Manuela Caprioli

Antioxidant Defenses Predict Long-Term Survival in a Passerine Bird

Background Normal and pathological processes entail the production of oxidative substances that can damage biological molecules and harm physiological functions. Organisms have evolved complex mechanisms of antioxidant defense, and any imbalance between oxidative challenge and antioxidant protection can depress fitness components and accelerate senescence. While the role of oxidative stress in pathogenesis and aging has been studied intensively in humans and model animal species under laboratory conditions, there is a dearth of knowledge on its role in shaping life-histories of animals under natural selection regimes. Yet, given the pervasive nature and likely fitness consequences of oxidative damage, it can be expected that the need to secure efficient antioxidant protection is powerful in molding the evolutionary ecology of animals. Here, we test whether overall antioxidant defense varies with age and predicts long-term survival, using a wild population of a migratory passerine bird, the barn swallow (Hirundo rustica), as a model. Methodology/Principal Findings Plasma antioxidant capacity (AOC) of breeding individuals was measured using standard protocols and annual survival was monitored over five years (2006–2010) on a large sample of selection episodes. AOC did not covary with age in longitudinal analyses after discounting the effect of selection. AOC positively predicted annual survival independently of sex. Individuals were highly consistent in their relative levels of AOC, implying the existence of additive genetic variance and/or environmental (including early maternal) components consistently acting through their lives. Conclusions Using longitudinal data we showed that high levels of antioxidant protection positively predict long-term survival in a wild animal population. Present results are therefore novel in disclosing a role for antioxidant protection in determining survival under natural conditions, strongly demanding for more longitudinal eco-physiological studies of life-histories in relation to oxidative stress in wild populations.

Anhydrobiosis in bdelloid species, populations and individuals.

Abstract Bdelloid rotifers are aquatic microinvertebrates common in water bodies and in unstable “terrestrial” habitats, such as mosses and lichens. The key to the adaptability to live in unstable habitats is their capacity to tolerate habitat desiccation through anhydrobiosis, that is assumed apomorphic to the taxon. The life history traits of some “moss” and “water” species of bdelloid are compared, showing that the water species have shorter life span, higher fecundity and earlier age at first reproduction than the moss species. These traits are discussed in the light of current life history theories. Contrary to the assumptions of the models, anhydrobiosis of bdelloids does not appear to imply energy demand. Past research on bdelloid anhydrobiosis is briefly reviewed, focusing on the factors that affect anhydrobiosis success, like morphological and physiological adjustments, and on the effect of events of anhydrobiosis during life time. Desiccation produces a time shift on the age of the bdelloid, which disregards the time spent as anhydrobiotic, following the so-called “Sleeping Beauty” model. Average fecundity is never found to decrease as a consequence of anhydrobiosis, but is either equal or even higher than that of a hydrated rotifer. Bdelloid populations seem to benefit from anhydrobiosis; fitness of a bdelloid is found to decline, if populations are maintained hydrated for several generations, but not if populations are cyclically desiccated. We hypothesize that anhydrobiosis can be an essential event for long-term survival of bdelloid populations.

Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order

Egg quality may mediate maternal allocation strategies according to progeny sex. In vertebrates, carotenoids have important physiological roles during embryonic and post‐natal life, but the consequences of variation in yolk carotenoids for offspring phenotype in oviparous species are largely unknown. In yellow‐legged gulls, yolk carotenoids did not vary with embryo sex in combination with egg laying date, order and mass. Yolk lutein supplementation enhanced the growth of sons from first eggs but depressed that of sons from last eggs, enhanced survival of daughters late in the season, and promoted immunity of male chicks and chicks from small eggs. Lack of variation in egg carotenoids in relation to sex and egg features, and the contrasting effects of lutein on sons and daughters, do not support the hypothesis of optimal sex‐related egg carotenoid allocation. Carotenoids transferred to the eggs may rather result from a trade‐off between opposing effects on sons or daughters.

