Variation in stress and innate immunity in the tree lizard (<Emphasis Type="Italic">Urosaurus ornatus</Emphasis>) across an urban–rural gradient

The urban environment presents new and different challenges to wildlife, but also potential opportunities depending on the species. As urban encroachment onto native habitats continues, understanding the impact of this expansion on native species is vital to conservation. A key physiological indicator of environmental disturbance is the vertebrate stress response, involving increases in circulating glucocorticoids (i.e. corticosterone), which exert influence on numerous physiological parameters including energy storage, reproduction, and immunity. We examined how urbanization in Phoenix, Arizona influences corticosterone levels, blood parasitism, and innate immunity in populations of tree lizards (Urosaurus ornatus) to determine whether urbanization may be detrimental or beneficial to this species. Both baseline and stress-induced corticosterone concentrations were significantly lower in urban lizards relative to the rural ones, however, the magnitude of the increase in corticosterone with stress did not differ across populations. Urban lizards also had a lower ratio of heterophils to lymphocytes, but elevated overall leukocyte count, as compared to lizards from the natural site. Urban and rural lizards did not differ in their prevalence of the blood parasite, Plasmodium mexicanum. Taken together, these results suggest that urban tree lizards may have suppressed overall corticosterone concentrations possibly from down-regulation as a result of frequent exposure to stressors, or increased access to urban resources. Also, urban lizards may have bolstered immunocompetence possibly from increased immune challenges, such as wounding, in the urban environment, or from greater energetic reserves being available as a result of access to urban resources.     

Life‐history differences across latitude in common side‐blotched lizards (Uta stansburiana)

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Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction?

A major challenge in biology is understanding how organisms partition limited resources among physiological processes. For example, offspring production and self-maintenance are important for fitness and survival, yet these critical processes often compete for resources. While physiological trade-offs between reproduction and immune function have been documented, their regulation remains unclear. Most current evidence suggests that physiological changes during specific reproductive states directly suppress various components of the immune system; however, some studies have not found this clear relationship. We performed two experiments in female tree lizards (Urosaurus ornatus) that demonstrate the presence of trade-offs between the reproductive and immune systems under controlled laboratory conditions. These results also support the hypothesis that these trade-offs are a facultative response to resource availability and are not obligatory responses to physiological changes during reproduction. We found that (1) experimentally increasing reproductive investment under limited resources resulted in suppressed immune function and (2) experimentally limiting resources resulted in immunosuppression but only during resource costly reproductive activities. There seems to be a critical balance of resources that is maintained between multiple processes, and changes in the balance between energy intake and output can have major consequences for immune function.     

Physiological change in an insular lizard population confirms the reversed island syndrome

Unpredictable environmental conditions and highly fluctuating population densities are believed to have produced a ‘reversed island syndrome’ (RIS) in an insular population of the Wall lizard on Licosa Islet, Italy. Several of the physiological, behavioural, and life‐history changes that constitute the RIS could result from positive selection on increased activity of melanocortins. For example, increased levels of α‐melanocyte‐stimulating hormone (MSH) should lead to increased investment in reproduction and increased immunocompetence in the island population. We tested the crucial assumption of this idea that plasma levels of α‐MSH in Licosa Islet lizards are elevated compared to those of the mainland relatives. We also tested for differences in reproductive effort between populations, by measuring plasma levels of 5‐α‐dihydrotestosterone in males and clutch mass in females. In addition, we assessed ectoparasite load as an indicator for the lizards’ resistance to environmental stress. In agreement with the RIS, we found that insular lizards exhibit higher α‐MSH levels, allocate more energy to reproduction, and have a reduced ectoparasite load compared to the nearest mainland population. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Reproductive investment is connected to innate immunity in a long-lived animal

