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1.  Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) 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.
doi:10.1007/s00360-008-0290-8
PMCID: PMC2774757  PMID: 18594834
disturbance; corticosterone; leukocytes; urbanization; parasites
2.  Sexual selection and alternative mating behaviours generate demographic stochasticity in small populations. 
Recent theory predicts that environmental variation and small population size facilitate the coexistence of alternative phenotypes despite unequal mean fitness. However, traditional studies of reproductive strategies often assume that the stability of alternative mating behaviours relies on equal male fitness. We present results from field observations and experimental manipulations of thermal resources on territories demonstrating the coexistence of alternative reproductive behaviours with unequal fitness. The side-blotched lizard Uta stansburiana exhibits two alternative strategies for territoriality: "usurp" and "defend". Paternity analysis revealed significantly greater mean fitness for "usurpers" than "defenders" in our study of natural variation. Moreover, variance in fitness was significantly higher for usurpers on both experimental and natural plots, implying that "usurp" is a risky strategy with potentially large pay-offs or none at all. We show theoretically that significantly higher variance in usurper fitness can allow for coexistence with defenders despite higher mean fitness of usurpers. This coexistence is facilitated by small population size. Our results have general implications for the evolution of alternative strategies and the maintenance of genetic diversity in small populations.
doi:10.1098/rspb.2001.1856
PMCID: PMC1690868  PMID: 11798431
3.  Adaptive Color Polymorphism and Unusually High Local Genetic Diversity in the Side-Blotched Lizard, Uta stansburiana 
PLoS ONE  2012;7(10):e47694.
Recently, studies of adaptive color variation have become popular as models for examining the genetics of natural selection. We examined color pattern polymorphism and genetic variation in a population of side-blotched lizards (Uta stansburiana) that is found in habitats with both dark (lava) and light colored (granite) substrates. We conducted a limited experiment for adult phenotypic plasticity in laboratory conditions. We recorded both substrate and lizard color patterns in the field to determine whether lizards tended to match their substrate. Finally we examined genetic variation in a gene (melanocortin 1 receptor) that has been shown to affect lizard color in other species and in a presumably neutral gene (mitochondrial cytochrome b). Populations were sampled in the immediate area of the lava flows as well as from a more distant site to examine the role of population structure. Our captive Uta did not change color to match their background. We show that side-blotched lizards tend to match the substrate on which it was caught in the field and that variation in the melanocortin 1 receptor gene does not correlate well with color pattern in this population. Perhaps the most remarkable result is that this population of side-blotched lizards shows extremely high levels of variation at both genetic markers, in the sense of allele numbers, with relatively low levels of between-allele sequence variation. Genetic variation across this small region was as great or greater than that seen in samples of pelagic fish species collected worldwide. Statistical analysis of genetic variation suggests rapid population expansion may be responsible for the high levels of variation.
doi:10.1371/journal.pone.0047694
PMCID: PMC3485026  PMID: 23133520
4.  A heterogeneous thermal environment enables remarkable behavioral thermoregulation in Uta stansburiana 
Ecology and Evolution  2014;4(17):3319-3329.
Ectotherms can attain preferred body temperatures by selecting specific temperature microhabitats within a varied thermal environment. The side-blotched lizard, Uta stansburiana may employ microhabitat selection to thermoregulate behaviorally. It is unknown to what degree habitat structural complexity provides thermal microhabitats for thermoregulation. Thermal microhabitat structure, lizard temperature, and substrate preference were simultaneously evaluated using thermal imaging. A broad range of microhabitat temperatures was available (mean range of 11°C within 1–2 m2) while mean lizard temperature was between 36°C and 38°C. Lizards selected sites that differed significantly from the mean environmental temperature, indicating behavioral thermoregulation, and maintained a temperature significantly above that of their perch (mean difference of 2.6°C). Uta's thermoregulatory potential within a complex thermal microhabitat structure suggests that a warming trend may prove advantageous, rather than detrimental for this population.
