Social, not genetic, programming of development and stress physiology of a colonial seabird.

Phenotypic differences often stem from genetic/maternal differences and/or early-life adaptations to local environmental conditions. In colonial animals, little is known on how variation in the social environment is embedded into individual phenotypes, nor what the consequences are on individual fitness. We conducted an experimental cross-fostering study on king penguins (Aptenodytes patagonicus), exchanging eggs among 134 pairs breeding in high-density (67 pairs) or low-density (67 pairs) areas of the same breeding colony. We investigated differences in parent and chick phenotypes and survival in relation to the density of their origin and foster environment. Adults breeding in colony areas of high density exhibited decreased resting behaviour and increased aggression and vigilance, increased hypometabolism during incubation fasts, and more moderate corticosterone responses shaped by exposure to chronic stressors (e.g. constant aggression by neighbours). Chick phenotypes were more influenced by the environment in which they were raised than their genetic/maternal origin. Chicks raised in high-density colonial environments showed enhanced weight gain and survival rates regardless of the density of their genetic parents' breeding areas. Our study experimentally shows advantages to breeding in colonial areas of higher breeder densities in king penguins, and highlights the importance of social settings in shaping phenotype expression in colonial seabirds.

Foster rather than biological parental telomere length predicts offspring survival and telomere length in king penguins.

Because telomere length and dynamics relate to individual growth, reproductive investment and survival, telomeres have emerged as possible markers of individual quality. Here, we tested the hypothesis that, in species with parental care, parental telomere length can be a marker of parental quality that predicts offspring phenotype and survival. In king penguins (Aptenodytes patagonicus), we experimentally swapped the single egg of 66 breeding pairs just after egg laying to disentangle the contribution of prelaying parental quality (e.g., genetics, investment in the egg) and/or postlaying parental quality (e.g., incubation, postnatal feeding rate) on offspring growth, telomere length and survival. Parental quality was estimated through the joint effects of biological and foster parent telomere length on offspring traits, both soon after hatching (day 10) and at the end of the prewinter growth period (day 105). We expected that offspring traits would be mostly related to the telomere lengths (i.e., quality) of biological parents at day 10 and to the telomere lengths of foster parents at day 105. Results show that chick survival up to 10 days was negatively related to biological fathers' telomere length, whereas survival up to 105 days was positively related to foster fathers' telomere lengths. Chick growth was not related to either biological or foster parents' telomere length. Chick telomere length was positively related to foster mothers' telomere length at both 10 and 105 days. Overall, our study shows that, in a species with biparental care, parents' telomere length is foremost a proxy of postlaying parental care quality, supporting the "telomere - parental quality hypothesis."

Habitat specialization predicts genetic response to fragmentation in tropical birds.

Habitat fragmentation is one of the most severe threats to biodiversity as it may lead to changes in population genetic structure, with ultimate modifications of species evolutionary potential and local extinctions. Nonetheless, fragmentation does not equally affect all species and identifying which ecological traits are related to species sensitivity to habitat fragmentation could help prioritization of conservation efforts. Despite the theoretical link between species ecology and extinction proneness, comparative studies explicitly testing the hypothesis that particular ecological traits underlies species-specific population structure are rare. Here, we used a comparative approach on eight bird species, co-occurring across the same fragmented landscape. For each species, we quantified relative levels of forest specialization and genetic differentiation among populations. To test the link between forest specialization and susceptibility to forest fragmentation, we assessed species responses to fragmentation by comparing levels of genetic differentiation between continuous and fragmented forest landscapes. Our results revealed a significant and substantial population structure at a very small spatial scale for mobile organisms such as birds. More importantly, we found that specialist species are more affected by forest fragmentation than generalist ones. Finally, our results suggest that even a simple habitat specialization index can be a satisfying predictor of genetic and demographic consequences of habitat fragmentation, providing a reliable practical and quantitative tool for conservation biology.

The oxidative debt of fasting: evidence for short- to medium-term costs of advanced fasting in adult king penguins.