Life-history theory predicts that organisms optimize their resource allocation strategy to maximize lifetime reproductive success. Individuals can flexibly reallocate resources depending on their life-history stage, and environmental and physiological factors, which lead to variable life-history strategies even within species. Physiological trade-offs between immunity and reproduction are particularly relevant for long-lived species that need to balance current reproduction against future survival and reproduction, but their underlying mechanisms are poorly understood. A major unresolved issue is whether the first-line innate immune function is suppressed by reproductive investment. In this paper, we tested if reproductive investment is associated with the suppression of innate immunity, and how this potential trade-off is resolved depending on physiological state and residual reproductive value. We used long-lived capital-breeding female eiders (Somateria mollissima) as a model. We showed that the innate immune response, measured by plasma bacteria-killing capacity (BKC), was negatively associated with increasing reproductive investment, i.e., with increasing clutch size and advancing incubation stage. Females in a better physiological state, as indexed by low heterophil-to-lymphocyte (H/L) ratios, showed higher BKC during early incubation, but this capacity decreased as incubation progressed, whereas females in poorer state showed low BKC capacity throughout incubation. Although plasma BKC generally declined with increasing H/L ratios, this decrease was most pronounced in young females. Our results demonstrate that reproductive investment can suppress constitutive first-line immune defence in a long-lived bird, but the degree of immunosuppression depends on physiological state and age.     

Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus

The energetic resources in an organism's environment are essential for executing a wide range of life-history functions, including immunity and reproduction. Most energetic budgets, however, are limited, which can lead to trade-offs among competing functions. Increasing reproductive effort tends to decrease immunity in many cases, and increasing total energy via supplemental feedings can eliminate this effect. Testosterone (T), an important regulator of reproduction, and food availability are thus both potential factors regulating life-history processes, yet they are often tested in isolation of each other. In this study, we considered the effect of both food availability and elevated T on immune function and reproductive behavior in sagebrush lizards, Sceloporus graciosus, to assess how T and energy availability affect these trade-offs. We experimentally manipulated diet (via supplemental feedings) and T (via dermal patches) in males from a natural population. We determined innate immune response by calculating the bacterial killing capability of collected plasma exposed to Escherichia coli ex vivo. We measured reproductive behavior by counting the number of courtship displays produced in a 20-min sampling period. We observed an interactive effect of food availability and T-patch on immune function, with food supplementation increasing immunity in T-patch lizards. Additionally, T increased courtship displays in control food lizards. Lizards with supplemental food had higher circulating T than controls. Collectively, this study shows that the energetic state of the animal plays a critical role in modulating the interactions among T, behavior and immunity in sagebrush lizards and likely other species.     

Adaptive reproductive variation along a pollution gradient in a wolf spider

When populations are exposed to environmental pollutants, growth and reproduction might be strongly reduced due to an increased detoxification effort. Sublethal metal pollution is therefore to be expected to cause the same selection pressure as a low resource habitat and might alter the reproductive strategy. Optimality models of life history theory predict that when resource availability is reduced, growth and reproductive output are reduced and that the release of fewer but larger propagules will be favoured. This was tested by applying a life history model to reproductive trait measurements in six populations of the wolf spider Pirata piraticus in which the assumptions of the model are satisfied. Internal Cd, Cu and Zn body burden were strongly correlated with each other, and differed strongly between the populations, indicating consistently differing metal exposure at the different sites. Pb levels were extremely variable within each population and did not differ between the populations. Females from populations with high concentrations of the first three heavy metals showed a strongly reduced reproductive output and fecundity, indicating a high reduction in resource availability due to detoxification processes. Egg size in contrast was negatively correlated with fecundity and reproductive output and as a consequence positively related with internal metal burden. Our results are thus in strong agreement with the predictions of the optimality models and confirm the benefits of a larger propagule size when resource availability is reduced.     

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.     

Rhesus macaques compensate for reproductive delay following ecological adversity early in life

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and life span. However, long‐lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter life spans. Here, we quantify the effects of major hurricanes and density dependence as sources of early‐life ecological adversity on Cayo Santiago rhesus macaque female reproduction and decompose their effects onto the mean age‐specific fertility, reproductive pace, and lifetime reproductive success (LRS). Females experiencing major hurricanes exhibit a delayed reproductive debut but maintain the pace of reproduction past debut and show a higher mean fertility during prime reproductive ages, relative to unaffected females. Increasing density at birth is associated to a decrease in mean fertility and reproductive pace, but such association is absent at intermediate densities. When combined, our study reveals that hurricanes early in life predict a delay‐overshoot pattern in mean age‐specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, this long‐lived population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no major negative fitness outcomes. Density presents a more complex relation with reproduction that suggests females experiencing a population regulated at intermediate densities early in life will escape density dependence and show optimized reproductive schedules. Our results support hypotheses about life history trade‐offs in which adversity‐affected females ensure their future reproductive potential by allocating more energy to growth or maintenance processes at younger adult ages.     

