Physiological Costs Of Reproduction Research Articles

The Physiological Costs of Reproduction in a Capital Breeding Fish.

AbstractReproduction represents the most energetically demanding period of life for many organisms. Capital breeders, such as anadromous sea trout (Salmo trutta), provide a particularly interesting group of organisms to study within the context of reproduction because they rely on energy stores accrued before breeding to reproduce and sustain all phenotypic and behavioral changes related to reproduction. Energy allocation into current reproduction therefore cannot be mitigated via food intake, resulting in an important life history trade-off. For this reason, exploring indexes related to energetics in salmonids can provide powerful insights into the physiological costs of reproduction. In this study, we sampled blood from and PIT tagged 232 fish captured in the wild before the spawning season. We recaptured and resampled 74 individuals (53 females and 21 males) at the end of the spawning season. Females were further divided into spawning phases (nonspawned, partially spawned, and spawned individuals), though males could not be classified as such. We compared nutritional correlates (triglycerides, cholesterol, calcium, inorganic phosphorus, and total protein), stress correlates (cortisol, sodium, potassium, chloride, and glucose), and indexes of tissue damage (aspartate aminotransferase) between initial capture and recapture as well as among spawning phases in females. We found that nutritional status decreased in all fish throughout the spawning season but that it was substantially lower in females that had spawned. We further found that spawning itself appears stressful, with elevated glucose in partially spawned females and elevated cortisol in male sea trout at recapture. Our findings thus support the idea that the cost of reproduction is energetically high and that incurred stress and a decrease in nutritional status are important physiological costs.

Seasonal and Sexual Variation of the Intermediate Metabolism and Body Condition Indexes in the LizardTropidurus catalanensis(Gudynas and Skuk, 1983) (Squamata: Tropiduridae)

Throughout the life cycle of organisms, nutrient intake is necessary for the maintenance of the functions of daily life and in preparation for a variety of biological events, such as molting, migration, hibernation, and reproduction. One of the most energetically costly events is reproduction. Present study sought to elucidate the seasonal variations in the markers of intermediate metabolism (total proteins, uric acid, glucose, total lipids, triglycerides, total cholesterol, VLDL cholesterol, and glycogen) and body condition indices (gonadossomatic, hepatosomatic, and abdominal fat index) in Tropidurus catalanensis, in order to know the physiological costs of reproduction in this species, also allowing these parameters to be used as markers in studies of environmental alterations. During the study period, 38 males and 35 females were collected. Tropidurus catalanensis is a lizard that inhabits the Pampa grasslands, a biome that stretches across Argentina, Brazil, and Uruguay. Results obtained reveal that this lizard exhibits a clear pattern of seasonal variation in its metabolism, as reflected mainly in levels of plasma total protein, liver glycogen, total lipids, and triglycerides in males and females; and in blood glucose and lipid, and liver protein levels in females. It bears stressing that all body condition indices analyzed varied over the course of the year. The parameters studied can be used to evaluate the impact of changes in environmental conditions on these animals. Winter months appear to trigger a reduction in overall metabolism, most intensely in males. Reproductive period seems to be the biological event that demands greater energy demand, leading to the mobilization of energy stocks mainly in females, where the search for food may be reduced in the months of reproductive peak (spring). The response pattern observed during the reproductive period suggests that this time represents a critical point in terms of the animal's adaptation to its life cycle.

Reproductive status, antioxidant defences and lipid peroxidation in Octopus tehuelchus (Cephalopoda: Octopodidae) females

ABSTRACTAs in other semelparous cephalopods, Octopus tehuelchus females enter a senescent state after spawning. In several taxa, damage to macromolecules that result from an imbalance between antioxidant defences and the production of reactive oxygen species (i.e. oxidative stress) has been postulated as one of the physiological costs of reproduction and one factor that contributes to ageing. In this work, we evaluate whether enzymatic and non-enzymatic antioxidant defences are conditioned by reproductive status in O. tehuelchus obtained from a wild population. The main antioxidant defences, catalase (CAT), superoxide dismutase (SOD), reduced gluthation (GSH) and lipid peroxidation (TBARS), were assessed in somatic and reproductive tissues from octopus females, at immature, mature and spent stages. Oviducal glands showed an increase in TBARS that coincides with a decrease in GSH when females reach a spent stage. No significant changes were observed in the assayed parameters on the ovary wall, digestive gland, mantle and gills along maturity stages. CAT activity was undetectable in most analysed tissues, SOD activity and GSH were similar to or lower than in other cephalopods, while average TBARS levels in somatic tissues were at least one order of magnitude higher than levels found in other molluscs. Our results show that during sexual maturation and after natural oxidative stress conditions (spawning), only oviducal glands show changes that can be linked with the physiological processes of different reproductive status. The low antioxidant defences and the flat protective reactions after spawning could be associated with the semelparous life history of this species.