In response to prolonged periods of fasting, animals have evolved metabolic adaptations helping to mobilize body reserves and/or reduce metabolic rate to ensure a longer usage of reserves. However, those metabolic changes can be associated with higher exposure to oxidative stress, raising the question of how species that naturally fast during their life cycle avoid an accumulation of oxidative damage over time. King penguins repeatedly cope with fasting periods of up to several weeks. Here, we investigated how adult male penguins deal with oxidative stress after an experimentally induced moderate fasting period (PII) or an advanced fasting period (PIII). After fasting in captivity, birds were released to forage at sea. We measured plasmatic oxidative stress on the same individuals at the start and end of the fasting period and when they returned from foraging at sea. We found an increase in activity of the antioxidant enzyme superoxide dismutase along with fasting. However, PIII individuals showed higher oxidative damage at the end of the fast compared with PII individuals. When they returned from re-feeding at sea, all birds had recovered their initial body mass and exhibited low levels of oxidative damage. Notably, levels of oxidative damage after the foraging trip were correlated to the rate of mass gain at sea in PIII individuals but not in PII individuals. Altogether, our results suggest that fasting induces a transitory exposure to oxidative stress and that effort to recover in body mass after an advanced fasting period may be a neglected carryover cost of fasting.

Oxidative stress and mitochondrial responses to stress exposure suggest that king penguins are naturally equipped to resist stress.

Exposure to unpredictable environmental stressors could influence animal health and fitness by inducing oxidative stress, potentially through downstream effects of glucocorticoid stress hormones (e.g. corticosterone) on mitochondrial function. Yet, it remains unclear whether species that have evolved in stochastic and challenging environments may present adaptations to alleviate the effects of stress exposure on oxidative stress. We tested this hypothesis in wild king penguins by investigating mitochondrial and oxidative stress responses to acute restraint-stress, and their relationships with baseline (potentially mirroring exposure to chronic stress) and stress-induced increase in corticosterone levels. Acute restraint-stress did not significantly influence mitochondrial function. However, acute restraint-stress led to a significant increase in endogenous antioxidant defences, while oxidative damage levels were mostly not affected or even decreased. High baseline corticosterone levels were associated with an up-regulation of the glutathione antioxidant system and a decrease in mitochondrial efficiency. Both processes might contribute to prevent oxidative damage, potentially explaining the negative relationship observed between baseline corticosterone and plasma oxidative damage to proteins. While stress exposure can represent an oxidative challenge for animals, protective mechanisms like up-regulating antioxidant defences and decreasing mitochondrial efficiency seem to occur in king penguins, allowing them to cope with their stochastic and challenging environment.

Maternal effects as drivers of sibling competition in a parent-offspring conflict context? An experimental test.

Maternal effects occur when the mother's phenotype influences her offspring's phenotype. In birds, differential allocation in egg yolk components can allow mothers to compensate for the competitive disadvantage of junior chicks. We hypothesize that the parent-older chick conflict peaks at intermediate conditions: parents benefit from the younger chick(s) survival, but its death benefits the older chick in terms of growth and survival. We thus expect maternal compensation to follow a bell-shaped pattern in relation to environmental conditions. We studied a black-legged kittiwake (Rissa tridactyla) population where previous results revealed increased allocation of yolk testosterone in younger as compared to older chicks in intermediate conditions, in line with our theoretical framework. We therefore predicted a maternally induced increase in aggressiveness, growth, and survival for younger chicks born in intermediate environmental conditions. Controlling for parental effects and chick sex, we manipulated food availability before egg laying to create a situation with intermediate (Unfed group) and good (Fed group) environmental conditions. Within each feeding treatment, we further created experimental broods where the natural hatching order was reversed to maximize our chances to observe an effect of feeding treatment on the younger chicks' aggressiveness. As predicted, we found that chick aggressiveness was higher in younger chicks born from the Unfed group (i.e., in intermediate environmental conditions), but only when they were put in a senior position, in reversed broods. Predictions on growth and survival were not confirmed. Mothers thus seem to favor the competitiveness of their younger chick in intermediate conditions via egg yolk components, but our study also suggests that hatching asynchrony need to be small for maternal compensation to be efficient. We emphasize the need for further studies investigating other chick behaviors (e.g., begging) and focusing on the relative role of different yolk components in shaping parent-offspring conflict over sibling competition.