Length of activity season drives geographic variation in body size of a widely distributed lizard

Understanding the factors that drive geographic variation in life history is an important challenge in evolutionary ecology. Here, we analyze what predicts geographic variation in life‐history traits of the common lizard, Zootoca vivipara, which has the globally largest distribution range of all terrestrial reptile species. Variation in body size was predicted by differences in the length of activity season, while we found no effects of environmental temperature per se. Females experiencing relatively short activity season mature at a larger size and remain larger on average than females in populations with relatively long activity seasons. Interpopulation variation in fecundity was largely explained by mean body size of females and reproductive mode, with viviparous populations having larger clutch size than oviparous populations. Finally, body size‐fecundity relationship differs between viviparous and oviparous populations, with relatively lower reproductive investment for a given body size in oviparous populations. While the phylogenetic signal was weak overall, the patterns of variation showed spatial effects, perhaps reflecting genetic divergence or geographic variation in additional biotic and abiotic factors. Our findings emphasize that time constraints imposed by the environment rather than ambient temperature play a major role in shaping life histories in the common lizard. This might be attributed to the fact that lizards can attain their preferred body temperature via behavioral thermoregulation across different thermal environments. Length of activity season, defining the maximum time available for lizards to maintain optimal performance, is thus the main environmental factor constraining growth rate and annual rates of mortality. Our results suggest that this factor may partly explain variation in the extent to which different taxa follow ecogeographic rules.     

Dose‐dependent effects of an immune challenge at both ultimate and proximate levels in Drosophila melanogaster

Immune responses are highly dynamic. The magnitude and efficiency of an immune response to a pathogen can change markedly across individuals, and such changes may be influenced by variance in a range of intrinsic (e.g. age, genotype, sex) and external (e.g. abiotic stress, pathogen identity, strain) factors. Life history theory predicts that up‐regulation of the immune system will come at a physiological cost, and studies have confirmed that increased investment in immunity can reduce reproductive output and survival. Furthermore, males and females often have divergent reproductive strategies, and this might drive the evolution of sex‐specific life history trade‐offs involving immunity, and sexual dimorphism in immune responses per se. Here, we employ an experiment design to elucidate dose‐dependent and sex‐specific responses to exposure to a nonpathogenic immune elicitor at two scales – the ‘ultimate’ life history and the underlying ‘proximate’ immune level in Drosophila melanogaster. We found dose‐dependent effects of immune challenges on both male and female components of reproductive success, but not on survival, as well as a response in antimicrobial activity. These results indicate that even in the absence of the direct pathogenic effects that are associated with actual disease, individual life histories respond to a perceived immune challenge – but with the magnitude of this response being contingent on the initial dose of exposure. Furthermore, the results indicate that immune responses at the ultimate life history level may indeed reflect underlying processes that occur at the proximate level.     

Potential ‘costs of reproduction’ in a skink: Inter‐ and intrapopulational variation

Reproductive costs are important determinants of reproductive effort in squamate reptiles. Consequently, differences in costs of reproduction between populations of geographically or climatically widespread species are likely to result in different patterns of reproductive effort. In the present study, the effect of pregnancy on sprint speed was examined in a small viviparous skink, Niveoscincus ocellatus (Gray 1845), from two populations at the climatic extremes of its distribution. Decreased sprint speed has the potential to be an important cost of reproduction in this species, through a reduced ability to avoid predation and/or decreased foraging efficiency. Lizards inhabiting the colder site were larger than those from the warmer site and, contrary to predictions from life history theory, had a higher reproductive effort. In both populations, sprint speed was lower in pregnant lizards than in either the same individuals after birth or non‐pregnant control lizards. Within each population, sprint speed was unrelated to the level of reproductive effort of the female in terms of either absolute mass of the reproductive burden or the burden relative to her post‐partum body mass. However, within each population, the mass of the clutch that an individual female was carrying relative to snout–vent length was an important determinant of her sprint speed while pregnant. Thus, within each population, a relatively high reproductive burden may potentially increase costs of reproduction in this species. Despite this relationship and predictions from life history theory suggesting that annual reproductive effort will be lower in populations with a large body size and delayed maturity, it is suggested that a higher reproductive effort at the cold site is possible because they have a higher absolute sprint speed because of their larger size and a relatively higher abundance of cover at the cold site, and differences in predation pressure may alter selective pressures on reproductive investment.     

