Timing-specific parental effects of ocean warming in a coral reef fish

Abstract

Population and species persistence in a rapidly warming world will be determined by an organism's ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the effects of two critical ontogenetic stages (juvenile development and reproduction) to the new-generation acclimation potential, by exposing the spiny chromis damselfish Acanthochromis polyacanthus to simulated ocean warming across two generations. By using hepatic transcriptomics, we discovered that the post-hatching developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offspring's response to warming. Conversely, parental reproduction and offspring embryogenesis in warmer water elicited stress response mechanisms in the offspring, with suppression of translation and mitochondrial respiration. Mismatches between parental developmental and reproductive temperatures deeply affected offspring gene expression profiles, and detrimental effects were evident when warming occurred both during parents' development and reproduction. This study reveals that the previous generation's developmental temperature contributes substantially to thermal acclimation potential during early life; however, exposure at reproduction as well as prolonged heat stress will likely have adverse effects on the species' persistence.

Keywords: climate change; gene expression; non-genetic inheritance; transcriptomics; transgenerational plasticity.

Figure 1.

Experimental design. F1 A. polyacanthus from wild-caught F0 developed either at present-day control temperature (control—blue) or elevated temperature (+1.5°C—orange) with seasonal and daily fluctuations. At 1.5 years of age, F1 individuals were paired in reciprocal sex crosses of the two thermal treatments and further exposed to control (blue rectangle) or elevated (orange rectangle) reproductive temperatures. The black ‘X’ indicates the F1 treatment that did not reproduce. F2 siblings were split after hatching into control or elevated temperatures, where they developed for 80 days.

Figure 2.

Offspring DEGs due to different thermal treatments. DEGs from pairwise comparisons between offspring with contrasting thermal histories. ‘PP’ stands for parental pair developmental thermal condition, where ‘C’ = both parents developed at control temperature, ‘h’ = one parent developed at control and one at +1.5°C and ‘H’ = both parents developed at +1.5°C. ‘R’ stands for reproductive and ‘Of’ for offspring developmental thermal conditions, where ‘C’ = control, ‘H’ = +1.5°C. The sizes of the circles are proportional to the number of DEGs between comparisons (FDR < 0.01).

Figure 3.

Expression profiles of DEGs showing interactive effects between the two parental exposure timings. DEGs were clustered based on their scaled expression profiles (Z-score). The numbers of genes per cluster are provided above each plot. In the parental pair development, ‘C’ = both parents developed at control temperature, ‘h’ = one parent developed at control and one at +1.5°C and ‘H’ = both parents developed at +1.5°C.