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  • Publication
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    Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long-lived bird
    (2017-2-13)
    Merkling, Thomas
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    Blanchard, Pierrick
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    Chastel, Olivier
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    Vallat, Armelle
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    Hatch, Scott A.
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    Danchin, Etienne
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    1. Individuals must trade-off between energetically costly activities to maximize their fitness. However, the underlying physiological mechanism remains elusive. Oxidative stress, the imbalance between reactive oxygen species production and antioxidant and/or repair activities, has been suggested to underlie life-history trade-offs: greater investment in reproduction supposedly generating higher oxidative damage, thus reducing life span. 2. While most studies used natural or experimental variation in offspring number to examine how reproduction affects oxidative stress, none studied the impact of offspring sex, although it could influence physiological costs and fitness, if the sexes differ in terms of energetic cost. 3. Here, we aim at further understanding how reproduction (in terms of offspring sex, experimentally manipulated and number, not manipulated) influences oxidative stress in a wild seabird, where sons are energetically costlier than daughters. We did so by conducting a chick fostering experiment (to disentangle foster and produced sex ratio) and using four oxidative stress markers plus baseline corticosterone. 4. First, the results suggest that individual physiological state before laying modulates upcoming reproductive effort. Individuals with higher pre-laying baseline corticosterone and lower antioxidant activity, estimated by their superoxide dismutase activity, subsequently invested more in reproduction, estimated by the cumulative number of days spent rearing chicks. Hence, it seems that only individuals that could afford to invest heavily in reproduction did so. 5. Then, we examined the effects of reproductive effort on individual physiological state at the end of the breeding season. Higher reproductive effort seemed to imply higher physiological costs. Oxidative stress, estimated by the ratio of oxidized over reduced glutathione, increased with more male-biased foster sex ratio among mothers but not among fathers, whereas baseline corticosterone did so in both sexes. Similarly, lipid oxidative damage to red blood cells increased with increasing cumulative number of days spent rearing chicks. 6. Our study provides the first evidence that brood sex ratio variation can affect oxidative balance, potentially in a sex-specific way, although more studies are needed to understand whether the observed physiological costs could lead to fitness costs. It also highlights the need to consider sex ratio in future studies investigating the role of oxidative stress in life-history trade-offs.
  • Publication
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    Alternative reproductive tactics, sperm mobility, and oxidative stress in Carollia perspicillata (Seba's short-tailed bat)
    (2017-1-1)
    Fasel, Nicolas Jean
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    Wesseling, Charlotte
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    Fernandez, Ahana Aurora
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    Vallat, Armelle
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    Richner, Heinz
    In social systems with alternative reproductive tactics, sneakers face a stronger sperm competition than harem males, and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus their allocation to the ejaculate may depend on social status. In this study on the frugivorous bat Carollia perspicillata, we assessed for harem and sneaker males, four sperm mobility traits, blood and ejaculate markers of the redox balance, and the ejaculate to blood ratios of the redox markers. Under higher sperm competition, sneaker males should allocate proportionally more antioxidant resources to the protection of sperm than harem males. In contrast, harem males should favour pre-copulatory functions, which comprise the protection of blood. We found significantly higher sperm velocity and sperm survival in sneakers. There was no correlation between sperm mobility and sperm enzymatic antioxidant activity or ejaculate levels of lipid peroxidation (oxidative damage). Ejaculate levels of lipid peroxidation and sperm survival showed a significantly positive correlation, which could be attributed to the role of reactive oxygen species for sperm capacitation. Harem and sneaker males showed similar levels of redox balance markers in ejaculate and blood. However, harem males showed a higher ratio of oxidized over reduced glutathione in blood, which may indicate higher cellular stress due to higher metabolism. Overall, our findings suggest that sneakers of C. perspicillata compensate for a stronger sperm competition by higher sperm mobility.
