Oxidative Cost Of Reproduction Research Articles

The Immunological and Oxidative Costs of Reproduction and Associations between Maternal and Egg Yolk Physiology in a Reptile

Energetic constraints caused by reproductive investment may incur immunological and oxidative costs to a female and potentially to her developing offspring. Oviparous reptiles are capable of altering offspring phenotype through differential allocation of physiological factors during vitellogenesis (yolk formation), depending upon the external environment and the physiological state of the female. Despite its importance in protecting developing offspring against infection, maternal transfer of immune factors has rarely been studied in reptiles. Furthermore, the extent to which offspring may be impacted by the inherent oxidative costs of vitellogenesis is not well understood. Using the Side-blotched Lizard (Uta stansburiana) as a model, we examined how reproductive investment (clutch size and mass) influenced maternal immunological (BKA) and oxidative state (ROMs) and whether these metrics covaried with egg yolk immunity and oxidative state. We assessed factors influencing variation in egg yolk BKA and ROMs within and across clutches from all females and found that females with smaller clutches had higher BKA and ROMs than females with larger clutches. There was also an overall positive relationship between maternal BKA and ROMs and clutch mass, regardless of clutch size. We did not find maternal and egg yolk BKA and ROMs to be directly related, but yolk ROMs decreased as egg mass increased. Within-clutch variation in yolk BKA and ROMs was not related to maternal investment, but variation among clutches was explained by maternal identity. Because egg yolk physiology can impose long-lasting or permanent changes to offspring, these results create a foundation for future work investigating factors contributing to yolk physiology and highlight the necessity of considering multiple physiological and ecological variables when conducting eco-immunological research.

Water availability and temperature induce changes in oxidative status during pregnancy in a viviparous lizard

Abstract Reproduction involves considerable reorganization in an organism's physiology that incurs potential toxicity for cells (e.g., oxidative stress) and decrease in fitness. This framework has been the cornerstone of the so‐called ‘oxidative cost of reproduction’, a theory that remains controversial and relatively overlooked in non‐model ectotherms. Here, we used two complementary approaches in natural and controlled conditions to test whether altered access to climate conditions (water and temperature resources) alters oxidative status and mediates reproductive trade‐offs in viviparous populations of the common lizard (Zootoca vivipara). First, we examined whether access to free‐standing water and differences in ambient temperature across 12 natural populations could be related to variation in oxidative status, reproductive effort and reproductive success. Second, we determined whether an experimental restriction to water triggers higher oxidative cost of reproduction and correlates with fitness measures (reproductive success, future survival rate and probability of future reproduction). Pregnant females exhibited higher sensitivity than males to natural or experimental limitations in temperature and water access. That is, in restricted environments, pregnant females with higher reproductive effort exhibited stronger oxidative damage despite enhanced non‐enzymatic antioxidant capacity. Enhanced antioxidant defensive capacity in pregnant females was positively correlated with higher reproductive success, whereas elevated oxidative damage negatively correlated with offspring annual survival. Altogether, our results revealed a context‐dependent oxidative cost of reproduction that was concomitant with a conflict in water demand from offspring. These new insights should be critical for understanding ectotherm responses to heat waves and summer droughts that are increasing in frequency and duration. A free Plain Language Summary can be found within the Supporting Information of this article.

Reproductive effort affects oxidative status and stress in an Antarctic penguin species: An experimental study

The oxidative cost of reproduction has been a matter of debate in recent years presumably because of the lack of proper experimental studies. Based on the hypothesis that different brood sizes produce differential reproductive costs, an experimental manipulation during breeding of Adélie penguins was conducted at Hope Bay, Antarctica, to study oxidative status and stress. We predict that a lower reproductive effort should be positively related to low oxidative and physiological stress. We randomly assigned nests with two chicks to a control reproductive effort group (CRE), and by removing one chick from some nests with two chicks, formed a second, low reproductive effort group (LRE). We examined how oxidative status in blood plasma (reactive oxygen metabolites, ROMs, and total antioxidant capacity, OXY) and stress (heterophil/lymphocyte ratio, H/L) responded to a lower production of offspring total biomass. Our nest manipulation showed significant differences in offspring total biomass, which was lower in the LRE group. As predicted, the LRE group had higher antioxidant capacity than individuals in the CRE group. We have also found, although marginally significant, interactions between sex and treatment in the three variables analysed. Females had higher OXY, lower ROMs and lower H/L ratio when rearing one chick, whereas males did so when rearing two except for OXY which was high regardless of treatment. Moreover, there was a significant negative correlation between the H/L ratio and OXY in females. Finally, we have found a negative and significant relationship between the duration of the experiment and OXY and ROMs and positive with H/L ratio which suggests that indeed breeding penguins are paying an effort in physiological terms in relation to the duration of the chick rearing. In conclusion, a reduction of the reproductive effort decreased oxidative stress in this long-lived bird meaning that a link exists between breeding effort and oxidative stress. However, our findings suggest different sex strategies which results in opposite physiological responses presumably depending on different life-history strategies in males and females.

