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  • Publication
    Accès libre
    Oxidative stress as a life history constraint: pespectives from a bat species with alternative reproductive tactics/
    (2018)
    Meniri, Magali
    ;
    ;
    Fasel, Nicolas
    Au cours de cette thèse, j’ai étudié le rôle du stress oxydant en tant que contrainte pour les traits d’histoire de vie, en utilisant les chauves-souris Fer de lance à lunettes (Carollia perspicillata) comme modèle d’étude. Chez cette espèce, les mâles présentent trois tactiques de reproduction alternatives qui ont des succès reproducteurs différents, et dont l’acquisition pourrait être influencée par les conditions de vie précoce. Tout d’abord, j’ai étudié l’effet du stress oxydant comme contrainte pendant le début de vie. J’ai induit un mauvais départ en utilisant une restriction alimentaire suivit par un rétablissement de la nourriture ad libitum. Bien que j’aie trouvé que la croissance générait du stress oxydant, je n’ai pas trouvé de coût physiologique à court-terme (stress oxydant et glucocorticoïdes) associé à la croissance compensatoire effectuée. De plus, la survie pendant la première année n’était pas clairement impactée par notre traitement. Ces résultats suggèrent que les jeunes ont été capable de mitiger efficacement les conséquences à court-terme d’un mauvais départ. Ensuite, j’ai étudié le rôle du stress oxydant comme contrainte pour la reproduction, afin de tester si la protection anti-oxydante peut représenter un médiateur du compromis d’allocation entre les traits pré- et post-copulatoires, permettant ainsi d’expliquer la qualité spermatique supérieure trouvée précédemment chez les mâles opportunistes. Au cours d’une expérience où j’ai manipulé expérimentalement les tactiques de reproduction des mâles, j’ai trouvé que tous les mâles, quelle que soit leur tactique, présentaient une qualité spermatique similaire (morphologie et capacité natatoire). Bien que les dommages oxydatifs impactassent négativement la capacité natatoire, le profil redox à la fois dans le sang et les éjaculats était le même pour tous les mâles. Globalement, nos résultats suggèrent qu’un compromis d’allocation entre l’investissement dans le soma et les éjaculats pourrait ne pas avoir lieu chez cette espèce. Comme d’autres études avant nous, nous n’avons pas trouvé de corrélation entre les capacités natatoires et la morphologie des spermatozoïdes, ce qui remet en question l’existence d’un lien fonctionnel entre ces deux traits. Enfin, nous proposons que les mâles puissent appliquer une stratégie de « bet-hedging gamétique » où la production de spermatozoïdes à la morphologie hautement variable pourrait permettre d’optimiser les capacités de fertilisation de l’éjaculat pour des risques de compétition spermatique variable.
    En conclusion, nous avons trouvé que le début de vie était associé à des niveaux élevés de stress oxydant, bien que la croissance compensatoire n’ait pas entrainé de coûts physiologique sur le court-terme. De plus, le stress oxydant ne semble pas contraindre l’expression des tactiques de reproduction alternatives. Je suggère donc que le stress oxydant ne représente pas une contrainte forte chez les chauves-souris Fer de lances à lunettes. Je propose également que les mâles harems puissent investir à la fois dans les traits pré- et post- copulatoires, afin de conjointement attirer les femelles et d’assurer la fertilisation. Enfin, je prône que les études expérimentales devraient, le plus possible, être conduites dans l’environnement naturel plutôt qu’en cages, et ai donc créé un piège sélectif à cet effet.
