Life-stage specificity and temporal variations in transcriptomes and DNA methylomes of the reef coral Pocillopora damicornis in response to thermal acclimation

Understanding the acclimation capacity of reef corals across generations to thermal stress and its underlying molecular underpinnings could provide insights into their resilience and adaptive responses to future climate change. Here, we acclimated adult brooding coral Pocillopora damicornis to high temperature (32 °C vs. 29 °C) for three weeks and analyzed the changes in phenotypes, transcriptomes and DNA methylomes of adult corals and their brooded larvae. Results showed that although adult corals did not show noticeable bleaching after thermal exposure, they released fewer but larger larvae. Interestingly, larval cohorts from two consecutive lunar days exhibited contrasting physiological resistance to thermal stress, as evidenced by the divergent responses of area-normalized symbiont densities and photochemical efficiency to thermal stress. RNA-seq and whole-genome bisulfite sequencing revealed that adult and larval corals mounted distinct transcriptional and DNA methylation changes in response to thermal stress. Remarkably, larval transcriptomes and DNA methylomes also varied greatly among lunar days and thermal treatments, aligning well with their physiological metrics. Overall, our study shows that changes in transcriptomes and DNA methylomes in response to thermal acclimation can be highly life stage-specific. More importantly, thermally-acclimated adult corals could produce larval offspring with temporally contrasting photochemical performance and thermal resilience, and such variations in larval phenotypes are associated with differential transcriptomes and DNA methylomes, and are likely to increase the likelihood of reproductive success and plasticity of larval propagules under thermal stress. [Display omitted] •Adult corals release fewer but larger larvae after heat acclimation.•Larval cohorts show temporally variable physiological traits and thermal resilience.•Responses of transcriptomes and DNA methylomes to heat are highly stage-specific.•Variations in larval Fv/Fm are correlated with differential transcriptomes and DNA methylomes.