  • Publication
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    Modification of sperm quality after sexual abstinence in the Seba's short tailed bat (Carollia perspicillata)
    (2016-5-4)
    Wesseling, Charlotte
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    Fasel, Nicolas Jean
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    Richner, Heinz
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    In polygynous mating systems, few males have stable access to sexual mates. With an expected higher copulation rate, harem males may deplete seminal fluids or increase epididymal sperm maturation, generating poor sperm quality. In a first study, we reported a higher sperm quality in sneaker males of Carollia perspicillata. To test whether the lower sperm quality observed in harem males was generated by an elevated copulation rate, we temporarily removed males of both social statuses from the colony. We thus assessed status-related changes of sperm quality resulting from sexual abstinence. Moreover, released from territory and female guarding, harem males were expected to show a reduction in somatic costs. On the basis of sperm competition models, we predicted a higher resource investment in the ejaculate with the reduction of pre-copulatory efforts. In line with our predictions, sperm quality of harem males improved significantly in contrast to sneaker males, whose sperm quality did not change. Without an increase in ejaculate lipid peroxidation, our results also provide evidence that the duration of sexual abstinence was not sufficient to generate sperm oxidative damage through senescence. Harem males did not show a reduction in blood lipid peroxidation or in the ratio of oxidized to reduced glutathione. In line with the maintenance of these somatic costs, harem males did not invest more superoxide dismutase to the ejaculate to maintain sperm quality. Our results suggest that a difference in copulation rate rather than an adaptation to sperm competition provides sneaker males with higher sperm quality in C. perspicillata.
  • Publication
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    Maternal effects as drivers of sibling competition in a parent–offspring conflict context? An experimental test
    (2016-5-3)
    Merkling, Thomas
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    Perrot, Charlotte
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    Ferdy, Jean-Baptiste
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    Gaillard, Laurent
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    Lefol, Emilie
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    Voisin, Emmanuelle
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    Hatch, Scott A.
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    Danchin, Etienne
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    Blanchard, Pierrick
    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.
  • Publication
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    Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits
    (2015-8-1)
    Jacob, Staffan
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    Parthuisot, Nathalie
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    Vallat, Armelle
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    Ramon-Portugal, Felipe
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    Heeb, Philipp
    Parasites influence allocation trade-offs between reproduction and self-maintenance and consequently shape host life-history traits. The host microbiome includes pathogenic and commensal micro-organisms that are remarkable in their diversity and ubiquity. However, experimental studies investigating whether the microbiome shapes host reproduction are still lacking. In this study, we tested whether the microbiome affects three important components of bird reproduction, namely (i) the maternal transfer of anti-microbial compounds to the eggs, (ii) the development of nestlings and (iii) the trade-off between reproduction and self-maintenance, here measured by the oxidative costs of reproduction. We experimentally modified the microbiome of wild breeding Great tits (Parus major) by spraying nests with liquid solution that either favoured or inhibited bacterial growth compared to a control. These treatments modified the bacterial communities in the nests and on adult feathers. We found that females from the treatment that decreased bacterial densities in the nests laid eggs with less carotenoids than females from the control, while we found no significant effect of increasing bacterial densities and modifying community composition compared to the control. Nestlings exposed to decreased bacterial densities grew faster and had longer tarsus length at fledging. Moreover, our analyses revealed that the relationship between investment in reproduction and oxidative damage was affected by the treatments. Adults raising larger clutches suffered higher oxidative damage in control nests, whereas this oxidative cost of reproduction was not detected when we modified bird microbiome. Our study provides experimental evidence for an effect of the microbiome on egg carotenoid investment, nestling development and oxidative cost of reproduction and thus highlights the major effect that the microbiome may have on the evolution of host life-history strategies.