    , In this thesis, I investigated the role of oxidative stress (OS) as a constraint for life history traits, using Seba’s short-tailed bats (Carollia perspicillata) as a model species. In this species, males exhibit three alternative reproductive tactics having unequal pay-offs, and whose acquisition could be impacted by early life conditions. First, I studied the effect of OS as a constraint during early life. I induced early adverse conditions using food restriction followed by ad libitum feeding. Although we found that growth generated oxidative damage, we did not find physiological short-term costs (OS and glucocorticoids) to compensatory growth. Moreover, survival during the first year was not significantly impacted by our treatment. These results suggest that pups were able to efficiently mitigate the short-term consequences of early-life adverse conditions. Then, I tested the role of OS as a constraint for reproduction and investigated whether antioxidant protection could mediate the trade-off between pre- and post-copulatory traits, and thus explain the higher sperm quality found previously in sneaker males. In an experiment where we manipulated males’ reproductive tactic, we found that all males, regardless of their tactic, exhibited similar sperm quality (sperm swimming performance and sperm morphology). Although oxidative damage negatively impacted sperm swimming performance, the redox profile of blood and ejaculates were similar for all males. Overall, our results suggest that a trade-off between investing in the soma or in the ejaculate might not occur. As other studies before, we did not find a correlation between sperm swimming performance and sperm morphology, which questions the existence of a functional link between those two traits. Finally, we propose that males may apply a “gametic bet-hedging” strategy, whereby they would produce highly morphologically variable sperm to optimize their sperm fertilizing abilities across varying sperm competition risks.
    In conclusion, we found that early life was associated with elevated levels of OS, although compensatory growth did not entail physiological costs on the short-term. Moreover, oxidative stress did not seem to constraint the expression of alternative reproductive tactics. Overall, I suggest that OS might not represent a strong constraint in Seba’s short-tailed bats. I suggest that harem males might invest in both pre- and post-copulatory traits to both attract females and secure fertilizations. Finally, I advocate for experimental studies to be conducted in the natural environment rather than in cages, and I designed a selective trap for that purpose.
  • Publication
    Accès libre
    Consequences of the different social roles in a cooperatively breeding society : insights from oxidative stress
    (2018) ; ;
    Bennet, Nigel C.
    De grandes différences dans l'expression des comportements coopératifs existent entre et au sein d´individus chez les espèces pratiquant la reproduction coopérative, où des aides reportent leur dispersion du groupe natal, renoncent à se reproduire et augmentent le succès reproducteur des parents. Comprendre ces différences a été un objectif majeur pour les écologistes évolutionnistes, et la théorie de la sélection de parentèle et de la valeur sélective inclusive ont apporté un éclairage important sur cette question. Des recherches importantes ont montré les rôles prépondérants des bénéfices de succès reproducteur indirects et du degré d'apparentement entre individus dans l'expression des comportements coopératifs. Cependant, peu d'études ont examiné les coûts directs encourus par les individus coopérants, alors même que ces coûts constituent la troisième composante de la sélection de parentèle. Le stress oxydant pourrait représenter un important coût à court terme des comportements coopératifs énergétiquement exigeants, car le stress oxydant peut entraîner une diminution de la fécondité et de la survie, diminuant ainsi la valeur sélective des individus. Dans cette thèse, j'étudie les coûts d'oxydation à court terme des comportements coopératifs chez un rongeur pratiquant la reproduction coopérative, le rat-taupe de Damaraland (Fukomys damarensis). J'ai tout d'abord développé une nouvelle méthode, sensible et sélective, pour permettre la quantification des dommages d'oxydation aux lipides (malondialdéhyde - MDA, Chapitre 2). J'ai ensuite expérimentalement manipulé les contributions coopératives chez des rats-taupes de Damaraland en captivité (Chapitre 3) et fournis la première preuve que l'augmentation des contributions coopératives induit un stress oxydant chez les mâles et les femelles. Bien que cela n'aboutisse pas à l'accumulation de dégâts d'oxydation dans les globules rouges (un tissu somatique), de tels dégâts sont visibles dans la lignée germinale des aides mâles (éjaculats), suggérant que ces mâles privilégient la protection antioxydant des tissus germinaux. Ces résultats suggèrent un compromis évolutif entre survie et reproduction, et suggère que les aides mâles peuvent subir des coûts en termes de valeur sélective en raison d'une diminution de fécondité causée par l'augmentation de leurs contributions coopératives. Enfin, j'ai testé la possibilité que les hormones glucocorticoïdes (GC) puissent réguler le lien entre les contributions coopératives et leurs coûts d'oxydation (Chapitre 4), en raison des effets des GC sur la régulation positive des comportements coopératifs, chez