Clock Gene Variation Is Associated with Breeding Phenology and Maybe under Directional Selection in the Migratory Barn Swallow

Background In diverse taxa, photoperiodic responses that cause seasonal physiological and behavioural shifts are controlled by genes, including the vertebrate Clock orthologues, that encode for circadian oscillator mechanisms. While the genetic network behind circadian rhythms is well described, relatively few reports exist of the phenological consequences of and selection on Clock genes in the wild. Here, we investigated variation in breeding phenology in relation to Clock genetic diversity in a long-distance migratory bird, the barn swallow (Hirundo rustica). Methodology/Principal Findings In a sample of 922 adult barn swallows from a single population breeding in Italy we found one very common (Q7) and three rare (Q5, Q6, Q8) length variants of a functionally significant polyglutamine repeat. Rare (2.9%) Q7/Q8 heterozygous females, but not males, bred significantly later than common (91.5%) Q7/Q7 females, consistent with the expectation that ‘long’ alleles cause late breeding, as observed in a resident population of another bird species. Because breeding date depends on arrival date from migration, present results suggest that the association between breeding date and Clock might be mediated by migration phenology. In addition, fecundity selection appears to be operating against Q7/Q8 because late migrating/breeding swallows have fewer clutches per season, and late breeding has additional negative selection effects via reduced offspring longevity. Genotype frequencies varied marginally non-significantly with age, as Q7/Q8 frequency showed a 4-fold reduction in old individuals. This result suggests negative viability selection against Q7/Q8, possibly mediated by costs of late breeding. Conclusions/Significance This is the first study of migratory birds showing an association between breeding phenology and Clock genotype and suggesting that negative selection occurs on a phenologically deviant genotype. Low polymorphism at Clock may constrain microevolutionary phenological response to changing climate, and may thus contribute to the decline of barn swallow populations.

Increased oxidative stress in barn swallows from the Chernobyl region.

The Chernobyl nuclear accident produced the largest unintended release of radionuclides in history, with dramatic consequences for humans and other organisms. Exposure to ionizing radiation is known to reduce circulating and stored levels of specific antioxidants in birds and humans, thus potentially increasing oxidative stress. However, overall effects of radioactive exposure on oxidative status have never been investigated in any free ranging vertebrate. We measured plasma antioxidant capacity and concentration of reactive oxygen metabolites in adult barn swallows (Hirundo rustica) from colonies with variable background radiation levels in the Chernobyl region in Ukraine and Belarus. We predicted that antioxidants would decrease while reactive oxygen metabolites would increase with exposure to increasing levels of radiation at the breeding sites. Consistent with this expectation, radiation level positively predicted plasma concentration of reactive oxygen metabolites, whereas no significant covariation was found with non-enzymatic plasma antioxidant capacity. An index of oxidative stress was also larger in barn swallows exposed to high contamination levels. Thus, radioactive contamination appeared to be responsible for the increased generation of reactive oxygen metabolites and the imbalance between reactive oxygen metabolites and non-enzymatic plasma antioxidant capacity.

Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care

Success in competition for limiting parental resources depends on the interplay between parental decisions over allocation of care and offspring traits. Birth order, individual sex and sex of competing siblings are major candidates as determinants of success in sib–sib competition, but experimental studies focusing on the combined effect of these factors on parent–offspring communication and within-brood competitive dynamics are rare. Here, we assessed individual food intake and body mass gain during feeding trials in barn swallow chicks differing for seniority and sex, and compared the intensity of their acoustic and postural solicitation (begging) displays. Begging intensity and success in competition depended on seniority in combination with individual sex and sex of the opponent. Junior chicks begged more than seniors, independently of satiation level (which was also experimentally manipulated), and obtained greater access to food. Females were generally weaker competitors than males. Individual sex and sex of the opponent also affected duration of begging bouts. Present results thus show that competition with siblings can make the rearing environment variably harsh for developing chicks, depending on individual sex, sex of competing broodmates and age ranking within the nest. They also suggest that parental decisions on the allocation of care and response of kin to signalling siblings may further contribute to the outcome of sibling competition.

Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex

BackgroundMaternal effects mediated by egg size and quality may profoundly affect offspring development and performance, and mothers may adjust egg traits according to environmental or social influences. In avian species, context-dependency of maternal effects may result in variation in egg composition, as well as in differential patterns of covariation among selected egg components, according to, for example, position in the laying sequence or offspring sex. We investigated variation in major classes of egg yolk components (carotenoids, vitamins and steroid hormones) in relation to egg size, position in the laying sequence and embryo sex in clutches of the Yellow-legged Gull (Larus michahellis). We also investigated their covariation, to highlight mutual adjustments, maternal constraints or trade-offs in egg allocation.ResultsLaying sequence-specific patterns of allocation emerged: concentration of carotenoids and vitamin E decreased, while concentrations of androgens increased. Vitamin A, estradiol and corticosterone did not show any change. There was no evidence of sex-specific allocation or covariation of yolk components. Concentrations of carotenoids and vitamins were positively correlated. Egg mass decreased along the laying sequence, and this decrease was negatively correlated with the mean concentrations of carotenoids in clutches, suggesting that nutritionally constrained females lay low quality clutches in terms of carotenoid content. Finally, clutches with smaller decline in antioxidants between first- and last-laid eggs had a larger increase in yolk corticosterone, suggesting that a smaller antioxidant depletion along the laying sequence may entail a cost for laying females in terms of increased stress levels.ConclusionsSince some of the analyzed yolk components (e.g. testosterone and lutein) are known to exert sex-specific phenotypic effects on the progeny in this species, the lack of sex-specific egg allocation by mothers may either result from trade-offs between contrasting effects of different egg components on male and female offspring, or indicate that sex-specific traits are controlled primarily by mechanisms of sexual differentiation, including endogenous hormone production or metabolism of exogenous antioxidants, during embryonic development.

Fine-tuned modulation of competitive behaviour according to kinship in barn swallow nestlings.

Kin selection theory predicts that, in species where progeny members compete for limiting parental care, individual offspring should be more prone to monopolize parental resources as their genetic relatedness to brood competitors decreases. Mixed parentage among broodmates may arise as a consequence, for example, of extra-pair fertilization or brood parasitism events. In this experimental study of barn swallows (Hirundo rustica), we reciprocally partially cross-fostered hatchlings between broods and compared the behaviour of pairs of related and unrelated broodmates in a competitive context, both under normal food provisioning regime and after mild food deprivation. We found that scramble competition for food mediated by visual and vocal solicitation displays (begging) is inversely related to relatedness among competitors, independent of their level of satiation. Nestlings may modulate their competitive behaviour according to vocal cues that vary with their origin and allow kin recognition. We also uncover direct fitness costs to both parents and offspring arising from mixed parentage in a brood, in terms of increased parental workload and reduced survival of the nestlings. Such previously neglected costs may select for reduced frequency of extra-pair fertilizations and brood parasitism in species with extensive parental care.

Sex‐related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the ‘rank advantage’ and the ‘differential susceptibility’ hypotheses, nor the ‘mate opportunity’ hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with ‘mate choice’ arguments, whereby females use condition‐dependent arrival date to assess mate quality.

Sexual Dimorphism in Melanin Pigmentation, Feather Coloration and Its Heritability in the Barn Swallow (Hirundo rustica)

Melanin is the main pigment in animal coloration and considerable variation in the concentrations of the two melanin forms (pheo- and eumlanin) in pigmented tissues exists among populations and individuals. Melanin-based coloration is receiving increasing attention particularly in socio-sexual communication contexts because the melanocortin system has been hypothesized to provide a mechanistic basis for covariation between coloration and fitness traits. However, with few notable exceptions, little detailed information is available on inter-individual and inter-population variation in melanin pigmentation and on its environmental, genetic and ontogenetic components. Here, we investigate melanin-based coloration in an Italian population of a passerine bird, the barn swallow (Hirundo rustica rustica), its sex- and age-related variation, and heritability. The concentrations of eu- and pheomelanin in the throat (brown) and belly (white-to-brownish) feathers differed between sexes but not according to age. The relative concentration of either melanin (Pheo:Eu) differed between sexes in throat but not in belly feathers, and the concentrations in males compared to females were larger in belly than in throat feathers. There were weak correlations between the concentrations of melanins within as well as among plumage regions. Coloration of belly feathers was predicted by the concentration of both melanins whereas coloration of throat feathers was only predicted by pheomelanin in females. In addition, Pheo:Eu predicted coloration of throat feathers in females and that of belly feathers in males. Finally, we found high heritability of color of throat feathers. Melanization was found to differ from that recorded in Hirundo rustica rustica from Scotland or from H. r. erythrogaster from North America. Hence, present results show that pigmentation strategies vary in a complex manner according to sex and plumage region, and also among geographical populations, potentially reflecting adaptation to different natural and sexual selection regimes, and that some coloration components seem to be highly heritable.