  • Publication
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    Electroejaculation and semen buffer evaluation in the microbat Carollia perspicillata
    (2015-3-1)
    Fasel, Nicolas Jean
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    Buff, Samuel
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    Richner, Heinz
    Scientific interests and conservation needs currently stress the necessity to better understanding bat reproductive biology. In this study, we present the first, safe, inexpensive, and reliable method to obtain sperm from a microbat species (Carollia perspicillata) by electroejaculation. This method revealed to be highly efficient (100% success rate). We obtained ejaculates composed of two characteristically different fractions. We compared three buffers and recommend using an Earle's balanced salt solution as a semen extender. Earle's balanced salt solution provided significant repeatable measure of swimming ability (intraclass correlation coefficient: 0.74, P < 0.01) and proportion of motile sperms (intraclass correlation coefficient: 0.08, P = 0.01) and allowed sperm to maintain optimal swimming capacity over time. None of the buffers could dissolve all the coagulated sperm. Although the trypsin buffer freed a larger fraction of spermatozoa in the ejaculate, it impaired swimming ability without improving motility, viability, and stamina. We thus argue that the sperm population analyzed with Earle's balanced salt solution is a representative of the ejaculate. Finally, we found that the mean sperm velocity of C perspicillata (78.8 Î¼m/s) is lower than that predicted by regressing sperm velocity on relative testes mass, a proxy of sperm competition. The question as to whether C perspicillata is an outsider for sperm velocity, or whether bats evolved yet another unique mechanism to cope with sperm competition deserves more investigations.
  • Publication
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    Corticosterone: effects on feather quality and deposition into feathers
    (2015-2-1)
    Jenni-Eiermann, Susanne
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    Vallat, Armelle
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    Jenni, Lukas
    The concentration of the glucocorticoid hormone corticosterone (CORT) is increasingly used in ecology and conservation biology as an integrated measure of the historical record of an individual's hypothalamo–pituitary–adrenal (HPA) activity during feather growth. However, where and how CORT is incorporated in feathers is incompletely known. * We therefore examined whether CORT is reliably measured with an enzyme immunoassay, where CORT is incorporated in the feather and where it affects feather quality, and whether CORT incorporation is related to plasma CORT levels, feather growth rate and melanin pigmentation. * During the regrowth of plucked tail feathers, we injected pigeons with tritium-labelled CORT, and implanted a CORT-releasing pellet to increase plasma CORT concentration for about 3 days. In feather segments, we measured labelled CORT (DPM3H) and we quantified CORT with an enzyme immunoassay EIA (CORTEIA) and double-checked the results with ultra-high performance liquid chromatography–tandem mass spectrometry (LCMS) (CORTMS). * Administered CORT affected feather structure and colour at the very base of the feather (epidermal collar, ramogenic zone) and reduced growth rate. In contrast, incorporation of CORT into the feather happened mainly in the blood quill, as shown with all three methods (DPM3H, CORTEIA and CORTMS). * Incorporation of CORT into feathers was only roughly proportional to plasma concentration, proportional to feather growth rate and increased with melanin pigmentation. * Measuring CORT in feather is a way to reveal past events of increased stress during feather growth in birds.
  • Publication
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  • Publication
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    Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird
    (2013)
    Losdat, Sylvain
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    Blount, Jonathan D.
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    Marri, V.
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    Maronde, L.
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    Richner, Heinz
    Stressful conditions experienced by individuals during their early development have long-term consequences on various life-history traits such as survival until first reproduction. Oxidative stress has been shown to affect various fitness-related traits and to influence key evolutionary trade-offs but whether an individual's ability to resist oxidative stress in early life affects its survival has rarely been tested. In the present study, we used four years of data obtained from a free-living great tit population (Parus major; n = 1658 offspring) to test whether pre-fledging resistance to oxidative stress, measured as erythrocyte resistance to oxidative stress and oxidative damage to lipids, predicted fledging success and local recruitment. Fledging success and local recruitment, both major correlates of survival, were primarily influenced by offspring body mass prior to fledging. We found that pre-fledging erythrocyte resistance to oxidative stress predicted fledging success, suggesting that individual resistance to oxidative stress is related to short-term survival. However, local recruitment was not influenced by pre-fledging erythrocyte resistance to oxidative stress or oxidative damage. Our results suggest that an individual ability to resist oxidative stress at the offspring stage predicts short-term survival but does not influence survival later in life.