Physiological dynamics,reproduction‐maintenance allocations,and life history evolution

Allocation of resources to competing processes of growth, maintenance, or reproduction is arguably a key process driving the physiology of life history trade‐offs and has been shown to affect immune defenses, the evolution of aging, and the evolutionary ecology of offspring quality. Here, we develop a framework to investigate the evolutionary consequences of physiological dynamics by developing theory linking reproductive cell dynamics and components of fitness associated with costly resource allocation decisions to broader life history consequences. We scale these reproductive cell allocation decisions to population‐level survival and fecundity using a life history approach and explore the effects of investment in reproduction or tissue‐specific repair (somatic or reproductive) on the force of selection, reproductive effort, and resource allocation decisions. At the cellular level, we show that investment in protecting reproductive cells increases fitness when reproductive cell maturation rate is high or reproductive cell death is high. At the population level, life history fitness measures show that cellular protection increases reproductive value by differential investment in somatic or reproductive cells and the optimal allocation of resources to reproduction is moulded by this level of investment. Our model provides a framework to understand the evolutionary consequences of physiological processes underlying trade‐offs and highlights the insights to be gained from considering fitness at multiple levels, from cell dynamics through to population growth.     

Corticosterone manipulation reveals differences in hierarchical organization of multidimensional reproductive trade-offs in r-strategist and K-strategist females

Life history trade-offs are often hierarchical with decisions at one level affecting lower level trade-offs. We investigated trade-off structure in female side-blotched lizards (Uta stansburiana), which exhibit two evolved strategies: yellow-throated females are K-strategists and orange-throated are r-strategists. Corticosterone treatment was predicted to differentially organize these females' reproductive decisions. Corticosterone-treated yellow females suppressed reproduction but survived well, and augmented egg mass without decreasing clutch size. Conversely, corticosterone enhanced mortality and reproductive rates in orange females, and increased egg mass only after lengthy exposure. Corticosterone did not affect post-laying condition, suggesting that corticosterone increased egg mass through enhanced energy acquisition (income breeding). Corticosterone enhanced survival of lightweight females, but decreased survival of heavy females, introducing a foraging vs. predation trade-off. We conclude that rather than being a direct, functional relationship, observed trade-offs between offspring size and number represent evolved differences in hierarchical organization of multidimensional trade-offs, particularly in response to stress.     

A pre‐breeding immune challenge delays reproduction in the female dark‐eyed junco Junco hyemalis

Precise timing of life‐history transitions in predictably changing environments is hypothesized to aid in individual survival and reproductive success, by appropriately matching an animal's physiology and behavior with prevailing environmental conditions. Therefore, it is imperative for individuals to time energetically costly life‐history stages (i.e. reproduction) so they overlap with seasonal peaks in food abundance and quality. Female lifetime reproductive fitness is affected by several factors that influence energy balance, including arrival date, timing of egg production, and energetic condition. Therefore, any extra energetic costs during reproduction may negatively affect timing of egg production, and ultimately a female's fitness. For example, mounting an immunological response elicits a high energetic cost, and this transfer of resources towards cell and immune system maintenance could have direct negative effects on reproductive timing. In order to determine whether an immune challenge delays onset of breeding (i.e. egg production), we administered either a humoral immune challenge (keyhole limpet hemocyanin (KLH)) (treatment) or physiological saline (control) to free‐living female dark‐eyed juncos Junco hyemalis in the period immediately prior to egg‐laying (～4 weeks). We found that KLH‐injected females artificially delayed clutch initiation when compared to control females. These data help to refine our understanding of how free‐living birds allocate resources between reproduction and self‐maintenance processes during the critical pre‐laying period of the annual cycle.     

The oxidative costs of territory quality and offspring provisioning

The costs of reproduction are an important constraint that shapes the evolution of life histories, yet our understanding of the proximate mechanism(s) leading to such life‐history trade‐offs is not well understood. Oxidative stress is a strong candidate measure thought to mediate the costs of reproduction, yet empirical evidence supporting that increased reproductive investment leads to oxidative stress is equivocal. We investigated whether territory quality and offspring provisioning increase oxidative stress in male snow buntings (Plectrophenax nivalis) using a repeated sampling design. We show that arrival oxidative stress is not a constraint on territory quality or the number of offspring fledged. Nevertheless, owners of higher‐quality territories experienced an oxidative cost, with this cost increasing more rapidly in younger males. Males that provisioned offspring at a high rate also experienced increased oxidative stress. Together, these findings support the potential role of oxidative stress in mediating life‐history trade‐offs. Future work should consider that reproductive workload is not limited to offspring care, and other activities – including territory defence – may contribute significantly to the costs of reproduction.     

