Publications by year
2022
Romero-Haro AÁ, Pérez-Rodríguez L, Tschirren B (2022). Intergenerational Costs of Oxidative Stress: Reduced Fitness in Daughters of Mothers That Experienced High Levels of Oxidative Damage during Reproduction.
Physiological and Biochemical Zoology,
95(1), 1-14.
Full text.
2021
Tschirren B, Romero Haro AA, Zahn S, Criscuolo F (2021). Sex-specific effects of experimental ectoparasite infestation on telomere length in great tit nestlings.
Journal of Evolutionary Biology Full text.
2020
Alonso-Alvarez C, Cantarero A, Romero-Haro AÁ, Chastel O, Pérez-Rodríguez L (2020). Life-long testosterone and antiandrogen treatments affect the survival and reproduction of captive male red-legged partridges (Alectoris rufa).
Behavioral Ecology and Sociobiology,
74(8).
Abstract:
Life-long testosterone and antiandrogen treatments affect the survival and reproduction of captive male red-legged partridges (Alectoris rufa)
Abstract: Sexual steroids can play an important role as life-history organizers. In males, high circulating testosterone levels induce physiological/behavioral costs and benefits, leading to trade-offs. However, studies simultaneously testing the impact of these levels in both fitness components (survival and fecundity) during lifetime are scarce and limited to wild birds. To determine the mortality causes or hormonal manipulation impacts on male fertility is, nonetheless, a difficult task in free-ranging animals that could be easier in captivity. We longitudinally monitored captive red-legged partridges (Alectoris rufa) and exposed males to high exogenous testosterone levels, anti-androgens, or a control treatment during each breeding period throughout their lives. Theory predicts that individuals maintaining high androgen levels should obtain higher fitness returns via reproduction, but suffer reduced longevity. Testosterone-treated male partridges, accordingly, lived shorter compared to controls, since they were more prone to die from a natural bacterial infection. However, the same birds seemed to have a lower capacity to fertilize eggs, probably due to endocrine feedback reducing testicular mass. These results show that exogenous testosterone can exert unpredicted effects on fitness parameters. Therefore, caution must be taken when drawing conclusions from non-fully controlled experiments in the wild. Males treated with the androgen-receptor blocker flutamide did not outlive controls as predicted by the life-history trade-off theory, but their mates laid eggs with higher hatching success. The latter could be due to mechanisms improving sperm quality/quantity or influencing maternal investment in egg quality. Testosterone receptor activity/amount could thus be as relevant to fitness as testosterone levels. Significance statement: it has repeatedly been hypothesized that high testosterone levels induce a cost in terms of reduced lifetime reproductive success. This can be due to reduced fecundity or via shorter lifespan. This is, however, only supported by a handful of studies, mostly in wild birds. We tested this in captive male red-legged partridges, which allowed us to determine reproductive success and mortality causes. We increased testosterone levels or blocked its action with antiandrogens throughout life. High testosterone levels reduced the survival by making birds more prone to die by infection. The eggs produced by their mates also showed lower hatching success, a probable manipulation artifact that should be considered in avian studies in the wild. Interestingly, the androgen-receptor blocker flutamide increased lifetime hatching success compared to controls, suggesting that androgen receptor amounts/activity are even more relevant to fitness than testosterone levels.
Abstract.
Romero-Haro AA, Alonso-Alvarez C (2020). Oxidative Stress Experienced during Early Development Influences the Offspring Phenotype.
The American Naturalist,
196(6), 704-716.
Full text.
2019
Cantarero A, Pérez-Rodríguez L, Romero-Haro AÁ, Chastel O, Alonso-Alvarez C (2019). Carotenoid-based coloration predicts both longevity and lifetime fecundity in male birds, but testosterone disrupts signal reliability.
PLoS ONE,
14(8).