Oxidative status and fitness components in the Seychelles warbler

Summary Oxidative damage, caused by reactive oxygen species during aerobic respiration, is thought to be an important mediator of life‐history trade‐offs. To mitigate oxidative damage, antioxidant defence mechanisms are deployed, often at the cost of resource allocation to other body functions. Both reduced resource allocation to body functions and direct oxidative damage may decrease individual fitness, through reducing survival and/or reproductive output. The oxidative costs of reproduction have gained much attention recently, but few studies have investigated the long‐term consequences of oxidative damage on survival and (future) reproductive output under natural conditions. Using a wild population of the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), we tested the prediction that high levels of reactive oxygen species, or high antioxidant investments to avoid oxidative damage, have fitness consequences because they reduce survival and/or reproductive output. We found that individuals with higher circulating non‐enzymatic antioxidant capacity had a lower probability of surviving until the next year. However, neither current reproductive output, nor future reproductive output in the surviving individuals, was associated with circulating non‐enzymatic antioxidant capacity or oxidative damage. The negative relationship between antioxidant capacity and survival that we observed concurs with the findings of an extensive comparative study on birds, however the mechanisms underlying this association remain to be resolved. A lay summary is available for this article.

Interacting effects of early dietary conditions and reproductive effort on the oxidative costs of reproduction.

The hypothesis that oxidative damage accumulation can mediate the trade-off between reproduction and lifespan has recently been questioned. However, in captive conditions, studies reporting no evidence in support of this hypothesis have usually provided easy access to food which may have mitigated the cost of reproduction. Here, I test the hypothesis that greater investment in reproduction should lead to oxidative damage accumulation and telomere loss in domestic zebra finches Taeniopygia guttata. Moreover, since the change or fluctuation in diet composition between early and late postnatal period can impair the ability to produce antioxidant defences in zebra finches, I also tested if early nutritional conditions (constant vs fluctuating early diet) influenced the magnitude of any subsequent costs of reproduction (e.g., oxidative damage and/or telomere shortening). In comparison to pairs with reduced broods, the birds that had to feed enlarged broods showed a higher level of oxidative DNA damage (8-OHdG), but brood size had no effect on telomeres. Fluctuating early diet composition reduced the capacity to maintain the activity of endogenous antioxidants (GPx), particularly when reproductive costs were increased (enlarged brood). The decline in GPx in birds feeding enlarged broods was accompanied by a change in bill colouration. This suggests that birds with lower endogenous antioxidant defences might have strategically increased the mobilization of antioxidants previously stored in other tissues (i.e., bill and liver) and thus, preventing an excessive accumulation of damage during reproduction.

Oxidative stress in a capital breeder (Vipera aspis) facing pregnancy and water constraints.

The physiological mechanisms underlying the 'cost of reproduction' remain under debate, though oxidative stress has emerged as a potential candidate. The 'oxidative cost of reproduction' has received considerable attention with regards to food and antioxidant availability; however, the limitation of water availability has thus far been neglected. In this study, we experimentally examined the combined effect of pregnancy and water deprivation on oxidative status in a viviparous snake (Vipera aspis), a species naturally exposed to periods of water and food deprivation. We predicted a cumulative effect of pregnancy and dehydration on oxidative stress levels. Our results support the occurrence of an oxidative cost of reproduction as we found higher oxidative damage levels in pregnant females than in non-reproductive individuals, despite an up-regulation of antioxidant defences. Surprisingly, water deprivation was associated with an up-regulation of antioxidant defences, and did not increase oxidative damage, either alone or in combination with reproduction.

Oxidative costs of reproduction in mouse strains selected for different levels of food intake and which differ in reproductive performance.

Oxidative damage caused by reactive oxygen species has been hypothesised to underpin the trade-off between reproduction and somatic maintenance, i.e., the life-history-oxidative stress theory. Previous tests of this hypothesis have proved equivocal, and it has been suggested that the variation in responses may be related to the tissues measured. Here, we measured oxidative damage (protein carbonyls, 8-OHdG) and antioxidant protection (enzymatic antioxidant activity and serum antioxidant capacity) in multiple tissues of reproductive (R) and non-reproductive (N) mice from two mouse strains selectively bred for high (H) or low (L) food intake, which differ in their reproductive performance, i.e., H mice have increased milk energy output (MEO) and wean larger pups. Levels of oxidative damage were unchanged (liver) or reduced (brain and serum) in R versus N mice, and no differences in multiple measures of oxidative protection were found between H and L mice in liver (except for Glutathione Peroxidase), brain or mammary glands. Also, there were no associations between an individual’s energetic investment (e.g., MEO) and most of the oxidative stress measures detected in various tissues. These data are inconsistent with the oxidative stress theory, but were more supportive of, but not completely consistent, with the ‘oxidative shielding’ hypothesis.