les rats-taupes de Damaraland, comme chez d'autres espèces pratiquant la reproduction coopérative. Chez les aides femelles, j'ai démontré que l'augmentation des niveaux de GC n'affecte pas le stress oxydant dans les érythrocytes, mais conduit à l'accumulation de dommages d'oxydation dans le plasma. Bien que le traitement aie conduit à l'augmentions concomitante des niveaux de GC, des contributions coopératives et du stress oxydant, les différentes relations entre ces variables suggèrent que les coûts d'oxydation induits par des niveaux élevés de GC et par des contributions coopératives accrues peuvent affecter indépendamment la valeur sélective des individus. En résumé, mes résultats suggèrent que, chez les espèces pratiquant la reproduction coopérative, les contributions coopératives et les mécanismes physiologiques responsables de leur régulation induisent des coûts d'oxydation à court terme susceptibles de s'accumuler et d'avoir un impact sur la valeur sélective inclusive des individus. Large differences in cooperative contributions are evident, both within and between individuals of cooperatively breeding species, where helpers forfeit their own reproduction and aid the breeders in raising their young. Understanding this variation has been a major goal for evolutionary ecologists and inclusive fitness theory has stimulated such investigation. Significant research has focused on the effects of differences in indirect fitness benefits and in relatedness between cooperating individuals, on the expression of cooperative behaviours. Yet, fewer studies have focused on the differences in direct fitness costs incurred by cooperative behaviours, the third relevant component of inclusive fitness theory. Oxidative stress represents a prominent candidate mechanism for underlying short-term costs of energetically demanding cooperative behaviours and may lead to decreased fecundity and survival, thereby affecting an individual’s direct fitness. In this thesis, I investigate the short-term oxidative costs of cooperative behaviours in a cooperatively breeding rodent, the Damaraland mole-rat (Fukomys damarensis). I started by developing a new, sensitive, and selective method, to allow the quantification of oxidative damage to lipids (malondialdehyde – MDA; Chapter 2) in further work of this thesis. I then experimentally manipulated cooperative contributions in captive Damaraland mole-rats (Chapter 3) and provided the first evidence that increases in cooperative contributions induce oxidative stress in males and females. Although this did not result in the accumulation of oxidative damage in a somatic tissue (erythrocytes), it did so in the germline of male helpers (ejaculates), suggesting that these males favour the protection of somatic over germline tissues against oxidative stress. These results are indicative of a trade-off between survival and reproduction, and helpers may experience fitness costs through decreased fecundity upon increased cooperative contributions. Lastly, I tested the possibility that glucocorticoid hormones (GCs) mediate a link between cooperative contributions and their oxidative costs (Chapter 4), due to GCs effects on the upregulation of cooperative behaviours in Damaraland mole-rats and other cooperative breeders. Using female helpers, I revealed that increased GC levels did not affect oxidative stress in erythrocytes but led to the accumulation of oxidative damage in the plasma. Although the treatment increased GC levels, cooperative contributions and oxidative stress, the different relationships between these variables suggest that the oxidative costs induced by elevated GC levels and by increased cooperative contributions may independently affect individuals’ direct fitness. In sum, my results suggest that cooperative contributions and the physiological mechanisms responsible for their regulation induce short-term oxidative costs, prone to accumulate and impact inclusive fitness in cooperatively breeding species.
  • Publication
    Accès libre
    Sensitive and selective quantification of free and total malondialdehyde in plasma using UHPLC-HRMS
    Quantification of malondialdehyde (MDA) as a marker of lipid peroxidation is relevant for many research fields. We describe a new sensitive and selective method to measure free and total plasmatic MDA, using derivatization with 2,4-dinitrophenylhydrazine (DNPH) and ultrahigh performance liquid chromatography-high resolution mass spectrometry (UHPLC-HRMS). Free and total MDA were extracted from minute sample amounts (10 μL) using acidic precipitation and alkaline hydrolysis followed by acidic precipitation, respectively. Derivatization was completed within 10 min at room temperature, and the excess DNPH discarded by liquid-liquid extraction. Quantification was achieved by internal standardization using dideuterated MDA as internal standard. The method lowest limit of quantification (LLOQ) was 100 nM and linearity spanned > 3 orders of magnitude. Intra- and inter-day precisions for total MDA were 2.9% and 3.0%, respectively, and those for free MDA were 12.8% and 24.9%, respectively. Accuracy was 101% and 107% at low and high concentrations, respectively. In human plasma, free MDA levels were 120 nM (SD 36.26) and total MDA levels were 6.7 μM (SD 0.46). In addition, we show the applicability of this method to measure MDA plasma levels from a variety of animal species, making it invaluable to scientists in various fields.