Physical and Physiological Costs of Reproduction in Watersnakes

Estimating the cost of reproduction is pivotal to understanding the trade-off between current and future reproductive success, a key prediction in life-history theory. Increases in the cost of each reproductive attempt theoretically reduce future reproductive ability. Further, costs may change as individuals grow thus changing the nature of this trade-off. Measuring changes in female locomotor ability during reproduction has been one effective method to measure the cost of reproduction for females. We measured female Diamond-backed Watersnake (Nerodia rhombifer) swimming speed during and after pregnancy to determine if there was a loss of locomotor ability. We then correlated these speeds with measures of reproductive burdening (as estimated by relative clutch mass) and body size to investigate if increased reproductive investment and body size changed locomotor ability and subsequent cost of reproduction. Female snakes swam slower during pregnancy than after. Larger relative clutch masses resulted in slo...

Transcriptomic response to injury sheds light on the physiological costs of reproduction in ant queens

The trade-off between reproduction and longevity is widespread among multicellular organisms. As an important exception, the reproductive females of perennial social insects (ants, honeybees, termites) are simultaneously highly fertile and very long-lived relative to their nonreproductive nestmates. The observation that increased fecundity is not coupled with decreased lifespan suggests that social insect queens do not have to reallocate resources between reproduction and self-maintenance. If queens have to compensate for the costs of reproduction on the level of the individual, the activation of other energy-demanding physiological processes might force them to reduce the production of eggs. To test this hypothesis in ant queens, we increased immunity costs by injury and measured the effect of this treatment on egg-laying rates and genomewide gene expression. Amputation of both middle legs led to a temporary decrease in egg-laying rates and affected the expression of 947 genes corresponding to 9% of the transcriptome. The changes comprised the upregulation of the immune and wound healing response on the one hand, and the downregulation of germ cell development, central nervous system development and learning ability on the other hand. Injury strongly influenced metabolism by inducing catabolism and repressing amino acid and nitrogen compound metabolism. By comparing our results to similar transcriptomic studies in insects, we found a highly consistent upregulation of immune genes due to sterile and septic wounding. The gene expression changes, complemented by the temporary decline of egg-laying rates, clearly reveal a trade-off between reproduction and the immune response in social insect queens.

Female Growth and Offspring Quality over Successive Spawnings in a Caridean Shrimp Neocaridina davidi (Decapoda, Atyidae) with Direct Development.

This study analyzed the quality of recently spawned eggs and of juveniles over five and six consecutive spawns, respectively, in a caridean shrimp Neocaridina davidi with direct development. The potential energetic antagonism between reproduction and somatic growth was also evaluated. The number of eggs per spawn per female was highest in the first spawn, while the number of recently hatched juveniles per spawn per female declined in the sixth spawn. Lower lipid concentration and energy content were detected in eggs of the fourth and fifth spawns, which may indicate for the first time a decrease in maternal provisioning as a result of multiple spawning in a decapod with direct development. This result had no effect on the size of eggs or of recently hatched juveniles, nor on the growth performance of juveniles during a 30-day period following hatching. Lipids were the most abundant biochemical component of eggs, followed by proteins and glycogen; the relative proportion of each component was probably related to embryonic development type. Egg volume was unsuitable as an indicator of nutrient content, as no correlation was found between these variables. The physiological costs of reproduction were evident from the lower energy content of females that reproduced versus females that remained virgin. The lower body weight of the reproductive females at the end of the experiment showed that allocation of resources to reproduction occurred at the expense of somatic growth. To our knowledge, this is the first empirical demonstration of a decapod with direct development.