Abstract:
Carotenoid-based coloration predicts both longevity and lifetime fecundity in male birds, but testosterone disrupts signal reliability
Sexual selection promotes the evolution of conspicuous animal ornaments. To evolve as signals, these traits must reliably express the "quality" of the bearer, an indicator of individual fitness. Direct estimates of individual fitness may include the contribution of longevity and fecundity. However, evidence of a correlation between the level of signal expression and these two fitness components are scarce, at least among vertebrates. Relative fitness is difficult to assess in the wild as age at death and extra-pair paternity rates are often unknown. Here, in captive male red-legged partridges, we show that carotenoid-based ornament expression, i.e. redness of the bill and eye rings, at the beginning of reproductive life predicts both longevity (1-7 years) and lifetime breeding output (offspring number and hatching success). The recently proposed link between the individual capacity to produce red (keto) carotenoid pigments and the efficiency of cell respiration could, ultimately, explain the correlation with lifespan and, indirectly, fecundity. Nonetheless, in males of avian species, carotenoid-based coloration in bare parts is also partially controlled by testosterone. We also manipulated androgen levels throughout life by treating males with testosterone or antiandrogen compounds. Treatments caused correlations between signal levels and both fitness components to disappear, thus making the signals unreliable. This suggests that the evolution of carotenoid-based sexual signals requires a tightly-controlled steroid metabolism.
Abstract.
2017
Galván I, Inácio Â, Romero-Haro AA, Alonso-Alvarez C (2017). Adaptive downregulation of pheomelanin-related Slc7a11 gene expression by environmentally induced oxidative stress.
Molecular Ecology,
26(3), 849-858.
Abstract:
Adaptive downregulation of pheomelanin-related Slc7a11 gene expression by environmentally induced oxidative stress
Pheomelanin is a sulphur-containing yellow-to-reddish pigment whose synthesis consumes the main intracellular antioxidant (glutathione; GSH) and its precursor cysteine. Cysteine used for pheomelanogenesis cannot be used for antioxidant protection. We tested whether the expression of Slc7a11, the gene regulating the transport of cysteine to melanocytes for pheomelanogenesis, is environmentally influenced when cysteine/GSH are most required for antioxidant protection. We found that zebra finches Taeniopygia guttata developing pheomelanin-pigmented feathers during a 12-day exposure to the pro-oxidant diquat dibromide downregulated the expression of Slc7a11 in feather melanocytes, but not the expression of other genes that affect pheomelanogenesis by mechanisms different from cysteine transport such as MC1R and Slc45a2. Accordingly, diquat-treated birds did not suffer increased oxidative stress. This indicates that some animals have evolved an adaptive epigenetic lability that avoids damage derived from pheomelanogenesis. This mechanism should be explored in human Slc7a11 to help combat some cancer types related to cysteine consumption.
Abstract.
Alonso-Alvarez C, Canelo T, Romero-Haro AÁ (2017). The oxidative cost of reproduction: Theoretical questions and alternative mechanisms.
BioScience,
67(3), 258-270.
Abstract:
The oxidative cost of reproduction: Theoretical questions and alternative mechanisms
The role of reproduction in increasing oxidative stress may be fundamental to understanding aging and the evolutionary trade-off between survival and fecundity. However, contradictory results among experimental studies have challenged the oxidative cost of reproduction. Limitations in experimental design may explain inconsistent findings. Nonetheless, some authors have argued that the hypothesis is founded on the faulty assumptions of an energy-based allocation trade-off and a direct positive link between metabolic rates and the production of reactive oxygen species (ROS) by the mitochondria. We propose that evolutionary trade-offs do not require the allocation of limiting resources and that reproduction may result in ROS-induced oxidative stress without increased mitochondrial ROS. We discuss the previously published oxidative-shielding hypothesis and propose two new hypotheses: hormesis and extortion for reproduction. These hypotheses aim to explain the counterintuitive results indicating that there is less oxidative damage in animals allowed to breed compared with those prevented from reproducing.
Abstract.
Griffith SC, Crino OL, Andrew SC, Nomano FY, Adkins-Regan E, Alonso-Alvarez C, Bailey IE, Bittner SS, Bolton PE, Boner W, et al (2017). Variation in Reproductive Success Across Captive Populations: Methodological Differences, Potential Biases and Opportunities.
Ethology,
123(1), 1-29.
Abstract:
Variation in Reproductive Success Across Captive Populations: Methodological Differences, Potential Biases and Opportunities
Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of ‘model’ species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory – the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency.
Abstract.
Full text.
2016
Romero-Haro AA, Sorci G, Alonso-Alvarez C (2016). The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species.
Proceedings of the Royal Society B: Biological Sciences,
283(1833).