doi:10.1002/ece3.1141
PMCID: PMC4228607  PMID: 25535549
Side-blotched lizard; thermal microhabitat; thermal preference; Uta stansburiana
5.  Differential reproductive responses to stress reveal the role of life-history strategies within a species 
Life-history strategies describe that ‘slow’- in contrast to ‘fast’-living species allocate resources cautiously towards reproduction to enhance survival. Recent evidence suggests that variation in strategies exists not only among species but also among populations of the same species. Here, we examined the effect of experimentally induced stress on resource allocation of breeding seabirds in two populations with contrasting life-history strategies: slow-living Pacific and fast-living Atlantic black-legged kittiwakes. We tested the hypothesis that reproductive responses in kittiwakes under stress reflect their life-history strategies. We predicted that in response to stress, Pacific kittiwakes reduce investment in reproduction compared with Atlantic kittiwakes. We exposed chick-rearing kittiwakes to a short-term (3-day) period of increased exogenous corticosterone (CORT), a hormone that is released during food shortages. We examined changes in baseline CORT levels, parental care and effects on offspring. We found that kittiwakes from the two populations invested differently in offspring when facing stress. In response to elevated CORT, Pacific kittiwakes reduced nest attendance and deserted offspring more readily than Atlantic kittiwakes. We observed lower chick growth, a higher stress response in offspring and lower reproductive success in response to CORT implantation in Pacific kittiwakes, whereas the opposite occurred in the Atlantic. Our findings support the hypothesis that life-history strategies predict short-term responses of individuals to stress within a species. We conclude that behaviour and physiology under stress are consistent with trade-off priorities as predicted by life-history theory. We encourage future studies to consider the pivotal role of life-history strategies when interpreting inter-population differences of animal responses to stressful environmental events.
doi:10.1098/rspb.2013.2090
PMCID: PMC3790493  PMID: 24089339
trade-offs; stress hormones; reproduction; populations; seabirds; life-history theory
6.  Endogenous ROS levels in C. elegans under exogenous stress support revision of oxidative stress theory of life-history tradeoffs 
Background
The oxidative stress theory of life-history tradeoffs states that oxidative stress caused by damaging free radicals directly underpins tradeoffs between reproduction and longevity by altering the allocation of energetic resources between these tasks. We test this theory by characterizing the effects of exogenous oxidative insult and its interaction with thermal stress and diet quality on a suite of life-history traits and correlations in Caenorhabditis elegans nematodes. We also quantify demographic aging rates and endogenous reactive oxygen species (ROS) levels in live animals.
Results
Our findings indicate a tradeoff between investment in reproduction and antioxidant defense (somatic maintenance) consistent with theoretical predictions, but correlations between standard life-history traits yield little evidence that oxidative stress generates strict tradeoffs. Increasing oxidative insult, however, shows a strong tendency to uncouple positive phenotypic correlations and, in particular, to reduce the correlation between reproduction and lifespan. We also found that mild oxidative insult results in lower levels of endogenous ROS accompanied by hormetic changes in lifespan, demographic aging, and reproduction that disappear in combined-stress treatments--consistent with the oxidative stress theory of aging.
Conclusions
Our findings demonstrate that oxidative stress is a direct contributor to life-history trait variation and that traditional tradeoffs are not necessary to invoke oxidative stress as a mediator of relationships between life-history traits, supporting previous calls for revisions to theory.
doi:10.1186/s12862-014-0161-8
PMCID: PMC4222818  PMID: 25056725
Aging; Fitness; Free radicals; Lifespan; Resource allocation
7.  An experimental test of frequency-dependent selection on male mating strategy in the field 
We provide field-based experimental evidence for the frequency-dependent nature of the fitness of alternative mating strategies. We manipulated the frequency of genetically determined phenotypic strategies in six wild populations of the side-blotched lizard, Uta stansburiana. The within-population pattern of mating was assessed using nine microsatellite loci to assign paternity. Within populations of the side-blotched lizard exist three colour morphs (orange, blue and yellow) associated with male mating strategy. The frequency of these morphs has previously been found to oscillate over a 4- to 5-year period. We found, as predicted, that the common phenotype lost fitness to its antagonist. The mating patterns of all six populations adhered to a priori predictions that were derived from previous empirical and theoretical observations on this system. We found that the frequency-dependent nature of male fitness could be accounted for by the composition of their competitors at a small local population level, driven by associations within a focal female's social neighbourhood.
doi:10.1098/rspb.2007.0361
PMCID: PMC2275174  PMID: 17550882
frequency-dependent selection; assortative mating; spatial associations; sexual conflict; side-blotched lizard
8.  Photographic Capture-Recapture Sampling for Assessing Populations of the Indian Gliding Lizard Draco dussumieri 
PLoS ONE  2013;8(2):e55935.