Effect of low doses of herbicide paraquat on antioxidant defense in Drosophila.

Despite a high toxicity, paraquat is one of the most widely used herbicides in the world. Our study evaluated the effect of paraquat exposure on antioxidant response and locomotion activity in Drosophila melanogaster. We examined the enzymatic activity of superoxide dismutase (SOD) and catalase, and the transcript levels of both enzymes. Flies were exposed to a wide range of paraquat concentrations (0.25 μM to 25 mM) for 12 h. SOD, at both transcript and enzymatic levels, revealed a biphasic dose-response curve with the peak at 2.5 μM paraquat. A similar dose-response curve was observed at transcript levels of catalase. Males revealed higher susceptibility to paraquat exposure, displaying higher lethality, increased levels of SOD activity, and increased peroxide levels than in females. We found that the exposure of females to 2.5 μM paraquat leads to an increase in locomotion activity. Because susceptibility to paraquat was enhanced by mating, the study supports the hypothesis of elevation of stress sensitivity as a physiological cost of reproduction.

Oxidative stress is a potential cost of breeding in male and female northern elephant seals.

The trade-off between current reproductive effort and survival is a key concept of life history theory. A variety of studies support the existence of this trade-off but the underlying physiological mechanisms are not well-understood. Oxidative stress has been proposed as a potential mechanism underlying the observed inverse relationship between reproductive investment and lifespan. Prolonged fasting is associated with oxidative stress including increases in the production of reactive oxygen species, oxidative damage and inflammation.Northern elephant seals (NES) undergo prolonged fasts while maintaining high metabolic rates during breeding. We investigated NES of both sexes to assess oxidative stress associated with extended breeding fasts. We measured changes in the plasma activity or concentrations of markers for oxidative stress in 30 adult male and 33 adult female northern elephant seals across their 1-3 month breeding fasts. Markers assessed included a pro-oxidant enzyme, several antioxidant enzymes, markers for oxidative damage to lipids, proteins and DNA, and markers for systemic inflammation.Plasma xanthine oxidase (XO), a pro-oxidant enzyme that increases production of oxidative radicals, and several protective antioxidant enzymes increased over breeding in both sexes. Males showed increased oxidative damage to lipids and DNA and increased systemic inflammation, while oxidative damage to proteins declined across breeding. In contrast, females showed no oxidative damage to lipids or DNA or changes in inflammation, but showed increases in oxidative damage to proteins. XO activity, antioxidant enzymes, oxidative damage markers, and inflammatory markers were strongly correlated in males but these relationships were weaker or non-existent in females.NES provide evidence for oxidative stress as a physiological cost of reproduction in a capital breeding mammal. Both sexes strongly up-regulated antioxidant defenses during breeding. Despite this response, and in contrast to similar duration non-breeding fasts in previous studies on conspecifics, there was evidence of oxidative damage to tissues. These data demonstrate the utility of using plasma markers to examine oxidative stress but also suggest the necessity of measuring a broad suite of plasma markers to assess systemic oxidative stress.

Reproduction is associated with a tissue-dependent reduction of oxidative stress in eusocial female Damaraland mole-rats (Fukomys damarensis).

Oxidative stress has been implicated as both a physiological cost of reproduction and a driving force on an animal's lifespan. Since increased reproductive effort is generally linked with a reduction in survival, it has been proposed that oxidative stress may influence this relationship. Support for this hypothesis is inconsistent, but this may, in part, be due to the type of tissues that have been analyzed. In Damaraland mole-rats the sole reproducing female in the colony is also the longest lived. Therefore, if oxidative stress does impact the trade-off between reproduction and survival in general, this species may possess some form of enhanced defense. We assessed this relationship by comparing markers of oxidative damage (malondialdehyde, MDA; protein carbonyls, PC) and antioxidants (total antioxidant capacity, TAC; superoxide dismutase, SOD) in various tissues including plasma, erythrocytes, heart, liver, kidney and skeletal muscle between wild-caught reproductive and non-reproductive female Damaraland mole-rats. Reproductive females exhibited significantly lower levels of PC across all tissues, and lower levels of MDA in heart, kidney and liver relative to non-reproductive females. Levels of TAC and SOD did not differ significantly according to reproductive state. The reduction in oxidative damage in breeding females may be attributable to the unusual social structure of this species, as similar relationships have been observed between reproductive and non-reproductive eusocial insects.

