Independence among physiological traits suggests flexibility in the face of ecological demands on phenotypes

Phenotypic flexibility allows animals to adjust their physiology to diverse environmental conditions encountered over the year. Examining how these varying traits covary gives insights into potential constraints or freedoms that may shape evolutionary trajectories. In this study, we examined relationships among haematocrit, baseline corticosterone concentration, constitutive immune function and basal metabolic rate in red knot Calidris canutus islandica individuals subjected to experimentally manipulated temperature treatments over an entire annual cycle. If covariation among traits is constrained, we predict consistent covariation within and among individuals. We further predict consistent correlations between physiological and metabolic traits if constraints underlie species-level patterns found along the slow-fast pace-of-life continuum. We found no consistent correlations among haematocrit, baseline corticosterone concentration, immune function and basal metabolic rate either within or among individuals. This provides no evidence for constraints limiting relationships among these measures of the cardiovascular, endocrine, immune and metabolic systems in individual red knots. Rather, our data suggest that knots are free to adjust individual parts of their physiology independently. This makes good sense if one places the animal within its ecological context where different aspects of the environment might put different pressures on different aspects of physiology.     

Do immunological,endocrine and metabolic traits fall on a single Pace‐of‐Life axis? Covariation and constraints among physiological systems

Variation in demographic and physiological attributes of life history is thought to fall on one single axis, a phenomenon termed the Pace-of-Life. A slow Pace-of-Life is characterized by low annual reproduction, long life span and low metabolic rate, a fast Pace-of-Life by the opposite characteristics. The existence of a single axis has been attributed to constraints among physiological mechanisms that are thought to restrict evolutionary potential. In that case, physiological traits should covary in the same fashion at the levels of individual organisms and species. We examined covariation at the levels of individual and subspecies in three physiological systems (metabolic, endocrine and immune) using four stonechat subspecies with distinct life-history strategies in a common-garden set-up. We measured basal metabolic rate, corticosterone as endocrine measure and six measures of constitutive immunity. Metabolic rate covaried with two indices of immunity at the individual level, and with corticosterone concentrations and one index of immunity at the subspecies level, but not with other measures. The different patterns of covariation among individuals and among subspecies demonstrate that links among physiological traits are loose and suggest that these traits can evolve independent of each other.     

Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years

A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks?? annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost?Cbenefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.     

Immune Activity,Body Condition and Human-Associated Environmental Impacts in a Wild Marine Mammal

Within individuals, immunity may compete with other life history traits for resources, such as energy and protein, and the damage caused by immunopathology can sometimes outweigh the protective benefits that immune responses confer. However, our understanding of the costs of immunity in the wild and how they relate to the myriad energetic demands on free-ranging organisms is limited. The endangered Galapagos sea lion (Zalophus wollebaeki) is threatened simultaneously by disease from domestic animals and rapid changes in food availability driven by unpredictable environmental variation. We made use of this unique ecology to investigate the relationship between changes in immune activity and changes in body condition. We found that during the first three months of life, changes in antibody concentration were negatively correlated with changes in mass per unit length, skinfold thickness and serum albumin concentration, but only in a sea lion colony exposed to anthropogenic environmental impacts. It has previously been shown that changes in antibody concentration during early Galapagos sea lion development were higher in a colony exposed to anthropogenic environmental impacts than in a control colony. This study allows for the possibility that these relatively large changes in antibody concentration are associated with negative impacts on fitness through an effect on body condition. Our findings suggest that energy availability and the degree of plasticity in immune investment may influence disease risk in natural populations synergistically, through a trade-off between investment in immunity and resistance to starvation. The relative benefits of such investments may change quickly and unpredictably, which allows for the possibility that individuals fine-tune their investment strategies in response to changes in environmental conditions. In addition, our results suggest that anthropogenic environmental impacts may impose subtle energetic costs on individuals, which could contribute to population declines, especially in times of energy shortage.     

