Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs

Abstract

Despite reports of parental exposure to stress promoting physiological adaptations in progeny in diverse organisms, there remains considerable debate over the significance and evolutionary conservation of such multigenerational effects. Here, we investigate four independent models of intergenerational adaptations to stress in C. elegans - bacterial infection, eukaryotic infection, osmotic stress and nutrient stress - across multiple species. We found that all four intergenerational physiological adaptations are conserved in at least one other species, that they are stress-specific, and that they have deleterious trade-offs in mismatched environments. By profiling the effects of parental bacterial infection and osmotic stress exposure on progeny gene expression across species we established a core set of 587 genes that exhibited a greater than 2-fold intergenerational change in expression in response to stress in C. elegans and at least one other species, as well as a set of 37 highly conserved genes that exhibited a greater than 2-fold intergenerational change in expression in all four species tested. Furthermore, we provide evidence suggesting that presumed adaptive and deleterious intergenerational effects are molecularly related at the gene expression level. Lastly, we found that none of the effects we detected of these stresses on C. elegans F1 progeny gene expression persisted transgenerationally three generations after stress exposure. We conclude that intergenerational responses to stress play a substantial and evolutionarily conserved role in regulating animal physiology and that the vast majority of the effects of parental stress on progeny gene expression are reversible and not maintained transgenerationally.

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

“…For example, the response to nodavirus infection is conserved between C. elegans and C. briggsae [38]. An intergenerational transcriptional response to Pseudomonas vranovensis was conserved between some, but not all species of Caenorhabditis [39]. A study looking at four different species of bacteria infecting the nematode Pristionchus pacificus also showed both similarities and differences between the transcriptional responses in the two hosts [40].…”

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

“…For example the response to nodavirus infection is conserved between C. elegans and C. briggsae (Chen et al ., 2017). An intergenerational transcriptional response to Pseudomonas vranovensis was conserved between some, but not all species of Caenorhabditis (Burton et al ., 2021). A study looking at different species of bacterial infection in the nematode Pristionchus pacificus also showed both similarities and differences between the transcriptional responses in the two hosts (Sinha et al ., 2012).…”

Cross Talk opposing view: The kids will be fine – a bit of parental stress won't affect them: Rodents are not good models for assessing transgenerational influences in humans

“…However, it should be noted that the behavioural impacts of MSUS are largely in conflict with the accepted clinical outcomes associated with childhood maltreatment, namely increased risk for emotional and behavioural problems (Schickedanz et al., 2018), as well as increased risk for type 1 diabetes (Landolt et al., 2002; Rechenberg et al., 2017). It has been proposed that offspring phenotype changes reflect intergenerational adaptations to perceived environmental adversity (stress) to boost the prospect of species survival, not too dissimilar from what has been discovered recently in Caenorhabditis elegans (Burton et al., 2021). It is possible that epigenetic inheritance exists to prepare the MSUS offspring for stressful environments, conferring them an inherent ‘resilience’ without having to undergo the same physiological and behavioural adaptations as their stressed parents.…”