The usage of invasive tagging methods to assess lizard populations has often been criticised, due to the potential negative effects of marking, which possibly cause increased mortality or altered behaviour. The development of safe, less invasive techniques is essential for improved ecological study and conservation of lizard populations. In this study, we describe a photographic capture-recapture (CR) technique for estimating Draco dussumieri (Agamidae) populations. We used photographs of the ventral surface of the patagium to identify individuals. To establish that the naturally occurring blotches remained constant through time, we compared capture and recapture photographs of 45 pen-marked individuals after a 30 day interval. No changes in blotches were observed and individual lizards could be identified with 100% accuracy. The population density of D. dussumieri in a two hectare areca-nut plantation was estimated using the CR technique with ten sampling occasions over a ten day period. The resulting recapture histories for 24 individuals were analysed using population models in the program CAPTURE. All models indicated that nearly all individuals were captured. The estimated probability for capturing D. dussumieri on at least one occasion was 0.92 and the estimated population density was 13±1.65 lizards/ha. Our results demonstrate the potential for applying CR to population studies in gliding lizards (Draco spp.) and other species with distinctive markings.
doi:10.1371/journal.pone.0055935
PMCID: PMC3572177  PMID: 23418477
9.  Lizard threat display handicaps endurance. 
Honest-signalling theory asserts that threat displays reliably advertise attributes that influence fighting success. Endurance, as measured by treadmill performance, predicts the outcome of agonistic interactions among lizards. If threat displays in lizards function to advertise endurance capacity then variation in threat displays should correlate with endurance. I tested this prediction for the duration of threat posturing in male side-blotched lizards (Uta stansburiana) and examined whether threat displays act as quality handicaps, reliable signals that expend the attribute that is advertised. Individual variation in the duration of threat posturing correlated with endurance, while an experimental reduction of endurance diminished the duration of threat posturing. As expected of a quality handicap, endurance fell below baseline after display production. A restriction of aerobic metabolism can account for this effect. In threat posturing, lateral compression of the thorax may interfere with respiration or with circulation, limiting aerobic metabolism and causing a compensatory increase in anaerobic metabolism, thereby generating lactate and diminishing locomotor capacity. Concentrations of lactate measured after display production were higher than baseline, consistent with the proposed mechanism. By restricting aerobic metabolism, the threat posture can act as a quality handicap, simultaneously advertising and expending the endurance capacity of displaying lizards.
doi:10.1098/rspb.2003.2343
PMCID: PMC1691337  PMID: 12803896
10.  Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporous graciosus 
Hormones and behavior  2009;57(2):134.
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 E. 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.
doi:10.1016/j.yhbeh.2009.09.019
PMCID: PMC2814879  PMID: 19800885
Context-dependent; Energy allocation; Innate immunity; Life history; Resources; Sceloporus; Trade-offs
11.  The link between immunity and life history traits in scleractinian corals 
PeerJ  2014;2:e628.
Immunity is an important biological trait that influences the survival of individuals and the fitness of a species. Immune defenses are costly and likely compete for energy with other life-history traits, such as reproduction and growth, affecting the overall fitness of a species. Competition among these traits in scleractinian corals could influence the dynamics and structural integrity of coral reef communities. Due to variability in biological traits within populations and across species, it is likely that coral colonies within population/species adjust their immune system to the available resources. In corals, the innate immune system is composed of various pathways. The immune system components can be assessed in the absence (constitutive levels) and/or presence of stressors/pathogens (immune response). Comparisons of the constitutive levels of three immune pathways (melanin synthesis, antioxidant and antimicrobial) of closely related species of Scleractinian corals allowed to determine the link between immunity and reproduction and colony growth. First, we explored differences in constitutive immunity among closely related coral species of the genus Meandrina with different reproductive patterns (gonochoric vs. hermaphrodite). We then compared fast-growing branching vs. slow-growing massive Porites to test co-variation between constitutive immunity and growth rates and morphology in corals. Results indicate that there seems to be a relationship between constitutive immunity and sexual pattern with gonochoric species showing significantly higher levels of immunity than hermaphrodites. Therefore, gonochoric species maybe better suited to resist infections and overcome stressors. Constitutive immunity varied in relation with growth rates and colony morphology, but each species showed contrasting trends within the studied immune pathways. Fast-growing branching species appear to invest more in relatively low cost pathways of the immune system than slow-growing massive species. In corals, energetic investments in life-history traits such as reproduction and growth rate (higher energy investment) seem to have a significant impact on their capacity to respond to stressors, including infectious diseases and coral bleaching. These differences in energy investment are critical in the light of the recent environmental challenges linked to global climate change affecting these organisms. Understanding physiological trade-offs, especially those involving the immune system, will improve our understanding as to how corals could/will respond and survive in future adverse environmental conditions associated with climate change.
doi:10.7717/peerj.628
PMCID: PMC4217183  PMID: 25374778
Coral disease; Constitutive and innate immunity; Hermaphrodite; Gonochoric; Colony morphology; Trade-off; Resource allocation; Scleractinia; Caribbean corals; Biological traits
12.  Reproductive Flexibility: Genetic Variation, Genetic Costs and Long-Term Evolution in a Collembola 
PLoS ONE  2008;3(9):e3207.