Do climatic conditions affect host and parasite phenotypes differentially? A case study of magpies and great spotted cuckoos

Climatic conditions, through their effects on resource availability, may affect important life history strategies and trade-offs in animals, as well as their interactions with other organisms such as parasites. This impact may depend on species-specific pathways of development that differ even among species with similar resource requirements (e.g., avian brood parasites and their hosts). Here we explore the degree of covariation between environmental-climatic conditions and nestling phenotypes (i.e., tarsus length, body mass, immune response to phytohemagglutinin injection) and ectoparasite loads of great spotted cuckoos (Clamator glandarius) and those of their magpie (Pica pica) hosts, both within and among 11 study years (1997–2011). Our main results were that (1) nestling phenotypes differed among years, but differently for great spotted cuckoos and magpies; (2) nestling phenotypes showed significant among-year covariation with breeding climatic conditions (temperature and precipitation); and (3) these associations differed for cuckoos and magpies for some phenotypic traits. As the average temperature at the beginning of the breeding season (April) increased, body mass and tarsus length increased only for cuckoos, but not for magpie hosts, while immune response decreased in both species. Finally, (4) the strength of the within-year relationships between the probability of ectoparasitism by Carnus hemapterus flies and laying date (used as an estimate of the within-year variation in climatic conditions) was negatively affected by the annual accumulated precipitation in April. These results strongly suggest that variation in climatic conditions would result in asymmetric effects on different species with respect to the probability of ectoparasitism, immunity and body size. Such asymmetric effects may affect animal interactions in general and those of brood parasites and their hosts in particular.     

No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl

Understanding immune function in the context of other life-history traits is crucial to understand the evolution of life histories, at both the individual and species levels. As the interest in assessing immune function for these comparative purposes grows, an important question remains unanswered: can immune function be broadly characterized using one or two simple measures? Often, interpretation of individual assays is ambiguous and relationships among different measures of immune function remain poorly understood. Thus, we employed five protocols to measure 13 variables of immune function in ten species of waterfowl (Anseriformes). All assays were based on a single blood sample subdivided into leukocyte (blood smear) and plasma (frozen until analysis) components. All assays were run using samples from every individual, and a nested analysis was used to partition variation/covariation at the levels of species and individuals within species. We detected positive correlations between functionally related measures of immunity within species, but these were absent from comparisons between species. A canonical correlation analysis revealed no significant relationships between the plasma and leukocyte assays at the levels of both individual and species, suggesting that these measures of immunity are neither competitive nor synergistic. We conclude that one measure of each assay type may be required to maximally characterize immune function in studies of a single species, while the same is not true in studies among species.     

Intraspecific Functional Trait Variation in a Tree Species (Lithocarpus dealbatus) along Latitude

We quantied intraspecic variation and covariation of leaf mass per area (LMA), leaf dry matter concentration (LD), leaf frost sensitivity (LFS) and Fv/Fm of leaves of 8 Lithocarpus dealbatus populations across the geographical distribution from north to south to determine the magnitude and whether it is related to environmental conditions, latitude and mean annual temperature. The results showed that the total variation (coefcient of variation) of LMA, LD, LFS and Fv/Fm were 160%, 177%, 211% and 401% respectively. The total intraspecic variation was contributed by the difference among populations, individuals and leaves. The difference among populations accounted for the largest total variation in LMA, LD and Fv/Fm, whereas the difference among leaves accounted for the largest total variation in LFS. On population level, LMA was significantly positive related to the latitude and Fv/Fm was significantly negative, but LD and LFS were not related to the latitude. LMA decreased while Fv/Fm increased significantly with the increase of mean annual temperature. LD was a downward quadratic variation, and LFS was upward with the increase of mean annual temperature. The principal component analysis of four functional traits showed that no population was located nearer to the origin of the first and second principal component, and populations at the edge of distribution area located at both sides of the first principal component axis. The results suggested that the environmental variation in the distribution could cause intraspecic variation of functional traits. There is no population could represent a species in functional traits. When an average trait value for species is considered and trait comparisons are done among species, intraspecific variation of traits could not be ignored.     

