maternal RNA, embryo survival, larval behavior, adult stress resistance, and liver transcriptomes.

The oocytes of the maternal generation retained a pronounced heat-shock signature across several weeks and multiple spawning events, with some functional components persisting into the oocytes of the subsequent generation. This maternal RNA signature differed fundamentally from somatic responses, which varied in sex and timepoint specificity, with minor intergenerational metabolic and stress effects in males.

Parental heat exposure also impacted offspring survival, larval behavior, and thermal tolerance, with these effects weakening across successive reproductive events and generations. The findings reveal distinct temporal dynamics in the germline versus the developing and adult soma, with persistent molecular information in maternal provisioning coexisting with fading offspring phenotypes.

This selective retention and fading of parental information align with theoretical predictions about the diminishing value of inherited information, potentially dictating cross-generational population-level responses to extreme events.