In a variable yet predictable world, organisms may use environmental cues to make adaptive adjustments to their phenotype. Such phenotypic flexibility is expected commonly to evolve in life history traits, which are closely tied to Darwinian fitness. Yet adaptive life history flexibility remains poorly documented. Here we introduce the collembolan Folsomia candida, a soil-dweller, parthenogenetic (all-female) microarthropod, as a model organism to study the phenotypic expression, genetic variation, fitness consequences and long-term evolution of life history flexibility. We demonstrate that collembola have a remarkable adaptive ability for adjusting their reproductive phenotype: when transferred from harsh to good conditions (in terms of food ration and crowding), a mother can fine-tune the number and the size of her eggs from one clutch to the next. The comparative analysis of eleven clonal populations of worldwide origins reveals (i) genetic variation in mean egg size under both good and bad conditions; (ii) no genetic variation in egg size flexibility, consistent with convergent evolution to a common physiological limit; (iii) genetic variation of both mean reproductive investment and reproductive investment flexibility, associated with a reversal of the genetic correlation between egg size and clutch size between environmental conditions ; (iv) a negative genetic correlation between reproductive investment flexibility and adult lifespan. Phylogenetic reconstruction shows that two life history strategies, called HIFLEX and LOFLEX, evolved early in evolutionary history. HIFLEX includes six of our 11 clones, and is characterized by large mean egg size and reproductive investment, high reproductive investment flexibility, and low adult survival. LOFLEX (the other five clones) has small mean egg size and low reproductive investment, low reproductive investment flexibility, and high adult survival. The divergence of HIFLEX and LOFLEX could represent different adaptations to environments differing in mean quality and variability, or indicate that a genetic polymorphism of reproductive investment reaction norms has evolved under a physiological tradeoff between reproductive investment flexibility and adult lifespan.
doi:10.1371/journal.pone.0003207
PMCID: PMC2527682  PMID: 18791644
13.  Life-History and Spatial Determinants of Somatic Growth Dynamics in Komodo Dragon Populations 
PLoS ONE  2012;7(9):e45398.
Somatic growth patterns represent a major component of organismal fitness and may vary among sexes and populations due to genetic and environmental processes leading to profound differences in life-history and demography. This study considered the ontogenic, sex-specific and spatial dynamics of somatic growth patterns in ten populations of the world’s largest lizard the Komodo dragon (Varanus komodoensis). The growth of 400 individual Komodo dragons was measured in a capture-mark-recapture study at ten sites on four islands in eastern Indonesia, from 2002 to 2010. Generalized Additive Mixed Models (GAMMs) and information-theoretic methods were used to examine how growth rates varied with size, age and sex, and across and within islands in relation to site-specific prey availability, lizard population density and inbreeding coefficients. Growth trajectories differed significantly with size and between sexes, indicating different energy allocation tactics and overall costs associated with reproduction. This leads to disparities in maximum body sizes and longevity. Spatial variation in growth was strongly supported by a curvilinear density-dependent growth model with highest growth rates occurring at intermediate population densities. Sex-specific trade-offs in growth underpin key differences in Komodo dragon life-history including evidence for high costs of reproduction in females. Further, inverse density-dependent growth may have profound effects on individual and population level processes that influence the demography of this species.
doi:10.1371/journal.pone.0045398
PMCID: PMC3446886  PMID: 23028983
14.  Density Dependence Triggers Runaway Selection of Reduced Senescence 
PLoS Computational Biology  2007;3(12):e256.
In the presence of exogenous mortality risks, future reproduction by an individual is worth less than present reproduction to its fitness. Senescent aging thus results inevitably from transferring net fertility into younger ages. Some long-lived organisms appear to defy theory, however, presenting negligible senescence (e.g., hydra) and extended lifespans (e.g., Bristlecone Pine). Here, we investigate the possibility that the onset of vitality loss can be delayed indefinitely, even accepting the abundant evidence that reproduction is intrinsically costly to survival. For an environment with constant hazard, we establish that natural selection itself contributes to increasing density-dependent recruitment losses. We then develop a generalized model of accelerating vitality loss for analyzing fitness optima as a tradeoff between compression and spread in the age profile of net fertility. Across a realistic spectrum of senescent age profiles, density regulation of recruitment can trigger runaway selection for ever-reducing senescence. This novel prediction applies without requirement for special life-history characteristics such as indeterminate somatic growth or increasing fecundity with age. The evolution of nonsenescence from senescence is robust to the presence of exogenous adult mortality, which tends instead to increase the age-independent component of vitality loss. We simulate examples of runaway selection leading to negligible senescence and even intrinsic immortality.
Author Summary
Senescent aging is an irreversible deterioration in physiological condition with age, which many organisms express even when removed from harmful environmental influences. The inevitability of senescence for repeatedly reproducing organisms has well-developed theoretical foundations. Since reproduction carries physiological costs, natural selection in a hazardous environment favors reaping early benefits, and delaying the cost in physiological decline until later in life when there is a greater chance of being dead from exogenous factors. But some organisms show negligible senescence, and a few, such as Hydra and the Bristlecone Pine, appear to have indefinite lifespans. We ask how such species could have evolved from ancestors with senescent life histories. In large populations, juveniles attempting recruitment into the adult population can be “crowded out” by already established adults. We show how this phenomenon can trigger a process of runaway selection on ever-reducing senescence, which can even result in the evolution of intrinsic immortality. Contrary to previous hypotheses, we find the rate of senescence to be insensitive to environmental hazard, which instead influences background, age-independent rates of physiological decline.
doi:10.1371/journal.pcbi.0030256
PMCID: PMC2230684  PMID: 18166075
15.  Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies 
Animal behaviour  2009;78(1):91-96.
Spatial abilities have been associated with many ecologically-relevant behaviors such as territoriality, mate choice, navigation and acquisition of food resources. Differential demands on spatial abilities in birds and mammals have been shown to affect the hippocampus, the region of the brain responsible for spatial processing. In some bird and mammal species, higher demands on spatial abilities are associated with larger hippocampal volumes. The medial and dorsal cortices are the putative reptilian homologues of the mammalian hippocampus, yet few studies have examined the relationship between these brain areas and differential spatial use strategies in reptiles. Further, many studies in birds and mammals compare hippocampal attributes between species that utilize space differently, potentially confounding species-specific effects with effects due to differential behaviors in spatial use. Here, we investigated the relationship between spatial use strategies and medial and dorsal cortical volumes in males of the side-blotched lizard (Uta stansburiana). In this species, males occur in three different morphs, each morph using different spatial niches: large territory holders, small territory holders and non-territory holders with home ranges smaller than the territories of small territory holders. We found that large territory holders had larger dorsal cortical volumes relative to the remainder of the telencephalon compared with non-territorial males, and small territory holders were intermediate. These results suggest that some aspect of holding a large territory may place demands on spatial abilities, which is reflected in a brain region thought partially responsible for spatial processing.
doi:10.1016/j.anbehav.2009.03.020
PMCID: PMC2701711  PMID: 20161271
dorsal cortex; hippocampus; spatial use; Uta stansburiana
16.  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.
doi:10.1098/rstb.2007.2145
PMCID: PMC2606756  PMID: 17686735
energy; protein; calcium; pregnancy; lactation; life-history
17.  Population, Behavioural and Physiological Responses of an Urban Population of Black Swans to an Intense Annual Noise Event 
PLoS ONE  2012;7(9):e45014.
Wild animals in urban environments are exposed to a broad range of human activities that have the potential to disturb their life history and behaviour. Wildlife responses to disturbance can range from emigration to modified behaviour, or elevated stress, but these responses are rarely evaluated in concert. We simultaneously examined population, behavioural and hormonal responses of an urban population of black swans Cygnus atratus before, during and after an annual disturbance event involving large crowds and intense noise, the Australian Formula One Grand Prix. Black swan population numbers were lowest one week before the event and rose gradually over the course of the study, peaking after the event, suggesting that the disturbance does not trigger mass emigration. We also found no difference in the proportion of time spent on key behaviours such as locomotion, foraging, resting or self-maintenance over the course of the study. However, basal and capture stress-induced corticosterone levels showed significant variation, consistent with a modest physiological response. Basal plasma corticosterone levels were highest before the event and decreased over the course of the study. Capture-induced stress levels peaked during the Grand Prix and then also declined over the remainder of the study. Our results suggest that even intensely noisy and apparently disruptive events may have relatively low measurable short-term impact on population numbers, behaviour or physiology in urban populations with apparently high tolerance to anthropogenic disturbance. Nevertheless, the potential long-term impact of such disturbance on reproductive success, individual fitness and population health will need to be carefully evaluated.
doi:10.1371/journal.pone.0045014
PMCID: PMC3443219  PMID: 23024783
18.  Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird 
Biology Letters  2013;9(1):20120888.
Stressful conditions experienced by individuals during their early development have long-term consequences on various life-history traits such as survival until first reproduction. Oxidative stress has been shown to affect various fitness-related traits and to influence key evolutionary trade-offs but whether an individual's ability to resist oxidative stress in early life affects its survival has rarely been tested. In the present study, we used four years of data obtained from a free-living great tit population (Parus major; n = 1658 offspring) to test whether pre-fledging resistance to oxidative stress, measured as erythrocyte resistance to oxidative stress and oxidative damage to lipids, predicted fledging success and local recruitment. Fledging success and local recruitment, both major correlates of survival, were primarily influenced by offspring body mass prior to fledging. We found that pre-fledging erythrocyte resistance to oxidative stress predicted fledging success, suggesting that individual resistance to oxidative stress is related to short-term survival. However, local recruitment was not influenced by pre-fledging erythrocyte resistance to oxidative stress or oxidative damage. Our results suggest that an individual ability to resist oxidative stress at the offspring stage predicts short-term survival but does not influence survival later in life.
doi:10.1098/rsbl.2012.0888
PMCID: PMC3565502  PMID: 23097463
oxidative stress; early-life conditions; local recruitment; fledging success; Parus major
19.  The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata) 
PLoS Biology  2005;4(1):e7.
