Little is known of the capacity that marine metazoans have to evolve under rapid pCO₂ changes. Consequently, we reared a marine polychaete, Ophryotrocha labronica, previously cultured for approximately 33 generations under a low/variable pH regime, under elevated and low pCO₂ for six generations. The strain used was found to be tolerant to elevated pCO₂ conditions. In generations F1 and F2 females’ fecundity was significantly lower in the low pCO₂ treatment. However, from generation F3 onwards there were no differences between pCO₂ treatments, indicating that trans‐generational effects enabled the restoration and maintenance of reproductive output. Whilst the initial fitness recovery was likely driven by trans‐generational plasticity (TGP), the results from reciprocal transplant assays, performed using F7 individuals, made it difficult to disentangle between whether TGP had persisted across multiple generations, or if evolutionary adaptation had occurred. Nonetheless, both are important mechanisms for persistence under climate change. Overall, our study highlights the importance of multi‐generational experiments in more accurately determining marine metazoans’ responses to changes in pCO₂, and strengthens the case for exploring their use in conservation, by creating specific pCO₂ tolerant strains of keystone ecosystem species.

Elevated CO₂ levels associated with ocean acidification (OA) have been shown to alter behavioural responses in coral reef fishes. However, all studies to date have used stable pCO₂ treatments, not considering the substantial diel pCO₂ variation that occurs in shallow reef habitats. Here, we reared juvenile damselfish, Acanthochromis polyacanthus, and clownfish, Amphiprion percula, at stable and diel cycling pCO₂ treatments in two experiments. As expected, absolute lateralization of A. polyacanthus and response to predator cue of Am. percula were negatively affected in fish reared at stable, elevated pCO₂ in both experiments. However, diel pCO₂ fluctuations reduced the negative effects of OA on behaviour. Importantly, in experiment two, behavioural abnormalities that were present in fish reared at stable 750 µatm CO₂ were largely absent in fish reared at 750 ± 300 µatm CO₂. Overall, we show that diel pCO₂ cycles can substantially reduce the severity of behavioural abnormalities caused by elevated CO₂. Thus, past studies may have over-estimated the impacts of OA on the behavioural performance of coral reef fishes. Furthermore, our results suggest that diel pCO₂ cycles will delay the onset of behavioural abnormalities in natural populations.

Marine ecosystems are currently in a state of flux, with ocean warming and acidification occurring at unprecedented rates. Phenotypic plasticity underpins acclimatory responses by shifting the mean phenotype in a population, which may buffer the negative effects of global change. However, little is known about how phenotypic plasticity evolves across multiple generations. We tested this by reciprocally-transplanting the polychaeteOphryotrocha labronicabetween control and global change scenarios (ocean warming and acidification in isolation and combined) over five generations. By comparing the reaction norms of four life-history traits across generations, we show that juvenile developmental rate in the combined scenario was the only trait that changed its plastic response across generations when transplanted back to control conditions, and that adaptive plasticity was conserved in most traits, despite significant levels of selection and strong declines in individual fitness in the multi-generational exposure. We suggest the change in level of plasticity in the combined scenario is caused by differential allocation of energy between the mean and the plasticity of the trait along the multigenerational exposure. The ability to maintain within-generational levels of plasticity under global change scenarios has important eco-evolutionary and conservation implications, which are examined under the framework of assisted evolution programs.

Human‐assisted, trans‐generational exposure to ocean warming and acidification has been proposed as a conservation and/or restoration tool to produce resilient offspring. To improve our understanding of the need for and the efficacy of this approach, we characterized life‐history and physiological responses in offspring of the marine polychaete Ophryotrocha labronica exposed to predicted ocean warming (OW: + 3°C), ocean acidification (OA: pH −0.5) and their combination (OWA: + 3°C, pH −0.5), following the exposure of their parents to either control conditions (within‐generational exposure) or the same conditions (trans‐generational exposure). Trans‐generational exposure to OW fully alleviated the negative effects of within‐generational exposure to OW on fecundity and egg volume and was accompanied by increased metabolic activity. While within‐generational exposure to OA reduced juvenile growth rates and egg volume, trans‐generational exposure alleviated the former but could not restore the latter. Surprisingly, exposure to OWA had no negative impacts within‐ or trans‐generationally. Our results highlight the potential for trans‐generational laboratory experiments in producing offspring that are resilient to OW and OA. However, trans‐generational exposure does not always appear to improve traits and therefore may not be a universally useful tool for all species in the face of global change.

Little is known about the life-history trade-offs and limitations, and the physiological mechanisms that are associated with phenotypic adaptation to future ocean conditions. To address this knowledge gap, we investigated the within- and trans-generation life-history responses and aerobic capacity of a marine polychaete, Ophryotrocha labronica, to elevated temperature and elevated temperature combined with elevated salinity for its entire lifespan. In addition, transplants between treatments were carried out at both the egg mass and juvenile stage to identify the potential influence of developmental effects. Within-generation, life-history trade-offs caused by the timing of transplant were only detected under elevated temperature combined with elevated salinity conditions. Polychaetes transplanted at the egg mass stage grew slower and had lower activities of energy metabolism enzymes but reached a larger maximum body size and lived longer when compared with those transplanted as juveniles. Trans-generation exposure to both elevated temperature and elevated temperature and salinity conditions restored 20 and 21% of lifespan fecundity, respectively. Trans-generation exposure to elevated temperature conditions also resulted in a trade-off between juvenile growth rates and lifespan fecundity, with slower growers showing greater fecundity. Overall, our results suggest that future ocean conditions may select for slower growers. Furthermore, our results indicate that life-history trade-offs and limitations will be more prevalent with the shift of multiple global change drivers, and thus there will be greater constraints on adaptive potential. This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.