Marine biofouling by the swiftly spreading invasive mussel (Musculista senhousia) has caused serious ecological and economic consequences in the global coastal waters. However, the fate of this highly invasive fouling species in a rapidly acidifying ocean remains unknown. Here, we demonstrated the impacts of ocean acidification within and across generations, to understand whether M. senhousia has the capacity to acclimate to changing ocean conditions. During the gonadal development, exposure of mussels to elevated pCO2 caused significant decreases of survival, growth performance and condition index, and shifted the whole-organism energy budget by inflating energy expenses to fuel compensatory processes, eventually impairing the success of spawning. Yet, rapid transgenerational acclimation occurred during the early life history stage and persisted into adulthood. Eggs spawned from CO2-exposed mussels were significantly bigger compared with those from non-CO2-exposed mussels, indicating increased maternal provisioning into eggs and hence conferring larvae resilience under harsh conditions. Larvae with a prior history of transgenerational exposure to elevated pCO2 developed faster and had a higher survival than those with no prior history of CO2 exposure. Transgenerational exposure significantly increased the number of larvae completing metamorphosis. While significant differences in shell growth were no longer observed during juvenile nursery and adult grow-out, transgenerationally exposed mussels displayed improved survival in comparison to non-transgenerationally exposed mussels. Metabolic plasticity arose following transgenerational acclimation, generating more energy available for fitness-related functions. Overall, the present study demonstrates the remarkable ability of M. senhousia to respond plastically and acclimate rapidly to changing ocean conditions.