The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history.
Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness.
Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.
An analysis of the causes of variation in post-reproductive lifespan reveals that fish senesce and that the evolution of lifespan in guppies is due to selection during their reproductive stage.
doi:10.1371/journal.pbio.0040007
PMCID: PMC1318473  PMID: 16363919
20.  Opposing effects on glutathione and reactive oxygen metabolites of sex, habitat, and spring date, but no effect of increased breeding density in great tits (Parus major) 
Ecology and Evolution  2013;3(8):2730-2738.
Abstract
Oxidative stress (i.e., more oxidants than antioxidants) has been proposed as a proximate currency in life-history trade-offs, which if studied in an ecological setting allow a more realistic perspective on the origin and evolution of trade-offs. Therefore, the aim here was to investigate the impact of ecological and individual factors for variation in markers of oxidative stress using both experimental and correlational data. Total glutathione (tGSH), oxidized glutathione (GSSG), plasma antioxidant capacity (OXY), and plasma-reactive oxygen metabolites (ROM) were measured in more than 700 breeding great tits (Parus major). The main results revealed a pronounced sex difference, with females having lower ROM and OXY, but higher tGSH compared with males. In addition, birds breeding in the evergreen areas had higher tGSH compared with those in the deciduous habitat, but the experimentally manipulated breeding density had no significant effect on any of the redox markers. Independent of the sex differences, the larger the reproductive investment the lower the ROM of both males and females. Taken together, the extracellular markers – ROM and OXY – revealed similar results and were highly correlated. Interestingly, the direction of their effects was in the opposite direction to the endogenously synthesized tGSH and GSSG. This highlights the need to combine extracellular markers with endogenously synthesized antioxidants to understand its implications for the origin and evolution of trade-offs in an ecological setting.
Oxidative stress has been proposed as a proximate currency in life-history trade-offs, which if studied in an ecological setting allow a more realistic perspective on the origin and evolution of trade-offs. Here multiple markers of oxidative stress were analysed in wild great tits. The results reveal that the endogenously synthesized antioxidant glutathione and markers of plasma oxidative stress are affected in opposing directions with regard to sex, habitat type, and spring date. Clutch size was negatively associated with oxidative damage, which suggests that those with high reproductive investment can combat physiological costs linked to oxidative stress. The experimentally manipulated breeding density did not influence oxidative stress physiology. The study highlights the need to measure multiple markers to understand the role of oxidative stress in limiting the expression of life-history traits and trajectories in different ecological contexts.
doi:10.1002/ece3.663
PMCID: PMC3930037  PMID: 24567835
Antioxidant; ecophysiology; hydroperoxides; life history; oxidative stress; passerine
21.  Functional Linkages for the Pace of Life, Life-history, and Environment in Birds 
For vertebrates, body mass underlies much of the variation in metabolism, but among animals of the same body mass, metabolism varies six-fold. Understanding how natural selection can influence variation in metabolism remains a central focus of Physiological Ecologists. Life-history theory postulates that many physiological traits, such as metabolism, may be understood in terms of key maturational and reproductive characteristics over an organism’s life-span. Although it is widely acknowledged that physiological processes serve as a foundation for life-history trade-offs, the physiological mechanisms that underlie the diversification of life-histories remain elusive. Data show that tropical birds have a reduced basal metabolism (BMR), field metabolic rate, and peak metabolic rate compared with temperate counterparts, results consistent with the idea that a low mortality, and therefore increased longevity, and low productivity is associated with low mass-specific metabolic rate. Mass-adjusted BMR of tropical and temperate birds was associated with survival rate, in accordance with the view that animals with a slow pace of life tend to have increased life spans. To understand the mechanisms responsible for a reduced rate of metabolism in tropical birds compared with temperate species, we summarized an unpublished study, based on data from the literature, on organ masses for both groups. Tropical birds had smaller hearts, kidneys, livers, and pectoral muscles than did temperate species of the same body size, but they had a relatively larger skeletal mass. Direct measurements of organ masses for tropical and temperate birds showed that the heart, kidneys, and lungs were significantly smaller in tropical birds, although sample sizes were small. Also from an ongoing study, we summarized results to date on connections between whole-organism metabolism in tropical and temperate birds and attributes of their dermal fibroblasts grown in cell culture. Cells derived from tropical birds had a slower rate of growth, consistent with the hypothesis that these cells have a slower metabolism. We found that dermal fibroblasts from tropical birds resisted chemical agents that induce oxidative and non-oxidative stress better than do cells from temperate species, consistent with the hypothesis that birds that live longer invest more in self-maintenance such as antioxidant properties of cells.
doi:10.1093/icb/icq024
PMCID: PMC3140270  PMID: 21558245
22.  Genotype-by-Environment Interactions and Adaptation to Local Temperature Affect Immunity and Fecundity in Drosophila melanogaster 
PLoS Pathogens  2008;4(3):e1000025.
Natural populations of most organisms harbor substantial genetic variation for resistance to infection. The continued existence of such variation is unexpected under simple evolutionary models that either posit direct and continuous natural selection on the immune system or an evolved life history “balance” between immunity and other fitness traits in a constant environment. However, both local adaptation to heterogeneous environments and genotype-by-environment interactions can maintain genetic variation in a species. In this study, we test Drosophila melanogaster genotypes sampled from tropical Africa, temperate northeastern North America, and semi-tropical southeastern North America for resistance to bacterial infection and fecundity at three different environmental temperatures. Environmental temperature had absolute effects on all traits, but there were also marked genotype-by-environment interactions that may limit the global efficiency of natural selection on both traits. African flies performed more poorly than North American flies in both immunity and fecundity at the lowest temperature, but not at the higher temperatures, suggesting that the African population is maladapted to low temperature. In contrast, there was no evidence for clinal variation driven by thermal adaptation within North America for either trait. Resistance to infection and reproductive success were generally uncorrelated across genotypes, so this study finds no evidence for a fitness tradeoff between immunity and fecundity under the conditions tested. Both local adaptation to geographically heterogeneous environments and genotype-by-environment interactions may explain the persistence of genetic variation for resistance to infection in natural populations.
Author Summary
Genetic variation for resistance to infection is ubiquitous in natural animal and plant populations. This observation runs counter to intuition that resistance should be an important determinant of fitness, and that alleles conferring low resistance should be eliminated by natural selection. We use the model insect Drosophila melanogaster to test the hypotheses that species-wide genetic variation for resistance may be maintained by a) adaptation of subpopulations to their local environmental conditions (temperature), b) genotype-by-environment interactions (GxE) determining resistance, and c) correlated fitness costs of resistance, or life history tradeoffs. We measure resistance to bacterial infection and fecundity at three experimental temperatures in D. melanogaster collected from three environmentally distinct subpopulations. Indeed, we find that flies from a tropical African subpopulation are, on average, less resistant to infection and less fecund at low temperature than are flies from temperate and semi-temperate populations in North America. We observe considerable GxE for both traits in all populations. Although individual flies are less fecund when they have more severe infections, the genetic correlations between resistance and fecundity are either positive or nonsignificant under our experimental conditions, so we do not find evidence of a life history tradeoff. We conclude that adaptation to local abiotic environment and GxE may maintain species-wide genetic variation for resistance to infection (and fecundity) in D. melanogaster, and by logical extension, other species.
doi:10.1371/journal.ppat.1000025
PMCID: PMC2265416  PMID: 18369474
23.  Payoffs, Not Tradeoffs, in the Adaptation of a Virus to Ostensibly Conflicting Selective Pressures 
PLoS Genetics  2014;10(10):e1004611.
The genetic architecture of many phenotypic traits is such that genes often contribute to multiple traits, and mutations in these genes can therefore affect multiple phenotypes. These pleiotropic interactions often manifest as tradeoffs between traits where improvement in one property entails a cost in another. The life cycles of many pathogens include periods of growth within a host punctuated with transmission events, such as passage through a digestive tract or a passive stage of exposure in the environment. Populations exposed to such fluctuating selective pressures are expected to acquire mutations showing tradeoffs between reproduction within and survival outside of a host. We selected for individual mutations under fluctuating selective pressures for a ssDNA microvirid bacteriophage by alternating selection for increased growth rate with selection on biophysical properties of the phage capsid in high-temperature or low-pH conditions. Surprisingly, none of the seven unique mutations identified showed a pleiotropic cost; they all improved both growth rate and pH or temperature stability, suggesting that single mutations even in a simple genetic system can simultaneously improve two distinct traits. Selection on growth rate alone revealed tradeoffs, but some mutations still benefited both traits. Tradeoffs were therefore prevalent when selection acted on a single trait, but payoffs resulted when multiple traits were selected for simultaneously. We employed a molecular-dynamics simulation method to determine the mechanisms underlying beneficial effects for three heat-shock mutations. All three mutations significantly enhanced the affinities of protein-protein interfacial bindings, thereby improving capsid stability. The ancestral residues at the mutation sites did not contribute to protein-protein interfacial binding, indicating that these sites acquired a new function. Computational models, such as those used here, may be used in future work not only as predictive tools for mutational effects on protein stability but, ultimately, for evolution.
