The Priming Impacts of Early Hypoxia Exposure in Abalone Parents Are Transmitted to Offspring

The early environmental disturbances may have lasting effects on the sensitivity and acclimation abilities of organisms in later life stages or even in subsequent generations. However, measuring the responses of marine species with long generation times across multiple generations is challenging. Here, we investigated the inter-generational carryover effects of early hypoxia exposure on Pacific abalone (Haliotis discus hannai), which takes two years to reach reproductive maturity. A five-year study revealed that embryonic hypoxia exposure in abalone parents (F₀) has long-lasting effects, which makes offspring (F₁) have higher specific growth rates and hypoxia tolerance despite these offspring having never been exposed to hypoxia. Embryonic hypoxia exposure did not reduce the genetic diversity (Na, Ne, I, Ho, He and F) of abalone between two generations, nor did it result in genetic differentiation (Fst and Nei's genetic distance) within a single generation. However, natural selection during the two-year culture period may have favoured F₀ individuals with superior fitness traits to survive, ultimately driving genetic divergence among the F₁ generation. Furthermore, differentially expressed genes (e.g., mthfr and shmt1) that reflect the single-generational, inter-generational, and multi-generational effects were involved in methylenetetrahydrofolate reductase activity and one carbon pool by folate. These genes might mediate the process by which F₀ embryonic hypoxia exposure alters the adaptive traits of the F₁ generation. This study revealed that the priming impacts of early hypoxia exposure might persist across generations through both genetic and non-genetic mechanisms, providing insights for protecting marine organisms under global climate change.