Oxidative stress in relation to reproduction, contaminants, gender and age in a long-lived seabird.

Reproduction is a demanding activity for animals, since they must produce, and in some cases protect and provision, their young. It is often overlooked that demands of reproduction may also be exacerbated by exposure to contaminants. In this study, we make use of an exceptional long-term dataset to perform a cross-sectional study on the long-lived wandering albatross (Diomedea exulans) in order to test the effects of reproduction, persistent organic pollutants [POPs: pesticides and polychlorinated biphenyls (PCBs)], mercury, individual age (3-47 years), and sex on the levels of plasma oxidative damage and inflammation. The results of our study support the hypothesis that oxidative damage may be a physiological cost of reproduction and that individuals carrying higher levels of organic or non-organic contaminants have higher oxidative damage. Levels of the inflammatory protein haptoglobin were similar between breeding and non-breeding birds, with the exception of breeding males which had the lowest levels of haptoglobin. Our data also show an effect of age and of organic contaminants on the plasma oxidative damage level, but not on plasma haptoglobin. In addition, plasma oxidative damage level increased with red blood cell mercury concentration in females but not in males. Hence, our study highlights that the harmful effects of contaminants may come through interaction with factors like life stage or gender, suggesting potential for high variation in susceptibility to contamination among individuals.

High basal metabolic rate does not elevate oxidative stress during reproduction in laboratory mice

Increased oxidative stress (OS) has been suggested as a physiological cost of reproduction. However, previous studies reported ambiguous results, with some even showing a reduction of oxidative damage during reproduction. We tested whether the link between reproduction and OS is mediated by basal metabolic rate (BMR), which has been hypothesized to affect both the rate of radical oxygen species production and antioxidative capacity. We studied the effect of reproduction on OS in females of laboratory mice divergently selected for high (H-BMR) and low (L-BMR) BMR, previously shown to differ with respect to parental investment. Non-reproducing L-BMR females showed higher oxidative damage to lipids (quantified as the level of malondialdehyde in internal organ tissues) and DNA (quantified as the level of 8-oxodG in blood serum) than H-BMR females. Reproduction did not affect oxidative damage to lipids in either line; however, it reduced damage to DNA in L-BMR females. Reproduction increased catalase activity in liver (significantly stronger in L-BMR females) and decreased it in kidneys. We conclude that the effect of reproduction on OS depends on the initial variation in BMR and varies between studied internal organs and markers of OS.

Bone loss is a physiological cost of reproduction in white-footed mice (Peromyscus leucopus)

Investment in offspring production often requires the mobilization of endogenous resources, a strategy that may negatively impact maternal condition. In mammals, skeletal ossification in growing offspring requires a large investment of calcium by mothers, and bone loss has been described in several species as a means of supporting this demand. Although bone loss can have adverse effects on the mother, its potential role in a reproductive trade-off has not been addressed. Using white-footed mice (Peromyscus leucopus), we tested the effect of dietary calcium availability on maternal skeletal condition during reproduction to assess if calcium availability drives a trade-off between maternal skeletal condition and offspring production. We provided mice with a low-calcium or standard diet and monitored reproductive output along with changes in bone mineral density and bone resorption (via serum concentrations of pyridinoline cross-links) throughout reproduction. Reproductive performance was not impaired by low calcium intake. Reproductive females on the low-calcium diet showed a significant reduction in bone mineral density relative to reproductive females consuming the standard diet and non-reproductive mice consuming the low-calcium diet, but no difference in bone resorptive activity. Our results suggest that when dietary calcium is limited white-footed mice reproduce at the expense of their skeletal condition, and may do so by limiting bone mineral accretion relative to resorption.

