Under pressure-exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions.

Background: Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. Changing partners may enhance breeding success but lead to more physiological costs. Methods: To investigate the physiological costs of reproduction upon partner changes, we measured and compared 21 biomarkers related to telomere dynamics, oxidative stress, inflammation, hematology, nutritional status, and muscle damage. We used a longitudinal approach with gannets (n = 38) over three contrasting years (2017, 2018 and 2019). Results: Our results suggest that annual breeding conditions exert a greater influence on physiological changes than partnership status. Individuals that changed partner experienced greater short-term stress than retained partners. This transient increase in stress was marked by short-term increases in oxidative lipid damage, lower antioxidant capacity, signs of inflammation, and greater weight loss than individuals that retained partners. During favorable conditions, individuals that changed mates had stabilized telomere length, decreased antioxidant capacity, glucose concentration, and muscle damage, along with increased oxygen transport capacity. Conversely, unfavorable breeding conditions led to increased telomere attrition, stabilized antioxidant capacity, decreased inflammation susceptibility, diminished oxygen transport capacity, and increased muscle damage. In the cases where partners were retained, distinct physiological changes were observed depending on the year's conditions, yet the telomere dynamics remained consistent across both partnership status categories. During the favorable year, there was an increase in unsaturated fatty acids and oxygen transport capacity in the blood, coupled with a reduction in inflammation potential and protein catabolism. In contrast, during the unfavorable year in the retained mates, we observed an increase in oxidative DNA damage, antioxidant capacity, weight loss, but a decrease in inflammation susceptibility as observed in changed mates. Discussion: Our study shows that behavioral flexibility such as mate switching can help seabirds cope with the challenges of food scarcity during reproduction, but these coping strategies may have a negative impact on physiological status at the individual level. In addition, the marked reduction in telomere length observed during harsh conditions, coupled with the stabilization of telomere length in favorable conditions, highlights the long-term physiological impact of annual breeding conditions on seabirds. These findings underscore the effect on their potential survival and fitness, emphasizing that the influence of annual breeding conditions is greater than that of partnership status.

Thermal tolerance and fish heart integrity: fatty acids profiles as predictors of species resilience.

The cardiovascular system is a major limiting system in thermal adaptation, but the exact physiological mechanisms underlying responses to thermal stress are still not completely understood. Recent studies have uncovered the possible role of reactive oxygen species production rates of heart mitochondria in determining species' upper thermal limits. The present study examines the relationship between individual response to a thermal challenge test (CTmax), susceptibility to peroxidation of membrane lipids, heart fatty acid profiles and cardiac antioxidant enzyme activities in two salmonid species from different thermal habitats (Salvelinus alpinus, Salvelinus fontinalis) and their hybrids. The susceptibility to peroxidation of membranes in the heart was negatively correlated with individual thermal tolerance. The same relationship was found for arachidonic and eicosapentaenoic acid. Total H2O2 buffering activity of the heart muscle was higher for the group with high thermal resistance. These findings underline a potential general causative relationship between sensitivity to oxidative stress, specific fatty acids, antioxidant activity in the cardiac muscle and thermal tolerance in fish and likely other ectotherms. Heart fatty acid profile could be indicative of species resilience to global change, and more importantly the plasticity of this trait could predict the adaptability of fish species or populations to changes in environmental temperature.

Life-history trade-offs and limitations associated with phenotypic adaptation under future ocean warming and elevated salinity.

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'.

Hybridization between char species (Salvelinus alpinus and Salvelinus fontinalis): a fast track for novel allometric trajectories.

Hybridization between closely related species can generate genetic and phenotypic variation, providing valuable biological material to assess the physiological impact of the structural or functional variability of different organs. In the present study, we examined growth rates of various organs and whole body in brook char, Arctic char and their reciprocal hybrids over a period of 281 days. Parental species achieved significantly higher body mass than their hybrids. Hybridization significantly reduced the relative size of the heart, liver and spleen. The relative size of pyloric caeca did not differ among the four groups. The observed lower growth performance of the hybrids compared to parental species strongly suggests that divergence in the relative size of digestive organs, liver and heart partly dictate growth capacity. Our results also suggest that the increased variability achieved through hybridization may prove useful in a genetic selection program.

Thermal tolerance and thermal sensitivity of heart mitochondria: Mitochondrial integrity and ROS production.

Cardiac mitochondrial metabolism provides 90% of the ATP necessary for the contractile exertion of the heart muscle. Mitochondria are therefore assumed to play a pivotal role in heart failure (HF), cardiovascular disease and ageing. Heat stress increases energy metabolism and oxygen demand in tissues throughout the body and imposes a major challenge on the heart, which is suspected of being the first organ to fail during heat stress. The underlying mechanisms inducing heart failure are still unclear. To pinpoint the processes implicated in HF during heat stress, we measured mitochondrial respiration rates and hydrogen peroxide production of isolated Arctic char (Salvelinus alpinus) heart mitochondria at 4 temperatures: 10°C (acclimation), 15°C, 20°C and 25°C (just over critical maximum). We found that at temperature ranges causing the loss of an organism's general homeostasis (between 20°C and 25°C) and with a substrate combination close to physiological conditions, the heat-induced increase in mitochondrial oxygen consumption levels off. More importantly, at the same state, hydrogen peroxide efflux increased by almost 50%. In addition, we found that individuals with low mitochondrial respiration rates produced more hydrogen peroxide at 10°C, 15°C and 20°C. This could indicate that individuals with cardiac mitochondria having a low respiratory capacity, have a more fragile heart and will be more prone to oxidative stress and HF, and less tolerant to temperature changes and other stressors. Our results show that, at temperatures close to the thermal limit, mitochondrial capacity is compromised and ROS production rates increase. This could potentially alter the performance of the cardiac muscle and lead to heat-induced HF underlining the important role that mitochondria play in setting thermal tolerance limits.

Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan?

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.

Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification?

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.