Contrasting life histories in neighbouring populations of a large mammal

Background

A fundamental life history question is how individuals should allocate resources to reproduction optimally over time (reproductive allocation). The reproductive restraint hypothesis predicts that reproductive effort (RE; the allocation of resources to current reproduction) should peak at prime-age, whilst the terminal investment hypothesis predicts that individuals should continue to invest more resources in reproduction throughout life, owing to an ever-decreasing residual reproductive value. There is evidence supporting both hypotheses in the scientific literature.

Methodology/Principal Findings

We used an uncommonly large, 38 year dataset on Alpine chamois (Rupicapra rupicapra) shot at various times during the rutting period to test these two hypotheses. We assumed that body mass loss in rutting males was strongly related to RE and, using a process-based approach, modelled how male relative mass loss rates varied with age. For different regions of our study area, we provide evidence consistent with different hypotheses for reproductive allocation. In sites where RE declined in older age, this appears to be strongly linked to declining body condition in old males. In this species, terminal investment may only occur in areas with lower rates of body mass senescence.

Conclusions/Significance

Our results show that patterns of reproductive allocation may be more plastic than previously thought. It appears that there is a continuum from downturns in RE at old age to terminal investment that can be manifest, even across adjacent populations. Our work identifies uncertainty in the relationship between reproductive restraint and a lack of competitive ability in older life (driven by body mass senescence); both could explain a decline in RE in old age and may be hard to disentangle in empirical data. We discuss a number of environmental and anthropogenic factors which could influence reproductive life histories, underlining that life history patterns should not be generalised across different populations.     

Life history of Bulimulus tenuissimus (D'Orbigny, 1835) (Gastropoda,Pulmonata, Bulimulidae): effect of isolation in reproductive strategy and in resources allocation over their lifetime

Despite the great diversity of tropical land snail species, the life history strategies of the great majority of them are unstudied. We studied reproduction, growth and survival patterns of the Brazilian species Bulimulus tenuissimus (D'Orbigny, 1835), and verified the effect of isolation on such patterns. We analyzed aspects of the life cycle of snails maintained in groups and in isolation. For both treatments, we determined the duration of the juvenile, adult and senescent stages. Growth pattern, life-time reproductive output, reproductive output during adult and senescent stages and longevity, were also verified. Isolation prolonged the duration of the juvenile stage, causing a decrease in life-time reproductive output and longevity. The reproductive pattern of the species is seasonal and, in grouped snails, three breeding periods occurred during their lifetime. The isolated snails reproduced by self-fertilization, and only reproduced once in their lifetime, indicating a significant change in reproductive strategy in the isolated individuals. Thus, isolation resulted in changes in energy allocation to growth, reproduction and survival. The results indicate that in adverse environmental conditions, life history traits can enhance the capacity for adaption.     

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.     

Reproductive allocation in pulsed-resource environments: a comparative study in two populations of wild boar

Pulsed resources influence the demography and evolution of consumer populations and, by cascading effect, the dynamics of the entire community. Mast seeding provides a case study for exploring the evolution of life history traits of consumers in fluctuating environments. Wild boar (Sus scrofa) population dynamics is related to seed availability (acorns/beechnuts). From a long-term monitoring of two populations subjected to markedly different environmental contexts (i.e., both low vs. high frequency of pulsed resources and low vs. high hunting pressure in Italy and in France, respectively), we assessed how pulsed resources shape the reproductive output of females. Using path analyses, we showed that in both populations, abundant seed availability increases body mass and both the absolute and the relative (to body mass) allocation to reproduction through higher fertility. In the Italian population, females equally relied on past and current resources for reproduction and ranked at an intermediate position along the capital-income continuum of breeding tactics. In contrast, in the French population, females relied on current more than past resources and ranked closer to the income end of the continuum. In the French population, one-year old females born in acorn-mast years were heavier and had larger litter size than females born in beechnut-mast years. In addition to the quantity, the type of resources (acorns/beechnuts) has to be accounted for to assess reliably how females allocate resources to reproduction. Our findings highlight a high plasticity in breeding tactics in wild boar females and provide new insight on allocation strategies in fluctuating environments.