Abstract:
The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species
In the early 2000s, a new component of the cost of reproduction was proposed: oxidative stress. Since then the oxidative cost of reproduction hypothesis has, however, received mixed support. Different arguments have been provided to explain this. Among them, the lack of a life-history perspective on most experimental tests was suggested. We manipulated the levels of a key intracellular antioxidant (glutathione) in captive zebra finches (Taeniopygia guttata) during a short period of early life and subsequently tested the oxidative cost of reproduction. Birds were allowed to mate freely in an outdoor aviary for several months. We repeatedly enlarged or reduced their broods to increase or reduce, respectively, breeding effort. Birds whose glutathione levels were reduced during growth showed higher erythrocyte resistance to free radical-induced haemolysis when forced to rear enlarged broods. This supports the hypothesis predicting the occurrence of developing programmes matching early and adult environmental conditions to improve fitness. Moreover, adult males rearing enlarged broods endured higher plasma levels of lipid oxidative damage than control males, whereas adult females showed the opposite trend. As most previous studies reporting non-significant or opposite results used females only, we also discuss some sex-related particularities that may contribute to explain unexpected results.
Abstract.
2015
Romero-Haro AA, Canelo T, Alonso-Alvarez C (2015). Early development conditions and the oxidative cost of social context in adulthood: an experimental study in birds.
Frontiers in Ecology and Evolution,
3(APR).
Abstract:
Early development conditions and the oxidative cost of social context in adulthood: an experimental study in birds
Environmental conditions during early life may shape phenotype in adulthood. Early adverse conditions may increase the oxidative stress in adults, which could affect their reproductive output and survival. It has also been hypothesized that the larger the reproductive investment, the higher the oxidative stress. We tested this and the potential influence of early oxidative stress on how individuals respond to a reproductive stimulation. The synthesis of the antioxidant glutathione was inhibited in captive zebra finches (Taeniopygia guttata) during growth. In adulthood, the expression of a carotenoid-based sexual signal, bill redness, increased in both sexes, with females also being heavier than controls. The social context of control and glutathione-inhibited males was then manipulated to stimulate precopulatory reproductive investments. Males were individually caged in front of a female or another male. We predicted that males enduring lower early antioxidant levels and placed close to a female should pay the highest cost of a hypothetical increase in bill redness in terms of oxidative damage. However, early conditions only influenced the male's phenotype via their partners. Males caged with females showed increases in circulating pigment (carotenoid) levels, but only when females endured early low antioxidant values. This was probably related to the higher attractiveness of these females. Nevertheless, the bill redness of males did not differ during the social manipulation. Moreover, males facing females from any early condition group showed lower oxidative damage levels in plasma lipids. This result agrees with some findings in rodents, also in captivity. However, the effect may be due to increased triglyceride levels and body mass in males not facing females, as variation in these traits explained oxidative damage variability. The importance of considering housing conditions and life history when interpreting oxidative stress-related trade-offs is highlighted.
Abstract.
Pérez-Rodríguez L, Romero-Haro AA, Sternalski A, Muriel J, Mougeot F, Gil D, Alonso-Alvarez C (2015). Measuring oxidative stress: the confounding effect of lipid concentration in measures of lipid peroxidation.
Physiological and Biochemical Zoology,
88(3), 345-351.
Abstract:
Measuring oxidative stress: the confounding effect of lipid concentration in measures of lipid peroxidation
Lipid peroxidation products are widely used as markers of oxidative damage in the organism. To properly interpret the information provided by these markers, it is necessary to know potential sources of bias and control confounding factors. Here, we investigated the relationship between two indicators of lipid mobilization (circulating levels of triglycerides and cholesterol) and two common markers of oxidative damage (plasma levels of malondialdehyde and hydroperoxides; the latter estimated from the d-ROMs assay kit). The following five avian species were studied: red-legged partridge (Alectoris rufa), zebra finch (Taeniopygia guttata), spotless starling (Sturnus unicolor), marsh harrier (Circus aeroginosus), and Montagu’s harrier (Circus pygargus). In all cases, plasma triglyceride levels positively and significantly correlated with lipid peroxidation markers, explaining between 8% and 34% of their variability. Plasma cholesterol, in contrast, showed a significant positive relationship only among spotless starling nestlings and a marginally significant association in zebra finches. These results indicate that lipid peroxidation marker levels covary with circulating lipid levels.We dis uss the potential causes and implications of this covariation and recommend that future studies that measure oxidative damage using lipid peroxidation markers report both raw and relative levels (i.e. corrected for circulating triglycerides). Whether the observed pattern also holds for other tissues and in other taxa would deserve further research.
Abstract.
Romero-Haro AA, Alonso-Alvarez C (2015). The level of an intracellular antioxidant during development determines the adult phenotype in a bird species: a potential organizer role for glutathione.