  • Publication
    Accès libre
    Oxidative stress affects sperm performance and ejaculate redox status in subordinate house sparrows
    (2017-5-15) ;
    Firth, Alexandra
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    Blareau, Sophie
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    Vallat, Armelle
    ;
    Oxidative stress (OS) is the result of random cellular damage caused by reactive oxygen species that leads to cell death, ageing, or illness. Most physiological processes can result in OS, which in turn has been identified as a major cause of infertility. In promiscuous species, the fertilizing ability of the ejaculate partly determines the male reproductive success. When dominance determines access to fertile females, theory predicts that lower ranking males should increase resource investment into enhancing ejaculate quality. We hypothesized that subordinate males should thus prioritize antioxidant protection of their ejaculates to protect them from OS. We put this hypothesis to the test, by chronically dosing wild House Sparrows with diquat (∼1mg/kg), an herbicide that increases pro-oxidant generation. We found that, although they increased their antioxidant levels in the ejaculate, diquat-treated males produced sperm with reduced velocity. Importantly, and contrary to our hypothesis, males at the bottom of the hierarchy suffered the largest reduction in sperm velocity. We suggest that resource access hinders individuals' ability to cope with environmental hazards. Our results point at OS as a likely physiological mechanism mediating ejaculate quality, while individual ability to access resources may play a role in constraining the extent to which such resources can be allocated into the ejaculate.
  • Publication
    Accès libre
    Antioxidant allocation modulates sperm quality across changing social environments
    In promiscuous species, male reproductive success depends on their ability to mate with fertile females and on the fertilizing ability of their sperm. In such species, theory predicts that, owing to a trade-off between pre- and post-copulatory reproductive traits, males with lesser access to females should increase resource investment into those sperm traits that enhance fertilization success–usually referred to as ejaculate quality. This prediction has been validated in several taxa, yet studies on the physiological mechanisms modulating ejaculate quality are lacking. Sperm cells are highly vulnerable to oxidative stress, which impairs male fertility. Therefore, males that better protect their sperm from oxidative stress are expected to achieve higher ejaculate quality. Based on theoretical expectations, and since social dominance is a major determinant of mating opportunity, we predicted that subordinate males should invest more into the antioxidant protection of their sperm in order to achieve higher ejaculate quality. We maintained 60 male and 60 female wild-caught house sparrows Passer domesticus in outdoor aviaries, where we experimentally manipulated male social status to test our predictions. We measured cellular oxidative stress and enzymatic antioxidant activity in blood and sperm both before and after manipulating social ranks. Before manipulating the social status, we found that ejaculate viability correlated with oxidative stress level in sperm, with dominant males producing more oxidized and less viable ejaculates. Further, males at the lower end of the hierarchy produced ejaculates of similar quality to those of dominant males, suggesting that restricted access to resources might limit male reproductive strategies. After experimentally manipulating the social status, males matched their ejaculate quality to their new rank, while increases in antioxidant investment into ejaculates paralleled increases in ejaculate viability. Oxidative stress has been proposed as a general constraint to the evolution of life histories. Our results highlight oxidative stress and strategic antioxidant allocation as important proximate physiological mechanisms underlying male reproductive strategies.
  • Publication
    Métadonnées seulement
  • Publication
    Métadonnées seulement
    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
    Métadonnées seulement
    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
    Métadonnées seulement
    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
    ;
    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
    Métadonnées seulement
    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
    ;
    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.