Manipulating reproductive effort leads to changes in female reproductive scheduling but not oxidative stress

The trade-off between reproductive investment and lifespan is the single most important concept in life-history theory. A variety of sources of evidence support the existence of this trade-off, but the physiological costs of reproduction that underlie this relationship remain poorly understood. The Free Radical Theory of Ageing suggests that oxidative stress, which occurs when there is an imbalance between the production of damaging Reactive Oxygen Species (ROS) and protective antioxidants, may be an important mediator of this trade-off. We sought to test this theory by manipulating the reproductive investment of female mice (Mus musculus domesticus) and measuring the effects on a number of life history and oxidative stress variables. Females with a greater reproductive load showed no consistent increase in oxidative damage above females who had a smaller reproductive load. The groups differed, however, in their food consumption, reproductive scheduling and mean offspring mass. Of particular note, females with a very high reproductive load delayed blastocyst implantation of their second litter, potentially mitigating the costs of energetically costly reproductive periods. Our results highlight that females use strategies to offset particularly costly periods of reproduction and illustrate the absence of a simple relationship between oxidative stress and reproduction.

Female Zebra Finches (Taeniopygia guttata) Are Chronically but Not Cumulatively “Anemic” during Repeated Egg Laying in Response to Experimental Nest Predation

Recently it has been recognized that reproduction itself, or the regulatory processes controlling reproduction, might contribute to physiological costs of reproduction. Reproductive anemia, a decrease in hematocrit and hemoglobin concentration, might provide one such mechanism underlying the costs of egg production in birds. In this study, we investigated the effect of repeated cycles of egg production in response to experimental nest predation (egg removal) on hematological traits in female zebra finches (Taeniopygia guttata). We predicted that if the negative effect of egg production on hematocrit and hemoglobin concentration was cumulative, with anemia being proportional to reproductive effort, then females laying more clutches, or laying successive clutches without recovery during incubation, would show greater reproductive anemia. In contrast, if females maintain hematocrit and hemoglobin concentration at some minimum functional level independent of reproductive effort, then there should be no difference in hematological traits among females laying two or more successive clutches. Our results supported the second of these hypotheses: egg-laying females had reduced hematocrit (-7.5%) and hemoglobin concentrations (-10%), but the extent of reproductive anemia did not differ among females laying either two or three successive clutches, with or without recovery during incubation, or in females laying 7-21 eggs. Females maintained low hematocrit and hemoglobin for 20-35 d, and we suggest that prolonged periods of anemia might be common and functionally important in free-living birds, for example, where females produce multiple successive clutches in response to high levels of nest predation or where they initiate a second clutch while still rearing first brood chicks.

Size‐independent age effects on reproductive effort in a small, short‐lived fish

Summary1. Age‐related changes in reproductive effort have been predicted by theoretical models and observed in a wide range of organisms. However, for indeterminate growers such as fish, an allometric relationship linking gonad weight to body size is commonly observed. There is often a positive linear relationship when these variables are log‐transformed, which by implication reduces the influence of age on reproductive effort.2. Contrasting with this usual pattern, we report a nonlinear relationship between gonad weight and fish size (after log‐transformation) in mosquitofish (Gambusia holbrooki), clearly resulting from age changes. The declining rate of increase of gonad mass as a function of body size revealed a higher reproductive effort for younger individuals relative to size.3. This size‐independent age effect on reproductive effort was predicted based on previous studies of mosquitofish and is certainly related to their particular life‐history strategy, combining an early maturation and short lifespan with the physiological costs of reproduction and over‐wintering. Our findings probably apply to other small, short‐lived species with similar life history.

REPRODUCTION AND IMMUNE HOMEOSTASIS IN A LONG-LIVED SEABIRD, THE NAZCA BOOBY (Sula granti)

Abstract The evolution of longevity requires that the marginal investment in self-maintenance at the expense of reproductive effort is favored by realizing a longer reproductive lifespan. This can occur when extrinsic mortality factors (weather, predators, etc.) are less important than intrinsic mortality factors, such as the physiological cost of reproduction. Long-lived pelagic seabirds have low annual reproductive output and prolonged offspring growth periods that are thought to have evolved to accommodate marine resource variability. The life-history theory of senescence predicts that these same taxa should minimize per diem reproductive costs and shift effects of resource variability to the offspring. To address this prediction, we measured parental effort, offspring growth, and one aspect of self-maintenance (serum immunoglobulin G concentration [IgG]) in a long-lived pelagic seabird, the Nazca Booby (Sula granti). We collected data on 38 families in the 2002–2003 breeding season on Isla Espanola, G...

The physiological costs of reproduction in small mammals

Life-history trade-offs between components of fitness arise because reproduction entails both gains and costs. Costs of reproduction can be divided into ecological and physiological costs. The latter have been rarely studied yet are probably a dominant component of the effect. A deeper understanding of life-history evolution will only come about once these physiological costs are better understood. Physiological costs may be direct or indirect. Direct costs include the energy and nutrient demands of the reproductive event, and the morphological changes that are necessary to facilitate achieving these demands. Indirect costs may be optional 'compensatory costs' whereby the animal chooses to reduce investment in some other aspect of its physiology to maximize the input of resource to reproduction. Such costs may be distinguished from consequential costs that are an inescapable consequence of the reproductive event. In small mammals, the direct costs of reproduction involve increased energy, protein and calcium demands during pregnancy, but most particularly during lactation. Organ remodelling is necessary to achieve the high demands of lactation and involves growth of the alimentary tract and associated organs such as the liver and pancreas. Compensatory indirect costs include reductions in thermogenesis, immune function and physical activity. Obligatory consequential costs include hyperthermia, bone loss, disruption of sleep patterns and oxidative stress. This is unlikely to be a complete list. Our knowledge of these physiological costs is currently at best described as rudimentary. For some, we do not even know whether they are compensatory or obligatory. For almost all of them, we have no idea of exact mechanisms or how these costs translate into fitness trade-offs.

Physiological costs of reproduction in the Sydney rock oyster Saccostrea glomerata. How expensive is reproduction?

In this study, triploid Sydney rock oysters Saccostrea glomerata, which do not reproduce and have only limited gonadal development, were used to calculate the cost of producing and maintaining somatic tissues. The consumption of oxygen was measured and converted to units of energy expended. The consumption of oxygen of diploid oysters, in different stages of the reproductive cycle, was also measured. Knowing the costs of producing and maintaining somatic tissues (obtained from the triploid oysters), it was possible to calculate the energy demand of somatic and reproductive tissues of diploid oysters. The focus of this study was to test whether this method would work, to investigate if this method would give results in accordance with modern life-history theory and to test hypotheses about costs of reproduction in oysters. It was found that in diploid oysters, 27% of the consumed oxygen was needed for reproductive processes. It was also found that the costs of production and maintenance of reproductive tissues were on average 84% of those of somatic tissues. Costs for the production and maintenance of somatic tissues decreased over time. Costs for reproduction also decreased, but were dependent on the stage of gonadal development. If the relative mass of gametes in the gonads was large, the costs were relatively small; if the mass was relatively small, the costs were large. Differences between traits of males and females were never significant, suggesting that reproductive effort and costs were similar in males and females. It was estimated that if diploid oysters did not reproduce, they could gain 64% more somatic ash-free dry mass. Thus, in terms of growth, reproduction is an expensive activity.

A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster.

The present study tests the hypothesis that reproduction is correlated with decreased oxidative stress resistance. In numerous species, it has been observed that longevity is negatively correlated with reproduction but the physiological basis of this cost is not well understood. In the present study, female egg production was stimulated by adding live yeast to the surface of Drosophila food. After females were held on yeast-supplemented and unmodified medium for 6-12 days, susceptibility to oxidative stress was measured by exposure to methyl viologen. Added yeast was associated with stress susceptibility of fertile females but not of sterile females. The results of the present study suggest that oxidative stress susceptibility is a physiological cost of reproduction.

A Dynamic Perspective on the Physiological Cost of Reproduction in Plants

The physiological cost of reproduction was investigated in a perennial plant species, Sidalcea oregana ssp. spicata. Two different classes of estimates of current reproductive investment were compared, with the goal of identifying the most powerful predictor of future reproductive effort. Static estimates, those typically used to measure current reproductive investment (i.e., biomass or nutrients allocated to reproduction), neglect the physiological processes that influence actual reproductive expenditure. Conversely, dynamic estimates that incorporate reproductive photosynthesis or respiration, nectar production, or reproductive nutrient resorption offer a more accurate assessment of current reproductive investment. I assessed the potential for nutrient resorption from senescing reproductive structures to mitigate the cost of reproduction. Significant proportions of nitrogen and phosphorus were resorbed from floral structures, but structures differed in resorption potential and efficiency. Moreover, ...