American Naturalist,
185(3), 390-405.
Abstract:
The level of an intracellular antioxidant during development determines the adult phenotype in a bird species: a potential organizer role for glutathione
Life-history traits are often involved in trade-offs whose outcome would depend on the availability of resources but also on the state of specific molecular signals. Early conditions can influence trade-offs and program the phenotype throughout the lifetime, with oxidative stress likely involved in many taxa. Here we address the potential regulatory role of a single intracellular antioxidant in lifehistory trade-offs. Blood glutathione levels were reduced in a large sample of birds (zebra finch Taeniopygia guttata) during development using the synthesis inhibitor buthionine sulfoximine (BSO). Results revealed several modifications in the adult phenotype. BSO-treated nestlings showed lower glutathione and plasma antioxidant levels. In adulthood, BSO birds endured greater oxidative damage in erythrocytes but stronger expression of a sexual signal. Moreover, adult BSO females also showed weaker resistance to oxidative stress but were heavier and showed better body condition. Results suggest that low glutathione values during growth favor the investment in traits that should improve fitness returns, probably in the form of early reproduction. Higher oxidative stress in adulthood may be endured if this cost is paid later in life. Either the presence of specific signaling mechanisms or the indirect effect of increased oxidative stress can explain our findings.
Abstract.
2014
Romero-Haro AA, Alonso-Alvarez C (2014). Covariation in oxidative stress markers in the blood of nestling and adult birds.
Physiological and Biochemical Zoology,
87(2), 353-362.
Abstract:
Covariation in oxidative stress markers in the blood of nestling and adult birds
Interest in the imbalance between the production of reactive oxygen species and the state of the antioxidant machinery- that is, oxidative stress-has recently grown among comparative physiologists and evolutionary/behavioral ecologists. The number and types of markers used to estimate oxidative stress is, however, under debate. The study of covariation among these markers is necessary to better interpret the information content of each independent variable. Here, the covariation in levels of 10 blood parameters in a group of zebra finches (Taeniopygia guttata) as nestlings and adults was analyzed across a large data set. Total glutathione levels in erythrocytes were negatively correlated with plasma carotenoid values in nestlings only, supporting the implication of carotenoids in the antioxidant machinery during a particularly stressful period of life. Plasma lipid levels (triglycerides [TRGs]) as well as plasma antioxidant capacity-the latter tested with and without control for uric acid levels-showed individual consistency with age. Plasma TRG and uric acid levels were strongly correlated with plasma lipid peroxidation and antioxidant capacity, respectively, suggesting an influence of recent intake or mobilization of energy stores on these variables. The meaning of oxidative stressmarkers, whether corrected or uncorrected for levels of nutritional metabolites, remains to be explored. Experiments manipulating diet composition and oxidative stress are necessary to confirm or reject the hypothesized causalities. © 2014 by the University of Chicago. All rights reserved.
Abstract.
2010
Ferragud A, Haro A, Sylvain A, Velázquez-Sánchez C, Hernández-Rabaza V, Canales JJ (2010). Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress.
Behavioural Brain Research,
210(1), 134-139.
Abstract:
Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress
Stress can induce preferential engagement of habit learning mediated by the basal ganglia, relative to learning that involves complex spatial associations contributed by the hippocampal formation. We explored in mice the influence that chronic episodes of social stress exert on the selection of cognitive/spatial vs. habit-based learning strategies. Male mice were exposed to repeated episodes of social confrontation and were categorized as dominant, subordinate or undetermined according to quantitative ethologically relevant parameters of aggression. Mice were then trained in a conditional discrimination task in the T-maze in the presence of allocentric cues until five correct choices were made. The T-maze was then turned 180° and mice were categorized as " cue-learners" or " place-learners" on the basis of their first response in the probe test. Mice showed a graded preference for place vs. cue learning strategies depending on their social categorization (control > undetermined > dominant > subordinate), which ranged from 55% in controls to only 10% in subordinate mice. The response of subordinate mice differed significantly from controls. Hippocampal neurogenesis was studied in the different groups of mice. In keeping with the tendency to engage habit learning, 2,5-bromodeoxyuridine (BrdU) incorporation in the DG was reduced in mice that experienced agonistic encounters, and so was the expression of doublecortin, a marker for immature neurons. These observations suggest that chronic social stress impairs neurogenesis in the adult hippocampus, weakens spatial learning and strengthens habit-like responses. © 2010 Elsevier B.V.
Abstract.