Cross-talk between tissues is critical for intergenerational acclimation to environmental change

Abstract

AbstractAn organism’s reaction to environmental changes is mediated by coordinated responses of multiple tissues. Additionally, parental priming may increase offsprings’ acclimation potential to changing environmental conditions. As acidification of oceans continues to intensify it is critical to assess the acclimation potential of species at the whole organismal scale. To do this we need to understand the cross-talk between tissues in regulating and responding to pH changes. Here by using a multi-tissue approach we determine the influence of 1) variation in parental behavioural tolerance and 2) parental environment, on molecular responses of their offspring in a coral reef fish. The gills and liver showed the highest transcriptional response to OA conditions in juvenile fish regardless of the parental environment, while the brain and liver showed the greatest signal of intergenerational acclimation. Key functional pathways that were altered in the brain and liver upon within-generational CO2exposure were restored to control levels when parents were exposure to OA conditions. Furthermore, the expression of a new complement of genes involved in key functions were altered in the offspring only when the parents were previously exposed to OA conditions. Therefore, previous parental conditioning to ocean acidification can reprogram tissue transcriptomic profiles of the offspring enabling them to better cope in an environment with elevated CO2levels. Overall, our results show that intergenerational plasticity is key in evolutionarily adaptation to global change and illustrates how transcriptional changes across multiple tissues integrate to facilitate organismal acclimation to OA.Significance statementWith the global climate changing rapidly, organisms need to acclimate to the new conditions to survive. Assessing the adaptive potential of complex organisms such as vertebrates is especially challenging as each tissue has its own unique function. However, acclimation of organisms to changes in their environment requires functional integration of all tissues which is usually overlooked in climate change research. Here we reveal that cross-communication between tissues is crucial in the adaptive response of organisms to future ocean conditions. Furthermore, both parental environment and parental behavioral variability influence the transcriptional reprograming of offspring tissues in response to elevated CO2. Overall, it is the integration of transcriptional changes across multiple tissues that mediates intergenerational plasticity to future changes in ocean chemistry.