Oxidative costs of reproduction: Oxidative stress in mice fed standard and low antioxidant diets

Lactation is one of the most energetically expensive behaviours, and trade-offs may exist between the energy devoted to it and somatic maintenance, including protection against oxidative damage. However, conflicting data exist for the effects of reproduction on oxidative stress. In the wild, a positive relationship is often observed, but in laboratory studies oxidative damage is often lower in lactating than in non-breeding animals. We hypothesised that this discrepancy may exist because during lactation food intake increases many-fold resulting in a large increase in the intake of dietary antioxidants which are typically high in laboratory rodent chow where they are added as a preservative.We supplied lactating and non-breeding control mice with either a standard or low antioxidant diet and studied how this affected the activity of endogenous antioxidants (catalase, superoxide dismutase; SOD, and glutathione peroxidise; GPx) and oxidative damage to proteins (protein carbonyls, PC) in liver and brain tissue. The low antioxidant diet did not significantly affect activities of antioxidant enzymes in brain or liver, and generally did not result in increased protein damage, except in livers of control mice on low antioxidant diet. Catalase activity, but not GPx or SOD, was decreased in both control and lactating mice on the low antioxidant diet. Lactating mice had significantly reduced oxidative damage to both liver and brain compared to control mice, independent of the diet they were given.In conclusion, antioxidant content of the diet did not affect oxidative stress in control or reproductive mice, and cannot explain the previously observed reduction in oxidative stress in lactating mammals studied in the laboratory. The reduced oxidative stress in the livers of lactating mice even under low antioxidant diet treatment was consistent with the ‘shielding’ hypothesis.

Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits

Summary 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.

Sex-Related Effects of Reproduction on Biomarkers of Oxidative Damage in Free-living Barn Swallows (Hirundo rustica)

According to life-history theory, the allocation of limiting resources to one trait has negative consequences for other traits requiring the same resource, resulting in trade-offs among life-history traits, such as reproduction and survival. In vertebrates, oxidative stress is increasingly being considered among the physiological mechanisms forming the currency of life-history trade-offs. In this study of the barn swallow (Hirundo rustica), we focus on the oxidative costs of reproduction, especially egg laying, by investigating the effects of breeding stage (pre- vs. post-laying) and progression of the season on three biomarkers of oxidative damage (OD) to plasma proteins, namely the concentration of malondialdehyde (MDA)-protein adducts and of protein thiol groups (PSH), and the protein carbonyl (PCO) content. Moreover, we investigated whether males and females differed in plasma OD levels, because the inherent sex differences in reproductive roles and physiology may originate sex-specific patterns of OD during breeding. We found that MDA-protein adduct levels were higher in the pre-laying than in the post-laying phase, that males had lower levels of MDA-modified proteins than females, and that the decline of MDA-protein adduct concentration between the pre- and the post-laying phase was more marked for females than males. In addition, MDA-protein adduct levels declined with sampling date, but only during the pre-laying phase. On the other hand, plasma PCO levels increased from the pre- to the post-laying phase in both sexes, and females had higher levels of PCO than males. PSH concentration was unaffected by breeding stage, sex or sampling date. On the whole, our findings indicate that biomarkers of protein oxidation closely track the short-term variation in breeding stage of both male and female barn swallows. Moreover, the higher protein OD levels observed among females compared to males suggest that egg laying entails oxidative costs, which might negatively affect female residual reproductive value.

Oxidative Cost of Reproduction Is Sex Specific and Correlated with Reproductive Effort in a Cooperatively Breeding Bird, the Florida Scrub Jay

Reproduction is energetically demanding, and how much an individual is able to invest in reproduction is often a function of its health state. An understanding of the relationship between oxidative balance and reproductive decisions, especially in free-living species, is still very limited. We evaluated the relationship between oxidative health and reproductive effort in a free-living population of the cooperatively breeding Florida scrub jay Aphelocoma coerulescens. Specifically, we assessed whether prebreeding oxidative damage levels predicted reproductive effort and subsequently whether postbreeding oxidative damage levels reflected reproductive effort. Prebreeding oxidative damage levels were negatively correlated with reproductive effort in males. In males, postbreeding levels of oxidative damage were significantly greater than prebreeding levels. Given that females exhibited no such patterns, our results suggest that in this species, males bear the brunt of the oxidative costs associated with reproduction.

The energetic and oxidative costs of reproduction in a free-ranging rodent

Summary 1. As understanding of the energetic costs of reproduction in birds and mammals continues to improve, oxidative stress is an increasingly cited example of a non-energetic cost of reproduction that may serve as a proximal physiological link underlying life-history trade-offs. 2. Here, we provide the first study to measure daily energy expenditure (DEE) and oxidative damage in a wild population. We measured both traits on eastern chipmunks (Tamias striatus) and assessed their relationships with age, reproductive status, litter size and environmental conditions. 3. We found that both physiological traits were correlated with environmental characteristics (e.g. temperature, seasons). DEE tended to increase with decreasing temperature, while oxidative damage was lower in spring, after a winter of torpor expression, than in autumn. We also found that DEE decreased with age, while oxidative damage was elevated in young individuals, reduced in animals of intermediate age and tended to increase at older age. 4. After controlling for age and environmental variables, we found that both female DEE and oxidative damage increased with litter size, although the latter increased weakly. 5. Our results corroborate findings from laboratory studies but highlight the importance of considering environmental conditions, age and reproductive status in broader analyses of the causes and consequences of physiological costs of reproduction in wild animals.