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The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species.

ABSTRACT: 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.

SUBMITTER: Romero-Haro AA

PROVIDER: S-EPMC4936042 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species.

Romero-Haro A A AA Sorci G G Alonso-Alvarez C C

Proceedings. Biological sciences 20160601 1833

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 an ...[more]

PMID: 27358368

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Project description:Introduction: Methoxychlor (MXC) is an organochlorine pesticide (OCP) that was formerly used worldwide as an insecticide against pests and mosquitoes. However, MXC is not biodegradable and has lipophilic characteristics; thus, it accumulates in organisms and affects reproductive function. MXC, as an estrogenic compound, promotes oxidative stress, induces oxidative stress damage to ovarian follicles, and causes miscarriages and stillbirths in females. In this research endeavor, our primary objective was to explore the ramifications of MXC regarding the developmental processes occurring during the initial stages of embryogenesis in pigs. Methods: In this study, we counted the blastocyst rate of early embryos cultured in vitro. We also examined the reactive oxygen species level, glutathione level, mitochondrial membrane potential, mitochondrial copy number and ATP level in four-cell stage embryos. Finally, apoptosis and DNA damage in blastocyst cells, as well as pluripotency-related and apoptosis-related genes in blastocyst cells were detected. The above experiments were used to evaluate the changes of MXC damage on early parthenogenetic embryo development. Results and Discussion: The results showed that early embryos exposed to MXC had a significantly lower cleavage rate, blastocyst rate, hatching rate, and total cell count compared with the control group. It was also of note that MXC not only increased the levels of reactive oxygen species (ROS), but also decreased the mitochondrial membrane potential (ΔΨm) and mitochondrial copy number during the development of early embryos. In addition, after MXC treatment, blastocyst apoptosis and DNA damage were increased, decreased cell proliferation, and the expression of pluripotency-related genes SOX2, NANOG, and OCT4 was down-regulated, while the expression of apoptosis-related genes BAX/BCL-2 and Caspase9 was up-regulated. Our results clearly show that MXC can have deleterious effects on the developmental processes of early porcine embryos, establishing the toxicity of MXC to the reproductive system. In addition, the study of this toxic effect may lead to greater concern about pesticide residues in humans and the use of safer pesticides, thus potentially preventing physiological diseases caused by chemical exposure.

Project description:ABSTRACT:Oxidative stress and telomere dynamics are considered to be powerful biomarkers quantifying a potential trade-off between current reproduction and self-maintenance. Recent studies confirmed the negative impact of elevated reproduction on telomeres, but the evidence for the cost of reproduction in terms of oxidative stress remains equivocal. In order to induce reproductive costs, we experimentally manipulated reproductive effort by increasing brood size in captive zebra finches (Taeniopygia guttata) and additionally challenged all birds by a low ambient temperature to facilitate detection of these costs. We were not able to show any negative effects of elevated reproductive effort on telomere dynamics and oxidative stress among parents, although brood enlargement was effective in terms of total mass and number of fledged young. Interestingly, irrespective of brood size treatment, we found a significant increase in antioxidant capacity at peak breeding while oxidative damage did not change with time. Our results may suggest that reproduction, instead of generating costs, may stimulate physiological functions promoting self-maintenance in terms of higher protection against free radicals. Possibly, opportunistic breeders such as zebra finches may not impede their future performance for the sake of current reproduction. SIGNIFICANCE STATEMENT:This study interrogates a molecular background behind one of the most intriguing trade-offs that potentially occurs between self-maintenance and reproduction. We manipulated breeding effort in zebra finches to understand if the cost of reproduction can be mediated by telomere dynamics and oxidative stress. In our study system, we did not detect the direct reproductive costs in terms of parental oxidative damage and telomere loss; instead, these costs were paid by the offspring in terms of their inhibited growth rate. Moreover, we found that entering into the reproductive state strongly stimulated self-maintenance by increasing antioxidant capacity in parents. Our results emphasize that current reproductive success is not always prioritized over investment in body maintenance preventing the oxidative cost of reproduction.

