Giuseppe Boncoraglio

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.

Female Burying Beetles Benefit from Male Desertion: Sexual Conflict and Counter-Adaptation over Parental Investment

Sexual conflict drives the coevolution of sexually antagonistic traits, such that an adaptation in one sex selects an opposing coevolutionary response from the other. Although many adaptations and counteradaptations have been identified in sexual conflict over mating interactions, few are known for sexual conflict over parental investment. Here we investigate a possible coevolutionary sequence triggered by mate desertion in the burying beetle Nicrophorus vespilloides, where males commonly leave before their offspring reach independence. Rather than suffer fitness costs as a consequence, our data suggest that females rely on the males absence to recoup some of the costs of larval care, presumably because they are then free to feed themselves on the carcass employed for breeding. Consequently, forcing males to stay until the larvae disperse reduces components of female fitness to a greater extent than caring for young singlehandedly. Therefore we suggest that females may have co-evolved to anticipate desertion by their partners so that they now benefit from the males absence.

Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings.

Parent-offspring conflicts lead the offspring to evolve reliable signals of individual quality, including parasite burden, which may allow parents to adaptively modulate investment in the progeny. Sex-related variation in offspring reproductive value, however, may entail differential investment in sons and daughters. Here, we experimentally manipulated offspring condition in the barn swallow (Hirundo rustica) by subjecting nestlings to an immune challenge (injection with bacterial lipopolysaccharide, LPS) that simulates a bacterial infection, and assessed the effects on growth, feather quality, expression of morphological (gape coloration) and behavioral (posture) begging displays involved in parent-offspring communication, as well as on food allocation by parents. Compared to sham-injected controls, LPS-treated chicks suffered a depression of body mass and a reduction of palate color saturation. In addition, LPS treatment resulted in lower feather quality, with an increase in the occurrence of fault bars on wing feathers. The color of beak flanges, feather growth and the intensity of postural begging were affected by LPS treatment only in females, suggesting that chicks of either sex are differently susceptible to the immune challenge. However, irrespective of the effects of LPS, parents equally allocated food among control and challenged offspring both under normal food provisioning and after a short period of food deprivation of the chicks. These results indicate that bacterial infection and the associated immune response entail different costs to offspring of either sex, but a decrease in nestling conditions does not affect parental care allocation, possibly because the barn swallow adopts a brood-survival strategy. Finally, we showed that physiological stress induced by pathogens impairs plumage quality, a previously neglected major negative impact of bacterial infection which could severely affect fitness, particularly among long-distance migratory birds.

Solicitation displays reliably reflect oxidative damage in barn swallow nestlings

Reproduction entails parental decisions over allocation of limiting resources. ‘Begging’ solicitation displays by the offspring have been hypothesised to evolve as reliable indicators of quality, allowing parents to adopt optimal allocation strategies. To function as such, however, begging signals must covary with offspring traits that affect viability. Here we tested whether oxidative damage of nestling barn swallows predicts begging bout duration, call amplitude and intensity of postural displays both under normal food provisioning and under food shortage. Oxidative damage as determined by normal metabolism, pathological conditions and functioning of the immune system can serve as a comprehensive indicator of offspring condition because it can profoundly affect viability, senescence and reproduction. Begging bout duration was negatively predicted by oxidative damage but only after food deprivation. Postural begging negatively covaried with oxidative damage, at least when nestlings were confronted with related nest mates. Plasma antioxidant capacity did not predict begging behaviour. Thus, we show for the first time that behavioural begging covaries with a comprehensive index of chick condition, lending support to reliability of such begging traits also as signals of quality rather than need or hunger only. Future studies are candidate to decouple the effect of hunger state and individual condition on behavioural begging.

Differential Maternal Testosterone Allocation among Siblings Benefits Both Mother and Offspring in the Zebra Finch Taeniopygia guttata

Parents are selected to preferentially invest in the offspring with highest reproductive value. One mechanism for achieving this is the modification of competitive asymmetries between siblings by maternal hormones. In many organisms, offspring value varies according to birth position in the brood, which determines survival chances and competitive advantage over access to resources. In birds, variation in yolk androgen allocation over the laying sequence is thought to modulate dominance of senior chicks over junior brood mates. We tested this hypothesis in zebra finches, which show a naturally decreasing pattern of within-clutch testosterone allocation. We abolished these within-clutch differences by experimentally elevating yolk testosterone levels in eggs 2–6 to the level of egg 1, and we assessed fitness measures for junior offspring (eggs 2–6), senior offspring (egg 1), and their mothers. Testosterone-injected eggs hatched later than control eggs. Junior, but not senior, chicks in testosterone-treated broods attained poorer phenotypic quality compared to control broods, which was not compensated for by positive effects on seniors. Mothers were generally unaffected by clutch treatment. Thus, naturally decreasing within-clutch yolk testosterone allocation appears to benefit all family members and does not generally enhance brood reduction by favoring senior chicks, in contrast to the widely held assumption.

With a little help from my kin: barn swallow nestlings modulate solicitation of parental care according to nestmates' need.