Current and time‐lagged effects of climate on innate immunity in two sympatric snake species

1. Changing environments result in alterations at all levels of biological organization, from genetics to physiology to demography. The increasing frequency of droughts worldwide is associated with higher temperatures and reduced precipitation that can impact population persistence via effects on individual immune function and survival.
2. We examined the effects of annual climate variation on immunity in two sympatric species of garter snakes from four populations in California over a seven‐year period that included the record‐breaking drought.
3. We examined three indices of innate immunity: bactericidal competence (BC), natural antibodies (NABs), and complement‐mediated lysis (CL).
4. Precipitation was the only climatic variable explaining variation in immune function: spring precipitation of the current year was positively correlated to Thamnophis sirtalis BC and NABs, whereas spring precipitation of the previous year was positively correlated to T. elegans BC and NABs. This suggests that T. elegans experiences a physiological time‐lag in response to reduced precipitation, which may reflect lack of capital for investment in immunity in the year following a dry year.
5. In general, our findings demonstrate compelling evidence that climate can influence wild populations through effects on physiological processes, suggesting that physiological indices such as these may offer valuable opportunities for monitoring the effects of climate.

     

Relationship between the annual rhythms in melatonin and immune system status in the tropical palm squirrel, Funambulus pennanti

Melatonin (MEL) regulation of seasonal variation in immunity has been studied extensively in temperate mammals. This report is the first on a tropical mammal, the Indian palm squirrel, F. pennanti. In response to the annual environmental cycle, we studied the rhythms of plasma MEL and the immune parameters of total blood leucocytes, absolute blood lymphocytes and blastogenic responses of blood, thymus and spleen lymphocytes. We found that in parallel with MEL all the immune parameters increased during the month of April onward, when natural day length, temperature, humidity and rainfall were increasing. Maximum values occurred during November (reproductively inactive phase) when the values of all the physical factors were comparatively low. Lowest values occurred during January-March (reproductively active phase) when the values of the physical factors were lowest. In order to establish a clear interrelationship between the pineal MEL and the immune system function, we manipulated these squirrels with exogenous MEL (25mg/100g B wt/day) at 1730 h during their pineal inactive phase (March) while another group was pinealectomized (Px) during November when their pineal was active. The MEL injection significantly increased all the immune parameters, while Px decreased them significantly. Hence, we suggest that MEL is immuno-enhancing for this tropical squirrel, and plays an important role in the maintenance of its immunity in accordance with the seasonal changes in environmental factors and gonadal status. (Chronobiology International, 18(1), 61-69, 2001)     

THE JOINT EVOLUTION OF DISPERSAL AND DORMANCY IN A METAPOPULATION WITH LOCAL EXTINCTIONS AND KIN COMPETITION

Dispersal and dormancy are two strategies that allow recolonization of empty patches and escape from kin competition. Because they presumably respond to similar evolutionary forces, it is tempting to consider that these strategies may substitute for each other. Yet in order to predict the outcome of the evolution of dispersal and dormancy, and to characterize the emerging covariation between both traits, it is necessary to consider models where dispersal and dormancy evolve jointly. Here, we analyze the evolution of dispersal and dormancy as a function of direct fitness costs, environmental variation, and competition among relatives. We consider two scenarios depending on whether the rates of dormancy for philopatric and dispersed individuals are constrained to be the same (unconditional dormancy) or allowed to be different (conditional dormancy). We show that only philopatric individuals should enter dormancy, at a rate increasing with increasing rates of local extinction and decreasing population sizes. When dormancy and dispersal evolve jointly, we observe a wide range of evolutionary outcomes. In particular, we find that the pattern of covariation between the evolutionarily stable rates of dispersal and dormancy is molded by the rate of extinction and the local population size.     

Variation and covariation in infectivity,virulence and immunodepression in the host–parasite association Gammarus pulex–Pomphorhynchus laevis

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis, in infecting and in immunodepressing its amphipod host, Gammarus pulex. We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.     

