Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird

Velando, A., Noguera, J.C., da Silva, A. e Kim, S.Y., 2019. Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird. Scientific reports, 9(1), p.2203.

It has been proposed that animals usually restrain their growth because fast growth leads to an increased production of mitochondrial reactive oxygen species (mtROS), which can damage mitochondrial DNA and promote mitochondrial dysfunction. Here, we explicitly test whether this occurs in a wild bird by supplementing chicks with a mitochondria-targeted ROS scavenger, mitoubiquinone (mitoQ), and examining growth rates and mtDNA damage. In the yellow-legged gull Larus michahellis, mitoQ supplementation increased the early growth rate of chicks but did not reduce mtDNA damage. The level of mtDNA damage was negatively correlated with chick mass, but this relationship was not affected by the mitoQ treatment. We also found that chick growth was positively correlated with both mtDNA copy number and the mitochondrial enzymatic activity of citrate synthase, suggesting a link between mitochondrial content and growth. Additionally, we found that mitoQ supplementation increased mitochondrial content (in males), altered the relationship between mtDNA copy number and damage, and downregulated some transcriptional pathways related to cell rejuvenation, suggesting that scavenging mtROS during development enhanced growth rates but at the expense of cellular turnover. Our study confirms the central role of mitochondria modulating life-history trade-offs during development by other mechanisms than mtROS-inflicted damage.


On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks

Noguera, J.C., Morales, J., Pérez, C. & Velando, A., 2010. On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behavioral Ecology, 21(3), pp.479-484.

Offspring solicit food to their parents by begging displays, which are important in the parent–offspring communication. Most theoretical approximations on this behavior have centered on the view of begging as an honest signal of need or as a form of scramble competition for resources. In both signaling models, costly begging is necessary to stabilize the begging strategy at equilibrium. Nevertheless, evidence supporting begging as costly behavior remains scarce. We investigated whether oxidative stress may represent a general form of proximate cost of begging and also whether begging is related to offspring nutritional condition. To test this, we experimentally modified the chicks’ nutritional condition and vitamin E availability and measured the effects on different begging components. The intensity of all begging components increased in chicks that were intake restricted, whereas vitamin E specifically enhance the total number of chatter calls given by chicks, mainly in those with a lower body size. Our results suggest that begging behavior is an antioxidant demanding activity and support the idea that oxidative stress may be a cost of begging. Our findings also suggest that begging behavior may be an honest signal of the nutritional and oxidative status of the chicks.

Yolk testosterone reduces oxidative damages during postnatal development

Noguera, J.C., Alonso-Alvarez, C., Kim, S.Y., Morales, J. & Velando, A., 2011. Yolk testosterone reduces oxidative damages during postnatal development. Biology letters, 7(1), pp.93-95.

Conditions experienced during early life can influence the development of an organism and several physiological traits, even in adulthood. An important factor is the level of oxidative stress experienced during early life. In birds, extra-genomic egg substances, such as the testosterone hormone, may exert a widespread influence over the offspring phenotype. Interestingly, testosterone can also upregulate the bioavailability of certain antioxidants but simultaneously increases the susceptibility to oxidative stress in adulthood. However, little is known about the effects of maternally derived yolk testosterone on oxidative stress in developing birds. Here, we investigated the role of yolk testosterone on oxidative stress of yellow-legged gull chicks during their early development by experimentally increasing yolk testosterone levels. Levels of antioxidants, reactive oxygen species and lipid oxidative damage were determined in plasma during nestlings’ growth. Our results revealed that, contrary to control chicks, birds hatched from testosterone-treated eggs did not show an increase in the levels of oxidative damage during postnatal development. Moreover, the same birds showed a transient increase in plasma antioxidant levels. Our results suggest that yolk testosterone may shape the oxidative stress-resistance phenotype of the chicks during early development owing to an increase in antioxidant defences and repair processes.

Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird

Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A., 2011. Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evolutionary ecology, 25(2), pp.461-472.