Author Summary
One of the most fundamental tradeoffs in evolutionary biology is between survival and reproduction. Many parasites experience distinct selective pressures during different stages of their life cycles; mutations arising during one stage may be beneficial, but come at a cost during another. For example, many viruses experience favorable growth conditions within a host punctuated with harsh conditions outside the host during transmission. We conducted an evolution experiment with a ssDNA microvirid bacteriophage selecting for growth within the host and capsid stability outside the host in the presence of extreme environmental conditions (low pH or high temperature), and we hypothesized detection of a tradeoff between reproduction and survival. We found that individual mutations gained under rapidly fluctuating selective pressures similar to those experienced by pathogens increased both growth rate and capsid stability; tradeoffs were completely absent. We compared the effects of beneficial mutations gained in response to selection for growth rate alone and found the expected tradeoffs on capsid stability. Tradeoffs therefore arise when selection is not working to avoid them. Otherwise, payoffs prevail.
doi:10.1371/journal.pgen.1004611
PMCID: PMC4183430  PMID: 25275498
24.  Environmental stress and reproduction in Drosophila melanogaster: starvation resistance, ovariole numbers and early age egg production 
Background
The Y model of resource allocation predicts a tradeoff between reproduction and survival. Environmental stress could affect a tradeoff between reproduction and survival, but the physiological mechanisms underlying environmental mediation of the tradeoff are largely unknown. One example is the tradeoff between starvation resistance and early fecundity. One goal of the present study was to determine if reduced early age fecundity was indeed a robust indirect response to selection for starvation resistance, by investigation of a set of D. melanogaster starvation selected lines which had not previously been characterized for age specific egg production. Another goal of the present study was to investigate a possible relationship between ovariole number and starvation resistance. Ovariole number is correlated with maximum daily fecundity in outbred D. melanogaster. Thus, one might expect that a negative genetic correlation between starvation resistance and early fecundity would be accompanied by a decrease in ovariole number.
Results
Selection for early age female starvation resistance favored survival under food deprivation conditions apparently at the expense of early age egg production. The total number of eggs produced by females from selected and control lines was approximately the same for the first 26 days of life, but the timing of egg production differed such that selected females produced fewer eggs early in adult life. Females from lines selected for female starvation resistance exhibited a greater number of ovarioles than did unselected lines. Moreover, maternal starvation resulted in progeny with a greater number of ovarioles in both selected and unselected lines.
Conclusion
Reduced early age egg production is a robust response to laboratory selection for starvation survival. Ovariole numbers increased in response to selection for female starvation resistance indicating that ovariole number does not account for reduced early age egg production. Further, ovariole number increased in a parallel response to maternal starvation, suggesting an evolutionary association between maternal environment and the reproductive system of female progeny.
doi:10.1186/1471-2148-6-57
PMCID: PMC1550266  PMID: 16848899
25.  When Stress Predicts a Shrinking Gene Pool, Trading Early Reproduction for Longevity Can Increase Fitness, Even with Lower Fecundity 
PLoS ONE  2009;4(6):e6055.
Background
Stresses like dietary restriction or various toxins increase lifespan in taxa as diverse as yeast, Caenorhabditis elegans, Drosophila and rats, by triggering physiological responses that also tend to delay reproduction. Food odors can reverse the effects of dietary restriction, showing that key mechanisms respond to information, not just resources. Such environmental cues can predict population trends, not just individual prospects for survival and reproduction. When population size is increasing, each offspring produced earlier makes a larger proportional contribution to the gene pool, but the reverse is true when population size is declining.
Principal Findings
We show mathematically that natural selection can favor facultative delay in reproduction when environmental cues predict a decrease in total population size, even if lifetime fecundity decreases with delay. We also show that increased reproduction from waiting for better conditions does not increase fitness (proportional representation) when the whole population benefits similarly.
Conclusions
We conclude that the beneficial effects of stress on longevity (hormesis) in diverse taxa are a side-effect of delaying reproduction in response to environmental cues that population size is likely to decrease. The reversal by food odors of the effects of dietary restriction can be explained as a response to information that population size is less likely to decrease, reducing the chance that delaying reproduction will increase fitness.
doi:10.1371/journal.pone.0006055
PMCID: PMC2699099  PMID: 19557134

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