Interrelations among immune defense indexes reflect major components of the immune system in a free-living vertebrate

Understanding the relationships among immune components in free-living animals is a challenge in ecoimmunology, and it is important not only for selecting the immune assays to be used but also for more knowledgeable interpretation of results. In this study, we investigated the relationships among six immune defense indexes commonly used by ecoimmunologists and measured simultaneously in individual free-living tree swallows. Three main axes of variation in immune function were identified using a principal components analysis, representing variation in T-cell, B-cell, and innate immunity. Measures within each axis tended to be positively correlated among individuals, while measures in different axes were uncorrelated. A trade-off between T-cell function and B-cell function became apparent only when variation among individuals in body condition, age, and general quality was taken into account. Interestingly, the level of natural antibodies, a component of innate immunity, showed the strongest association with components of acquired B-cell function, possibly reflecting a common underlying genetic mechanism, as has been documented in poultry. Our results indicate that despite the complexity of the immune system, important insights can be gained by using the currently available assays but in a more comprehensive approach than has generally been used in the field of ecoimmunology.     

WATER STRESS ALTERS THE GENETIC ARCHITECTURE OF FUNCTIONAL TRAITS ASSOCIATED WITH DROUGHT ADAPTATION IN AVENA BARBATA

Environmental stress can alter genetic variation and covariation underlying functional traits, and thus affect adaptive evolution in response to natural selection. However, the genetic basis of functional traits is rarely examined in contrasting resource environments, and consequently, there is no consensus regarding whether environmental stress constrains or facilitates adaptive evolution. We tested whether resource availability affects genetic variation for and covariation among seven physiological traits and seven morphological/performance traits by growing the annual grass Avena barbata in dry and well-watered treatments. We found that differences in the overall genetic variance–covariance ( G ) matrix between environments were driven by physiological traits rather than morphology and performance traits. More physiological traits were heritable in the dry treatment than the well-watered treatment and many of the genetic correlations among physiological traits were environment dependent. In contrast, genetic variation and covariation among the morphological and performance traits did not differ across treatments. Furthermore, genetic correlations between physiology and performance were stronger in the dry treatment, which contributed to differences in the overall G -matrix. Our results therefore suggest that physiological adaptation would be constrained by low heritable variation in resource-rich environments, but facilitated by higher heritable variation and stronger genetic correlations with performance traits in resource-poor environments.     

不同种源刨花楠林下幼苗叶功能性状与地理环境的关系

研究9个种源地天然刨花楠林下幼苗主要叶功能性状差异及其与地理环境的关系,分析刨花楠林下幼苗对地理环境变化的响应与适应机制.结果表明: 不同种源间刨花楠林下幼苗主要叶功能性状种内变异系数较大(8.8%～28.2%),其中种源间比叶面积、叶相对含水率、叶组织密度和叶厚差异显著,表明刨花楠林下幼苗具有较强的叶片形态可塑性.叶组织密度与叶干物质含量、叶相对含水率均呈显著正相关,与比叶面积、叶厚则呈显著负相关;比叶面积与叶干物质含量、叶面积均呈显著负相关,反映刨花楠林下幼苗可通过叶片性状组合的调整和平衡以响应地理环境变化.影响刨花楠林下幼苗叶功能性状可塑性的主要环境因子为经度、纬度、>10 ℃年积温和年均温.叶厚随着经度的增加而降低,叶干物质含量和叶相对含水率则随着经度的增加而增加;叶组织密度与经度和年均温呈显著正相关,且经度对其影响大于年均温;叶面积与>10 ℃年积温和经度呈显著正相关,且前者对其影响大于后者.     

Seasonal changes in immune response and parasite impact on hosts

Seasonal changes in the impact of parasites on hosts should result in seasonal changes in immune function. Since both ectoparasites and endoparasites time their reproduction to that of their hosts, we can predict that hosts have been selected to show an annual peak in their ability to raise an immune response during the reproductive season. We found large seasonal changes in immune function between the breeding and the nonbreeding season for a sample of temperate bird species. These changes amounted to a decrease in spleen mass from the breeding to the nonbreeding season by on average 18% across 71 species and a seasonal decrease in T-cell-mediated immunity by on average 33% across 13 species. These seasonal changes in immune function differed significantly among species. The condition dependence of immune function also differed between the breeding and the nonbreeding season, with individuals in prime condition particularly having greater immune responses during breeding. Analyses of ecological factors associated with interspecific differences in seasonal change of immune function revealed that hole-nesting species had a larger increase in immune function during the breeding season than did open nesters. Since hole nesters suffer greater reduction in breeding success because of virulent parasites than do open nesters, this seasonal change in immune function is suggested to have arisen as a response to the increased virulence of parasites attacking hole-nesting birds.     