Why do animals not grow at their maximal rates? It has been recently proposed that fast growth leads to the accumulation of cellular damages due to oxidative stress, influencing subsequent performances and life span. Therefore, the trade-off between fast growth and oxidative stress may potentially function as an important constraint in the evolution of growth trajectories. We test this by examining a potential antagonistic pleiotropy between growth and blood resistance to controlled free radical attack in a wild bird using a cross-fostering design and robust quantitative genetic analyses. In the yellow-legged gull Larus michahellis decreased resistance to oxidative stress at age 8 days was associated with faster growth in mass, across the first 8 days of life, suggesting a trade-off between mass growth and oxidative-stress-related somatic maintenance. We found a negative genetic correlation between chick growth and resistance to oxidative stress, supporting the presence of the genetic trade-off between the two traits. Therefore, investment of somatic resources in growth could be constrained by resistance to oxidative stress in phenotypic and genetic levels. Our results provide first evidence for a potential genetic trade-off between life-history and underlying physiological traits in a wild vertebrate. Future studies should explore genetic trade-offs between life-history traits and other oxidative-stress-related traits.

Heritability of resistance to oxidative stress in early life

Kim, S.Y., Noguera, J.C., Morales, J. & Velando, A., 2010. Heritability of resistance to oxidative stress in early life. Journal of Evolutionary Biology, 23(4), pp.769-775.

Oxidative stress has recently been suggested to play an important role in life-history evolution, but little is known about natural variation and heritability of this physiological trait. Here, we explore phenotypic variation in resistance to oxidative stress of cross-fostered yellow-legged gull (Larus cachinnans) chicks. Resistance to oxidative stress was not related to plasma antioxidants at hatching, which are mostly derived from maternal investment into eggs. Common environmental effects on phenotypic variation in resistance to oxidative stress were not significant. Heritability was relatively low and nonsignificant in hatchlings, but interestingly, the chicks of age 8 days showed high and significant heritability (h2 = 0.59). Our results suggest that resistance to oxidative stress is determined mainly by the genotype as chicks grow. Further work is required to explore the genetic role of oxidative stress in life-history evolution.

Thrifty development: early‐life diet restriction reduces oxidative damage during later growth

Noguera, J.C., Lores, M., Alonso‐Álvarez, C. and Velando, A., 2011. Thrifty development: early‐life diet restriction reduces oxidative damage during later growth. Functional Ecology, 25(5), pp.1144-1153.

1. Conditions during early stages of life may have an important effect on phenotype, by inducing programmed responses that may remain throughout the lifetime of an animal. One very important factor that can promote long-term changes in phenotype is restriction of food intake (dietary restriction, DR).
2. Recently, it has been shown that DR may induce an increase in antioxidant and repair mechanisms as a result of hormetic responses. Interestingly, the induction of antioxidant and repair mechanisms may be triggered by transitory increases in reactive oxygen species. Dietary-derived antioxidants, such as vitamin E, may be important to determine the compensatory effect of DR.
3. To investigate the effect of DR on attenuation of oxidative damage, we manipulated dietary intake (by restricting food ingestion) and antioxidant availability (by vitamin E supplementation) during the first days of life of yellow-legged gull (Larus michahellis) chicks. We then measured oxidative status and body mass during the early development of chicks.
4. We found that an early short event of food shortage strongly affected the oxidative status of the chicks and their growth patterns. We observed less oxidative damage to proteins and DNA in dietary restricted chicks, after the period of food restriction, than in non-restricted chicks. Unexpectedly, vitamin E supplementation did not suppress the hormetic effect of DR, but instead increased it.
5. These novel results support the idea that short events of DR during early development induce a reduction in oxidative damage in wild animals. The results suggest that DR promotes the induction of an early hormetic response in some antioxidant defence processes and/or repair mechanisms. These findings have important implications for our understanding of how early conditions may shape the phenotype of an organism, and also for the study of evolutionary trade-offs during early growth.

Oil pollution increases plasma antioxidants but reduces coloration in a seabird

Pérez, C., Lores, M. & Velando, A. Oil pollution increases plasma antioxidants but reduces coloration in a seabird. Oecologia 163, 875–884 (2010).

It has been suggested that condition-dependent signals may be a useful measure of environmental quality. In this study, we tested the hypothesis that oil pollution enhances oxidative stress and impairs expression of a carotenoid-based signal in a wild population of the yellowlegged gull (Larus michahellis). During the courtship period, a group of gulls were fed a supplementary diet containing heavy fuel oil from the Prestige oil spill and were compared with control gulls fed a similar supplementary diet without fuel oil. Blood levels of polycyclic aromatic hydrocarbons, the most toxic components of crude oils, were higher (30%) in the Prestige oil-fed gulls than in the control gulls. Plasma concentrations of vitamin E and carotenoids were also significantly higher in the Prestige oil-fed gulls (31 and 27%, respectively). Although, the plasma levels of lipid peroxidation markers were higher (13%) in gulls fed with Prestige oil than in the control gulls, these differences were not significant, possibly because of the small number of gulls analyzed. The red bill spot was significantly smaller (16%) in the oil-fed gulls than in the control individuals. This study provides the first experimental evidence that a carotenoid-based signal in a freeliving seabird is affected by exposure to oil pollution and is hence indicative of environmental quality. Since the yellow-legged gull belongs to a complex of species widely distributed throughout the northern hemisphere, the method described may constitute a useful tool for evaluating sublethal effects of oil spills in seabirds.

