Ocean warming and acidification are concomitant global drivers that are currently threatening the survival of marine organisms. How species will respond to these changes depends on their capacity for plastic and adaptive responses. Little is known about the mechanisms that govern plasticity and adaptability or how global changes will influence these relationships across multiple generations. Here, we exposed the emerging model marine polychaete Ophryotrocha labronica to conditions simulating ocean warming and acidification, in isolation and in combination over five generations to identify: (i) how multiple versus single global change drivers alter both juvenile and adult life-history traits; (ii) the mechanistic link between adult physiological and fitness-related life-history traits; and (iii) whether the phenotypic changes observed over multiple generations are of plastic and/or adaptive origin. Two juvenile (developmental rate; survival to sexual maturity) and two adult (average reproductive body size; fecundity) life-history traits were measured in each generation, in addition to three physiological (cellular reactive oxygen species content, mitochondrial density, mitochondrial capacity) traits. We found that multi-generational exposure to warming alone caused an increase in juvenile developmental rate, reactive oxygen species production and mitochondrial density, decreases in average reproductive body size and fecundity, and fluctuations in mitochondrial capacity, relative to control conditions. Exposure to ocean acidification alone had only minor effects on juvenile developmental rate. Remarkably, when both drivers of global change were present, only mitochondrial capacity was significantly affected, suggesting that ocean warming and acidification act as opposing vectors of stress across multiple generations.

Regulating intracellular pH (pH i ) is critical for optimising the metabolic activity of corals, yet the mechanisms involved in pH regulation and the buffering capacity within coral cells are not well understood. Our study investigated how the presence of symbiotic dinoflagellates affects the response of pH i to P CO2 -driven seawater acidification in cells isolated from Pocillopora damicornis. Using the fluorescent dye BCECF-AM, in conjunction with confocal microscopy, we simultaneously characterised the pH i response in host coral cells and their dinoflagellate symbionts, in symbiotic and non-symbiotic states under saturating light, with and without the photosynthetic inhibitor DCMU. Each treatment was run under control (pH 7.8) and CO 2 -acidified seawater conditions (decreasing pH from 7.8 to 6.8). After 105 min of CO 2 addition, by which time the external pH (pH e ) had declined to 6.8, the dinoflagellate symbionts had increased their pH i by 0.5 pH units above control levels when in the absence of DCMU. In contrast, in both symbiotic and non-symbiotic host coral cells, 15 min of CO 2 addition (0.2 pH unit drop in pH e ) led to cytoplasmic acidosis equivalent to 0.3-0.4 pH units irrespective of whether DCMU was present. Despite further seawater acidification over the duration of the experiment, the pH i of non-symbiotic coral cells did not change, though in host cells containing a symbiont cell the pH i recovered to control levels when photsynthesis was not inhibited. This recovery was negated when cells were incubated with DCMU. Our results reveal that photosynthetic activity of the endosymbiont is tightly coupled with the ability of the host cell to recover from cellular acidosis after exposure to high CO 2 /low pH.

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.