Project description:BackgroundReactive oxygen species (ROS)-induced oxidative stress is well known to play a major role in male infertility. Sperm are sensitive to ROS damaging effects because as male germ cells form mature sperm they progressively lose the ability to repair DNA damage. However, how oxidative DNA lesions in sperm affect early embryonic development remains elusive.ResultsUsing cattle as model, we show that fertilization using sperm exposed to oxidative stress caused a major developmental arrest at the time of embryonic genome activation. The levels of DNA damage response did not directly correlate with the degree of developmental defects. The early cellular response for DNA damage, γH2AX, is already present at high levels in zygotes that progress normally in development and did not significantly increase at the paternal genome containing oxidative DNA lesions. Moreover, XRCC1, a factor implicated in the last step of base excision repair (BER) pathway, was recruited to the damaged paternal genome, indicating that the maternal BER machinery can repair these DNA lesions induced in sperm. Remarkably, the paternal genome with oxidative DNA lesions showed an impairment of zygotic active DNA demethylation, a process that previous studies linked to BER. Quantitative immunofluorescence analysis and ultrasensitive LC-MS-based measurements revealed that oxidative DNA lesions in sperm impair active DNA demethylation at paternal pronuclei, without affecting 5-hydroxymethylcytosine (5hmC), a 5-methylcytosine modification that has been implicated in paternal active DNA demethylation in mouse zygotes. Thus, other 5hmC-independent processes are implicated in active DNA demethylation in bovine embryos. The recruitment of XRCC1 to damaged paternal pronuclei indicates that oxidative DNA lesions drive BER to repair DNA at the expense of DNA demethylation. Finally, this study highlighted striking differences in DNA methylation dynamics between bovine and mouse zygotes that will facilitate the understanding of the dynamics of DNA methylation in early development.ConclusionsThe data demonstrate that oxidative stress in sperm has an impact not only on DNA integrity but also on the dynamics of epigenetic reprogramming, which may harm the paternal genetic and epigenetic contribution to the developing embryo and affect embryo development and embryo quality.

Project description:BackgroundEffective communication between sexual partners is essential for successful reproduction. Avian parents with biparental incubation need to know how to negotiate, when and who will incubate, and how to harmonize partner exchange at the nest. Although considerable effort has been dedicated to studies of incubation rhythms, few studies have investigated how behavioural signals serve to tighten cooperation between parents. Moreover, existing studies are almost exclusively restricted to species in which long distances between incubating and non-incubating parents prevent continuous communication during incubation. Thus, the most frequently described parental exchange system is a simple model characterized by the return of the non-incubating parent to the nest itself. Here, we propose more complex parental exchange behaviour in the Northern Lapwing (Vanellus vanellus), a territorial species capable of continuous partner communication during incubation and with a highly variable male contribution to incubation.ResultsNorthern Lapwing females regularly vocalized shortly before departing from the nest, while males mostly left the nest quietly. Responsiveness of the male to female vocalization, perhaps in combination with her flying away from the nest, helped to synchronize incubation care by increasing the probability of exchange, and also by shortening the exchange gaps. In contrast, a male-to-female exchange gap most often occurred after the male quietly flew away from the nest. The frequency of female vocal signalling was not correlated with the male incubation effort on a between-nest scale, but the highest probability of a female-to-male exchange occurred after vocal signalling by females with the most nest-attentive males. Conversely, lowered effort by females to vocalize in the night was accompanied by lower willingness of males to incubate.ConclusionsOur results suggest that (1) that the incubating parent can communicate with the non-incubating partner using sex-specific behavioural signals, and this helps to synchronize parental exchange on the nest, (2) this signalling may combine acoustic and visual cues, and (3) the efficiency of this signalling might influence the overall nest attendance. The presumption that the repertoire of behavioural signals during reproduction will be much more complex in territorial species that are capable of continuous communication between the partners during the incubation period should be further tested.

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The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species.

Publications

The oxidative cost of reproduction depends on early development oxidative stress and sex in a bird species.

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