Warming during embryogenesis induces a lasting transcriptomic signature in fishes

Ripley, Daniel M.; Garner, Terence; Hook, Samantha A.; Veríssimo, Ana; Grunow, Bianka; Moritz, Timo; Clayton, Peter; Shiels, Holly A.; Stevens, Adam

doi:10.1016/j.scitotenv.2023.165954

Cited by 4 publications

(2 citation statements)

References 64 publications

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“…Gametes are vulnerable to environmental temperature, with consequences for offspring traits-especially in externally fertilizing speciessuch as reduced size and swimming performance in lavaret (Coregonus lavaretus) larvae sired by sperms exposed to warming [82]. Environmental cues experienced during embryogenesis are also expected to greatly, and often irreversibly, affect the phenotype through developmental WGP [25], with warming during embryogenesis impacting later fish life traits and transcriptional signatures [83][84][85]. However, embryonic WGP usually shows adaptive rather than maladaptive consequences, with fish performing better in the warmer environment if exposed to elevated temperatures during embryogenesis [83,84].…”

Section: Discussionmentioning

confidence: 99%

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

Bonzi,

Spinks,

Donelson

et al. 2024

Proc. R. Soc. B.

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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.

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Section: Discussionmentioning

confidence: 99%

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

Bonzi,

Spinks,

Donelson

et al. 2024

Proc. R. Soc. B.

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“…Elements of complex systems are co-ordinated by higher order interactions 9 . This coordination can be assessed using entropy 13 , which measures network structure, combined with measuring network path directness. They have been used to examine early human embryology 14,15 and hypergraph topology has been used to assess mechanism in neural, ecological and social systems 11 .…”

Section: Introductionmentioning

confidence: 99%

Analysis of higher order interactions quantifies co-ordination in the epigenome and reveals novel biological relationships in Kabuki syndrome

Cuvertino,

Garner,

Martirosian

et al. 2024

Preprint

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Complex direct and indirect relationships between multiple variables are a characteristic of all natural systems and are defined as higher order interactions (HOIs). Traditional differential and network analyses fail to account for the richness of omic datasets and miss HOIs. We investigated genome-wide peripheral blood DNA methylation data from Kabuki syndrome type 1 (KS1) and control individuals, identified 2,002 differentially methylated points (DMPs), and inferred 17 differentially methylated regions, which represent only 189 DMPs. We followed these results with quantification of HOIs by applying hypergraph network models on all the CpGs in the two datasets and revealed differences in co-ordination of the DMPs along with lower entropy and higher co-ordination of the peripheral epigenome in KS1 implying reduced network complexity. We demonstrate that the hypergraph approach captures substantially more information, enables factoring trans-relationships, and identifies biologically relevant pathways that escape the standard analyses. These findings construct the basis of a suitable model that is not computationally intensive for the analysis of the organisation of the epigenome in rare diseases. This approach can be applied to other types of omic datasets, and to other fields of science and medicine to investigate mechanism in big data.

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