Among‐lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback

Geographic variation in parasite communities can drive evolutionary divergence in host immune genes. However, biotic and abiotic environmental variation can also induce plastic differences in immune function among populations. At present, there is little information concerning the relative magnitudes of heritable vs. induced immune divergence in natural populations. We examined immune gene expression profiles of threespine stickleback (Gasterosteus aculeatus) from six lakes on Vancouver Island, British Columbia. Parasite community composition differs between lake types (large or small, containing limnetic‐ or benthic‐like stickleback) and between watersheds. We observed corresponding differences in immune gene expression profiles among wild‐caught stickleback, using a set of seven immune genes representing distinct branches of the immune system. To evaluate the role of environmental effects on this differentiation, we experimentally transplanted wild‐caught fish into cages in their native lake, or into a nearby foreign lake. Transplanted individuals' immune gene expression converged on patterns typical of their destination lake, deviating from their native expression profile. Transplant individuals' source population had a much smaller effect, suggesting relatively weak genetic underpinning of population differences in immunity, as viewed through gene expression. This strong environmental regulation of immune gene expression provides a counterpoint to the large emerging literature documenting microevolution and genetic diversification of immune function. Our findings illustrate the value of studying immunity in natural environmental settings where the immune system has evolved and actively functions.     

Do carotenoids buffer testosterone-induced immunosuppression? An experimental test in a colourful songbird

Testosterone (T) is hypothesized to be an important honesty reinforcer of animal sexual signals. Owing to its immunosuppressive effects, only those individuals that can immunologically withstand high T levels can develop the most exaggerated traits. To date, few studies have isolated phenotypic or genotypic buffers that provide 'high-quality' animals with such an advantage. Dietary carotenoid pigments may in fact confer such a benefit because when in high supply carotenoids boost immunocompetence and coloration in animals like birds and fishes. We examined the experimental effect of T elevation on carotenoid and immune status in male and female zebra finches (Taeniopygia guttata) and found that T was immunostimulatory in a generalized cell-mediated challenge. We also detected a significant interaction between T treatment and the change in plasma carotenoids that occurred during the immune challenge; the relationship between blood carotenoid change and immunity was positive in controls and negative in T-implanted birds. This suggests that, while correlationally birds with high carotenoid stores were inherently better at mounting strong immune responses, experimentally administered T induced birds to deplete carotenoids for maximizing their health. Our findings highlight a nutrient-specific mechanism by which animals escape high immune costs of T elevation and thus can still elevate ornamentation.     

Disintegrating the fly: A mutational perspective on phenotypic integration and covariation

The structure of environmentally induced phenotypic covariation can influence the effective strength and magnitude of natural selection. Yet our understanding of the factors that contribute to and influence the evolutionary lability of such covariation is poor. Most studies have either examined environmental variation without accounting for covariation, or examined phenotypic and genetic covariation without distinguishing the environmental component. In this study, we examined the effect of mutational perturbations on different properties of environmental covariation, as well as mean shape. We use strains of Drosophila melanogaster bearing well‐characterized mutations known to influence wing shape, as well as naturally derived strains, all reared under carefully controlled conditions and with the same genetic background. We find that mean shape changes more freely than the covariance structure, and that different properties of the covariance matrix change independently from each other. The perturbations affect matrix orientation more than they affect matrix eccentricity or total variance. Yet, mutational effects on matrix orientation do not cluster according to the developmental pathway that they target. These results suggest that it might be useful to consider a more general concept of “decanalization,” involving all aspects of variation and covariation.