In altricial species, offspring competing for access to limiting parental resources (e.g. food) are selected to achieve an optimal balance between the costs of scrambling for food, the benefits of being fed and the indirect costs of subtracting food to relatives. As the marginal benefits of acquiring additional food decrease with decreasing levels of need, satiated offspring should be prone to favour access to food by their needy kin, thus enhancing their own indirect fitness, while concomitantly reducing costs of harsh competition with hungry broodmates. We tested this prediction in feeding trials of barn swallow (Hirundo rustica) nestlings by comparing begging behaviour and food intake of two similar‐sized nestmates, one of which was food‐deprived (FD). Non‐food‐deprived (NFD) offspring modulated begging intensity depending on their nestmates need: when competing with FD nestmates, NFD nestlings reduced both the intensity and frequency of begging displays compared to themselves in the control trial before food deprivation. Hence, NFD nestlings reduced their competitiveness to the advantage of FD nestmates, which obtained more feedings and showed a threefold larger increase in body mass. Moderation of individual selfishness can therefore be adaptive in the presence of a needier kin, because the indirect fitness benefits of promoting its condition can outweigh the costs of forgoing being fed, and because it limits the cost of begging escalation against a vigorous competitor.

Parental effects alter the adaptive value of an adult behavioural trait

The parents phenotype, or the environment they create for their young, can have long-lasting effects on their offspring, with profound evolutionary consequences. Yet, virtually no work has considered how such parental effects might change the adaptive value of behavioural traits expressed by offspring upon reaching adulthood. To address this problem, we combined experiments on burying beetles (Nicrophorus vespilloides) with theoretical modelling and focussed on one adult behavioural trait in particular: the supply of parental care. We manipulated the early-life environment and measured the fitness payoffs associated with the supply of parental care when larvae reached maturity. We found that (1) adults that received low levels of care as larvae were less successful at raising larger broods and suffered greater mortality as a result: they were low-quality parents. Furthermore, (2) high-quality males that raised offspring with low-quality females subsequently suffered greater mortality than brothers of equivalent quality, which reared larvae with higher quality females. Our analyses identify three general ways in which parental effects can change the adaptive value of an adult behavioural trait: by influencing the associated fitness benefits and costs; by consequently changing the evolutionary outcome of social interactions; and by modifying the evolutionarily stable expression of behavioural traits that are themselves parental effects. DOI: http://dx.doi.org/10.7554/eLife.07340.001

Parent-absent signalling of need and its consequences for sibling competition in the barn swallow

In species with parental care, competition among siblings for access to limited parental resources is common. Sibling competition can be mediated by begging behaviour, a suite of different visual and acoustic displays by which offspring solicit parental care. These are mostly addressed to the parents upon food provisioning, but can also be performed in the absence of the attending parents. This so-called parent-absent begging (PAB) may function as an intrabrood communication signal and potentially affect intrabrood competition dynamics for access to food. We investigated the role of PAB in moulding sibling interactions and its effect on food intake among altricial barn swallow (Hirundo rustica) nestlings, both under normal and experimentally reduced food intake. Frequency of PAB increased after food deprivation. Nestlings that had performed PAB increased their begging intensity upon the subsequent parental feeding visit, while siblings reduced their own begging level, but only when they had not been food-deprived. As a consequence, nestlings which had performed PAB before parental arrival had larger chances of receiving food. However, nestlings did not benefit from displaying PAB when competing with food-deprived siblings. Our findings show that PAB reliably reflects need of food, indicating that a nestling will vigorously compete for the subsequent food item. By eavesdropping siblings PAB displays, nestlings may optimally balance the costs of scrambling competition, the direct fitness gains of being fed and the indirect fitness costs of subtracting food to needy kin. However, large asymmetries in satiation between competitors may lead individual offspring to monopolize parental resources, irrespective of PAB displays.

Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defence

Burying beetles (Nicrophorus vespilloides) bear distinctive and variable orange-black patterning on their elytra and produce an anal exudate from their abdomen when threatened. During breeding, the anal exudates contribute to the antimicrobial defence of the breeding resource. We investigated whether the anal exudates also provide a responsive chemical defence, which is advertised to potential avian predators by the beetle’s orange and black elytral markings. We found that that the orange-black elytral markings of the burying beetle are highly conspicuous for avian predators against range of backgrounds, by using computer simulations. Using bioassays with wood ants, we also showed that the burying beetle’s anal exudates are aversive to potential predators. From these results, and other evidence in the literature, we conclude that the evidence for aposematism in the burying beetle is as strong as the evidence for many other classically aposematic species, such as defended Hymenopterans, ladybirds or poisonous frogs. Nevertheless, we also report unexpectedly high levels of individual variation in coloration and chemical defences, as well as sex differences. We suggest that this variation might be due partly to conflicting selection pressures, particularly on the dual function of the exudates, and partly to nutritional differences in the developmental environment. The ecology of the burying beetles (Nicrophorus spp.) differs markedly from better-studied aposematic insects. This genus thus offers new potential for understanding the evolution of aposematism in general.

No evidence of a cleaning mutualism between burying beetles and their phoretic mites

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass.