Reproduction alters oxidative status when it is traded‐off against longevity

Oxidative stress has been proposed to mediate one of the most important aspects of life‐history evolution: the trade‐off between reproduction and self‐maintenance. However, empirical studies have cast doubt on the generality of this intriguing notion. Here, we hypothesize that reproduction alters oxidative status only when a trade‐off between reproduction and self‐maintenance occurs. Accordingly, in female Bicyclus anynana butterflies, we found that reproduction affected oxidative markers only under challenging thermal conditions that made the trade‐off between reproduction and longevity emerge. Interestingly, under such conditions, butterflies favored longevity over reproduction, suggesting that self‐maintenance mechanisms were activated. Accordingly, butterflies reproducing under challenging thermal conditions exhibited enhanced antioxidant defenses and stable oxidative damage. Altogether, our results indicate that a trade‐off between reproduction and self‐maintenance is indeed a necessary condition for reproduction to alter oxidative status, and that the effects of such a trade‐off on oxidative status depend on whether priority is given to self‐maintenance or reproduction. Assessing the existence of the trade‐off between self‐maintenance and reproduction, and whether self‐maintenance is prioritized relative to reproduction is therefore crucial for understanding variation in oxidative status in reproducing animals, which may clarify the general implication of oxidative stress in the resolution of life‐history trade‐offs.     

Neurally Active Stress Peptide Inhibits Territorial Defense in Wild Birds

It is unclear whether the behavioral effects of peptides in laboratory studies always reflect natural conditions. Here we test whether we can detect measurable behavioral changes after rapidly injecting peptides into the brains of wild birds. We used a modified stereotaxic-like technique to inject corticotrophin-releasing factor (CRF) and arginine vasotocin (AVT, the nonmammalian form of arginine vasopressin), two hormones important in the stress response, into the brains of wild, freely behaving, male white-crowned sparrows (Zonotrichia leucophrys). We then monitored subsequent territorial behavior to determine whether CRF or AVT altered this behavior. Surprisingly, the potent stressors of capture and surgery did not eliminate territorial behavior, with many birds resuming territorial defense within 60–90 min after surgery. Centrally acting CRF, however, significantly reduced territorial defense whereas centrally acting AVT had no effect. These results indicate that the behavioral affects of peptides can be studied under natural conditions.     

Patterns of benthic algae and cyanobacteria along twin‐stressor gradients of nutrients and fine sediment: a stream mesocosm experiment

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GENETIC CORRELATION BETWEEN RESISTANCE TO OXIDATIVE STRESS AND REPRODUCTIVE LIFE SPAN IN A BIRD SPECIES

Evolutionary theories propose that aging is the result of a trade‐off between self‐maintenance and reproduction, and oxidative stress may play a crucial role in such a trade‐off. Phenotypic manipulations have revealed that a high investment in reproduction leads to a decline in the organism's resistance to oxidative stress, which could in turn accelerate aging. Here, by using quantitative genetic analyses as a tool to disentangle genetic effects from phenotypic variances, the relationship between resistance to oxidative stress at sexual maturity and two key reproductive life‐history traits (i.e., number of breeding events during life and age at last reproduction) was analyzed in cross‐fostered zebra finches. The age of last reproduction had high narrow‐sense heritability, whereas the number of breeding events and oxidative stress resistance showed medium and low heritabilities, respectively. We detected positive genetic correlations between early resistance to oxidative stress and both life‐history traits, suggesting that the efficiency of the antioxidant machinery at maturity may be related to individual reproductive investment throughout lifetime, possibly by influencing the pattern of cellular senescence. Genes encoding for resistance to oxidative stress would have pleiotropic effects on reproductive capacity and aging. Further work is required to confirm this assert.     

Recovery and immune priming modulate the evolutionary trajectory of infection‐induced reproductive strategies

In response to parasite exposure, organisms from a variety of taxa undergo a shift in reproductive investment that may trade off with other life‐history traits including survival and immunity. By suppressing reproduction in favour of somatic and immunological maintenance, hosts can enhance the probability of survival and recovery from infection. By plastically enhancing reproduction through terminal investment, on the other hand, hosts under the threat of disease‐induced mortality could enhance their lifetime reproductive fitness through reproduction rather than survival. However, we know little about the evolution of these strategies, particularly when hosts can recover and even bequeath protection to their offspring. In this study, we develop a stochastic agent‐based model that competes somatic maintenance and terminal investment strategies as they trade off differentially with lifespan, parasite resistance, recovery and transgenerational immune priming. Our results suggest that a trade‐off between reproduction and recovery can drive directional selection for either terminal investment or somatic maintenance, depending on the cost of reproduction to lifespan. However, some conditions, such as low virulence with a high cost of reproduction to lifespan, can favour diversifying selection for the coexistence of both strategies. The introduction of transgenerational priming into the model favours terminal investment when all strategies are equally likely to produce primed offspring, but favours somatic maintenance if it confers even a slight priming advantage over terminal investment. Our results suggest that both immune priming and recovery may modulate the evolution of reproductive shift diversity and magnitude upon exposure to parasites.     

Interactive and cumulative effects of multiple human stressors in marine systems

Humans impact natural systems in a multitude of ways, yet the cumulative effect of multiple stressors on ecological communities remains largely unknown. Here we synthesized 171 studies that manipulated two or more stressors in marine and coastal systems and found that cumulative effects in individual studies were additive (26%), synergistic (36%), and antagonistic (38%). The overall interaction effect across all studies was synergistic, but interaction type varied by response level (community: antagonistic, population: synergistic), trophic level (autotrophs: antagonistic, heterotrophs: synergistic), and specific stressor pair (seven pairs additive, three pairs each synergistic and antagonistic). Addition of a third stressor changed interaction effects significantly in two‐thirds of all cases and doubled the number of synergistic interactions. Given that most studies were performed in laboratories where stressor effects can be carefully isolated, these three‐stressor results suggest that synergies may be quite common in nature where more than two stressors almost always coexist. While significant gaps exist in multiple stressor research, our results suggest an immediate need to account for stressor interactions in ecological studies and conservation planning.     

Evidence for multiple stressor interactions and effects on coral reefs

Concern is growing about the potential effects of interacting multiple stressors, especially as the global climate changes. We provide a comprehensive review of multiple stressor interactions in coral reef ecosystems, which are widely considered to be one of the most sensitive ecosystems to global change. First, we synthesized coral reef studies that examined interactions of two or more stressors, highlighting stressor interactions (where one stressor directly influences another) and potentially synergistic effects on response variables (where two stressors interact to produce an effect that is greater than purely additive). For stressor‐stressor interactions, we found 176 studies that examined at least 2 of the 13 stressors of interest. Applying network analysis to analyze relationships between stressors, we found that pathogens were exacerbated by more costressors than any other stressor, with ca. 78% of studies reporting an enhancing effect by another stressor. Sedimentation, storms, and water temperature directly affected the largest number of other stressors. Pathogens, nutrients, and crown‐of‐thorns starfish were the most‐influenced stressors. We found 187 studies that examined the effects of two or more stressors on a third dependent variable. The interaction of irradiance and temperature on corals has been the subject of more research (62 studies, 33% of the total) than any other combination of stressors, with many studies reporting a synergistic effect on coral symbiont photosynthetic performance (n = 19). Second, we performed a quantitative meta‐analysis of existing literature on this most‐studied interaction (irradiance and temperature). We found that the mean effect size of combined treatments was statistically indistinguishable from a purely additive interaction, although it should be noted that the sample size was relatively small (n = 26). Overall, although in aggregate a large body of literature examines stressor effects on coral reefs and coral organisms, considerable gaps remain for numerous stressor interactions and effects, and insufficient quantitative evidence exists to suggest that the prevailing type of stressor interaction is synergistic.     

The cost of chronic stress: impacts of a nonhabituating stress response on metabolic variables and swimming performance in sturgeon

Metabolic scope for activity (MSA) and critical swimming velocity (U(crit)) were measured in green sturgeon exposed to two stressors daily for 28 consecutive days. The results were compared with unstressed fish in an effort to measure the "cost" of chronic stress. Chronic stress was simulated by exposing fish to a randomized order of acute stressors: a 5-min chasing stressor, a 10-min water depth reduction stressor, or a 5-min confinement stressor. The acute cortisol response to each stressor was initially determined, and the maintenance of that response was verified in 7-d intervals during the chronic stress regime. Exposure to the chronic stress regime resulted in a 25% reduction of MSA caused by significantly increased maintenance metabolic rate (0.27+/-0.01 vs. 0.19+/-0.02 mg O(2) h(-1) g(-1), chronic and control fish, respectively) but did not affect the U(crit) of sturgeon. In addition, a 50% reduction in liver glycogen levels and a twofold increase of resting plasma glucose levels were measured in chronically stressed fish. We conclude that our chronic stress regime resulted in a significant maintenance cost to green sturgeon, possibly because of their inability to habituate to the stressors, but did not decrease their swimming performance.     

Higher investment in flight morphology does not trade off with fecundity estimates in a poleward range‐expanding damselfly

1. Evolutionary increases in dispersal‐related traits are frequently documented during range expansions. Investment in flight‐related traits is energetically costly and a trade‐off with fecundity may be expected during range expansion. 2. However, in contrast to wing‐dimorphic species, this trade‐off is not general in wing‐monomorphic species. In the absence of a dispersal‐‐fecundity trade‐off, an increased investment in clutch size at the expansion front is expected possibly at a cost of reduced offspring size. 3. The study evaluated investment in female flight morphology and fecundity‐related traits (clutch size, hatchling size) and potential trade‐offs among these traits in replicated populations of the poleward range‐expanding damselfly Coenagrion scitulum. 4. Females at the expansion front had a higher relative thorax length, indicating an increased investment in flight; this can be explained by spatial sorting of dispersal ability or in situ natural selection at the expansion front. Edge females produced larger hatchlings, however, this pattern was totally driven by the population‐specific thermal larval regimes and could not be attributed to the range expansion per se. By contrast, clutch sizes did not differ between core and edge populations. There was no signal of a dispersal–fecundity trade‐off either for a trade‐off between clutch size and hatchling size. 5. These results indicate that evolution of a higher dispersal ability at the expansion front of C. scitulum does not trade off with investment in fecundity, hence a dispersal–fecundity trade‐off is unlikely to slow down range expansion of this species.     

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework

Despite the abundance of literature on organismal responses to multiple environmental stressors, most studies have not matched the timing of experimental manipulations with the temporal pattern of stressors in nature. We test the interactive effects of diel‐cycling hypoxia with both warming and decreased salinities using ecologically realistic exposures. Surprisingly, we found no evidence of negative synergistic effects on Olympia oyster growth; rather, we found only additive and opposing effects of hypoxia (detrimental) and warming (beneficial). We suspect that diel‐cycling provided a temporal refuge that allowed physiological compensation. We also tested for latent effects of warming and hypoxia to low‐salinity tolerance using a seasonal delay between stressor events. However, we did not find a latent effect, rather a threshold survival response to low salinity that was independent of early life‐history exposure to warming or hypoxia. The absence of synergism is likely the result of stressor treatments that mirror the natural timing of environmental stressors. We provide environmental context for laboratory experimental data by examining field time series environmental data from four North American west coast estuaries and find heterogeneous environmental signals that characterize each estuary, suggesting that the potential stressor exposure to oysters will drastically differ over moderate spatial scales. This heterogeneity implies that efforts to conserve and restore oysters will require an adaptive approach that incorporates knowledge of local conditions. We conclude that studies of multiple environmental stressors can be greatly improved by integrating ecologically realistic exposure and timing of stressors found in nature with organismal life‐history traits.     

A review of urban impacts on avian life‐history evolution: Does city living lead to slower pace of life?

The concept of a pace‐of‐life syndrome describes inter‐ and intraspecific variation in several life‐history traits along a slow‐to‐fast pace‐of‐life continuum, with long lifespans, low reproductive and metabolic rates, and elevated somatic defences at the slow end of the continuum and the opposite traits at the fast end. Pace‐of‐life can vary in relation to local environmental conditions (e.g. latitude, altitude), and here we propose that this variation may also occur along an anthropogenically modified environmental gradient. Based on a body of literature supporting the idea that city birds have longer lifespans, we predict that urban birds have a slower pace‐of‐life compared to rural birds and thus invest more in self maintenance and less in annual reproduction. Our statistical meta‐analysis of two key traits related to pace‐of‐life, survival and breeding investment (clutch size), indicated that urban birds generally have higher survival, but smaller clutch sizes. The latter finding (smaller clutches in urban habitats) seemed to be mainly a characteristic of smaller passerines. We also reviewed urbanization studies on other traits that can be associated with pace‐of‐life and are related to either reproductive investment or self‐maintenance. Though sample sizes were generally too small to conduct formal meta‐analyses, published literature suggests that urban birds tend to produce lower‐quality sexual signals and invest more in offspring care. The latter finding is in agreement with the adult survival hypothesis, proposing that higher adult survival prospects favour investment in fewer offspring per year. According to our hypothesis, differences in age structure should arise between urban and rural populations, providing a novel alternative explanation for physiological differences and earlier breeding. We encourage more research investigating how telomere dynamics, immune defences, antioxidants and oxidative damage in different tissues vary along the urbanization gradient, and suggest that applying pace‐of‐life framework to studies of variation in physiological traits along the urbanization gradient might be the next direction to improve our understanding of urbanization as an evolutionary process.     

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.     

Urban stream denitrifier communities are linked to lower functional resistance to multiple stressors associated with urbanization

The microbial communities in urban stream ecosystems are subject to complex combinations of stressors. These same microbial communities perform the critical ecosystem service of removing excess reactive nitrogen. We asked whether the denitrifying microbial communities in urban streams differ in their functional resistance to common urban stressors from communities from nonurban streams. We exposed inocula from a highly polluted urban stream and a nearby nonurban stream to three different stressors, added alone and in combination. Stressors represent the common urban impacts of thermal pollution (10°C), trace metal exposure (ionic silver (Ag⁺)), and salinization (addition of NaCl). We used reduction in nitrite (NO₂ ^?) concentrations under anaerobic conditions as a proxy for denitrification potential. Nonurban stream denitrifying microbial communities were more diverse than their urban counterparts. Denitrification potential for both communities was unaffected by exposure to any individual stressor. However, denitrification rates by the less diverse urban microbial inoculum decreased in response to combined heavy metal and salt stress, while nonurban communities were unaffected. These findings support the hypothesis that higher diversity may confer greater functional resistance in response to multiple stressors and do not support the idea that stressful conditions select for communities that are functionally resilient to multiple stressors.     

Using a newly introduced framework to measure ecological stressor interactions

Understanding how stressors combine to affect population abundances and trajectories is a fundamental ecological problem with increasingly important implications worldwide. Generalisations about interactions among stressors are challenging due to different categorisation methods and how stressors vary across species and systems. Here, we propose using a newly introduced framework to analyse data from the last 25 years on ecological stressor interactions, for example combined effects of temperature, salinity and nutrients on population survival and growth. We contrast our results with the most commonly used existing method – analysis of variance (ANOVA) – and show that ANOVA assumptions are often violated and have inherent limitations for detecting interactions. Moreover, we argue that rescaling – examining relative rather than absolute responses – is critical for ensuring that any interaction measure is independent of the strength of single‐stressor effects. In contrast, non‐rescaled measures – like ANOVA – find fewer interactions when single‐stressor effects are weak. After re‐examining 840 two‐stressor combinations, we conclude that antagonism and additivity are the most frequent interaction types, in strong contrast to previous reports that synergy dominates yet supportive of more recent studies that find more antagonism. Consequently, measuring and re‐assessing the frequency of stressor interaction types is imperative for a better understanding of how stressors affect populations.     

Meta‐analysis indicates that oxidative stress is both a constraint on and a cost of growth

Oxidative stress (OS) as a proximate mechanism for life‐history trade‐offs is widespread in the literature. One such resource allocation trade‐off involves growth rate, and theory suggests that OS might act as both a constraint on and a cost of growth, yet studies investigating this have produced conflicting results. Here, we use meta‐analysis to investigate whether increased OS levels impact on growth (OS as a constraint on growth) and whether greater growth rates can increase OS (OS as a cost of growth). The role of OS as a constraint on growth was supported by the meta‐analysis. Greater OS, in terms of either increased damage or reduced levels of antioxidants, was associated with reduced growth although the effect depended on the experimental manipulation used. Our results also support an oxidative cost of growth, at least in terms of increased oxidative damage, although faster growth was not associated with a change in antioxidant levels. These findings that OS can act as a constraint on growth support theoretical links between OS and animal life histories and provide evidence for a growth–self‐maintenance trade‐off. Furthermore, the apparent oxidative costs of growth imply individuals cannot alter this trade‐off when faced with enhanced growth. We offer a starting platform for future research and recommend the use of oxidative damage biomarkers in nonlethal tissue to investigate the growth–OS relationship further.     

Plasticity and constraint in response to early‐life stressors among late/final jomon period foragers from Japan: Evidence for life history trade‐offs from incremental microstructures of enamel

This study evaluates two hypotheses that address how Late/Final Jomon period people responded to early‐life stress using linear enamel hypoplasia (LEH) and incremental microstructures of enamel. The first hypothesis predicts that Jomon people who experienced early‐life stressors had greater physiological competence in responding to future stress events (predictive adaptive response). The second hypothesis predicts that Jomon people traded‐off in future growth and maintenance when early investment in growth and survival was required (plasticity/constraint). High resolution tooth impressions were collected from intact, anterior teeth and studied under an engineer's measuring microscope. LEH were identified based on accentuated perikymata and depressions in the enamel surface profile. Age of formation for each LEH was estimated by summing counts of perikymata and constants associated with crown initiation and cuspal enamel formation times. The relationship between age‐at‐first‐defect formation, number of LEH, periodicity between LEH, and mortality was evaluated using multiple regression and hazards analysis. A significant, positive relationship was found between age‐at‐death relative to age‐at‐first‐defect formation and a significant, negative relationship was found between number of LEH relative to age‐at‐first‐defect formation. Individuals with earlier forming defects were at a significantly greater risk of forming defects at later stages of development and dying at younger ages. These results suggest that Late/Final Jomon period foragers responded to early‐life stressors in a manner consistent with the plasticity/constraint hypothesis of human life history. Late/Final Jomon period individuals were able to survive early‐life stressors, but this investment weakened responses to future stress events and exacerbated mortality schedules. Am J Phys Anthropol 155:537–545, 2014. © 2014 Wiley Periodicals, Inc.     

Potential local adaptation in populations of invasive reed canary grass (Phalaris arundinacea) across an urbanization gradient

Urban stressors represent strong selective gradients that can elicit evolutionary change, especially in non‐native species that may harbor substantial within‐population variability. To test whether urban stressors drive phenotypic differentiation and influence local adaptation, we compared stress responses of populations of a ubiquitous invader, reed canary grass (Phalaris arundinacea). Specifically, we quantified responses to salt, copper, and zinc additions by reed canary grass collected from four populations spanning an urbanization gradient (natural, rural, moderate urban, and intense urban). We measured ten phenotypic traits and trait plasticities, because reed canary grass is known to be highly plastic and because plasticity may enhance invasion success. We tested the following hypotheses: (a) Source populations vary systematically in their stress response, with the intense urban population least sensitive and the natural population most sensitive, and (b) plastic responses are adaptive under stressful conditions. We found clear trait variation among populations, with the greatest divergence in traits and trait plasticities between the natural and intense urban populations. The intense urban population showed stress tolerator characteristics for resource acquisition traits including leaf dry matter content and specific root length. Trait plasticity varied among populations for over half the traits measured, highlighting that plasticity differences were as common as trait differences. Plasticity in root mass ratio and specific root length were adaptive in some contexts, suggesting that natural selection by anthropogenic stressors may have contributed to root trait differences. Reed canary grass populations in highly urbanized wetlands may therefore be evolving enhanced tolerance to urban stressors, suggesting a mechanism by which invasive species may proliferate across urban wetland systems generally.     

Microbial stress priming: a meta‐analysis

Microbes have to cope with complex and dynamic environments, making it likely that anticipatory responses provide fitness benefits. Mild, previous stressors can prepare microbes (stress priming) to further and potentially damaging stressors (triggering). We here quantitatively summarize the findings from over 250 trials of 34 studies including bacteria and fungi, demonstrating that priming to stress has a beneficial impact on microbial survival. In fact, survival of primed microbes was about 10‐fold higher compared with that in non‐primed microbes. Categorical moderators related to microbial taxonomy and the kind of stress applied as priming or as triggering revealed significant differences of priming effect size among 14 different microbial species, 6 stress categories and stressor combination. We found that priming by osmotic, physiological and temperature stress had the highest positive effect sizes on microbial response. Cross‐protection was evident for physiological, temperature and pH stresses. Microbes are better prepared against triggering by oxidative, temperature and osmotic stress. Our finding of an overall positive mean effect of priming regardless of the microbial system and particular stressor provides unprecedentedly strong evidence of the broad ecological significance of microbial stress priming. These results further suggest that stress priming may be an important factor in shaping microbial communities.     

Psychosocial modifiers of response to stress

The impact of stress upon an organism is far more complex than the simple design of most stress research implies. We offer an expanded model for studying the relation of stressors to pathological outcomes, which takes into account both the adaptive capacity of the organism before the stressor occurs and the defenses marshalled in response to the stressor. The model also distinguishes among the initial responses of alarm, sustained defensive behaviors, and the relatively irreversible endstates which remain after resistance has ended. Realizing that only a multidiscomplinary approach can begin to capture the wholeness of human experience, this research paradigm anticipates that stressors, adaptive capacities, defenses, alarm reactions, and pathologial end-states will take place at the biological, psychological, interpersonal and sociocultural levels simultaneously and successively. Data on life change stress and psychological health outcomes gathered as part of the Air Traffic Controller Health Change Study are analyzed to illustrate the use of the model in identifying psychosocial and biological modifiers of response to stress.