Availability of nonpigmentary antioxidant affects red coloration in gulls

Pérez, C., Lores, M. & Velando, A. Availability of nonpigmentary antioxidant affects red coloration in gulls. Behavioral Ecology 19, 967–973 (2008).

Red, orange, and yellow carotenoid-based colorations displayed by fishes and birds may function as honest sexual signals of the bearer’s quality. However, the mechanisms underlying the expression of these traits and the information they convey are still controversial. Because carotenoids are antioxidants and carotenoid-based pigmentation is bleached as a consequence of oxidative processes, it has been suggested that the pigmentation may signal antioxidant status. We tested this hypothesis in the yellow-legged gull (Larus michahellis), a seabird that exhibits a carotenoid-based red spot on the lower mandible. The availability of a nonpigmentary antioxidant (i.e., vitamin E) to the gulls was modified before egg laying by means of a supplementary feeding experiment. During the incubation period, breeding pairs were captured to assess the intensity of the color and the size of the red bill spots. We measured the plasma level of lipid peroxidation, total antioxidant capacity, and carotenoids. We found that males that received vitamin E supplements had larger red spot than control birds but that color intensity was not affected by the supplements. Moreover, we found that only those plasma carotenoids involved in the red coloration were affected by the antioxidant supplementation, suggesting an active mechanism to increase red coloration. Overall, our results provide experimental evidence for the hypothesis that carotenoid-based coloration reflects the bearer’s antioxidant status in male gulls.

Pre-fledgling oxidative damage predicts recruitment in a long-lived bird

Noguera, J. C., Kim, S.-Y. & Velando, A. Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biology letters rsbl20110756 (2011).

Empirical evidence has shown that stressful conditions experienced during development may exert long-term negative effects on life-history traits. Although it has been suggested that oxidative stress has long-term effects, little is known about delayed consequences of oxidative stress experienced early in life in fitness-related traits. Here, we tested whether oxidative stress during development has long-term effects on a life-history trait directly related to fitness in three colonies of European shags Phalacrocorax aristotelis. Our results revealed that recruitment probability decreased with oxidative damage during the nestling period; oxidative damage, in turn, was related to the level of antioxidant capacity. Our results suggest a link between oxidative stress during development and survival to adulthood, a key element of population dynamics.

Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks

Lucas, A., Morales, J. & Velando, A. Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks. Journal of Experimental Biology 217, 1253–1262 (2014).

Micronutrients are essential for normal metabolic processes during early development. Specifically, it has been suggested that diet-derived carotenoids can play a key role in physiological functions because of their antioxidant and immunostimulant properties. However, their role as antioxidants remains controversial. Additionally, it is also unclear whether oxidative stress mediates their immunostimulatory effects. In this field study, we separately supplemented yellow-legged gull (Larus michahellis) chicks with two carotenoids (lutein and β-carotene) with different molecular structures and different transformation pathways into other oxidative forms of carotenoids. We quantified their effect on the oxidative status and the immune response of chicks before and after an oxidative challenge with paraquat, a pro-oxidant molecule. Prior to oxidative challenge, none of the carotenoid treatments affected the oxidative status of chicks, but they enhanced the inflammatory response to an antigen compared with controls. The oxidative challenge enhanced plasma vitamin E levels (but not in β-carotene-supplemented chicks) and the antioxidant capacity in the short term. Interestingly, lutein-supplemented chicks showed lower oxidative damage to proteins than non-lutein-supplemented chicks. After the oxidative challenge, the positive effect of carotenoid supplementation on the immune response disappeared. Thus, these results suggest differential effects of two carotenoids with different molecular structures on the oxidative status. Lutein but not β-carotene helps to combat oxidative damage after a free-radical exposure. Additionally, the results indicate that the immunostimulatory effects of carotenoids are linked to oxidative status during early life.