Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

Animals living in temporally dynamic environments experience variation in resource availability, climate and threat of infection over the course of the year. Thus, to survive and reproduce successfully, these organisms must allocate resources among competing physiological systems in such a way as to maximize fitness in changing environments. Here, we review evidence supporting the hypothesis that physiological trade-offs, particularly those between the reproductive and immune systems, mediate part of the seasonal changes detected in the immune defences of many vertebrates. Abundant recent work has detected significant energetic and nutritional costs of immune defence. Sometimes these physiological costs are sufficiently large to affect fitness (e.g. reproductive output, growth or survival), indicating that selection for appropriate allocation strategies probably occurred in the past. Because hormones often orchestrate allocations among physiological systems, the endocrine mediators of seasonal changes in immune activity are discussed. Many hormones, including melatonin, glucocorticoids and androgens have extensive and consistent effects on the immune system, and they change in systematic fashions over the year. Finally, a modified framework within which to conduct future studies in ecological immunology is proposed, viz. a heightened appreciation of the complex but intelligible nature of the vertebrate immune system. Although other factors besides trade-offs undoubtedly influence seasonal variation in immune defence in animals, a growing literature supports a role for physiological trade-offs and the fitness consequences they sometimes produce.     

Social status,immune response and parasitism in males: a meta-analysis

In male vertebrates, two conflicting paradigms—the energetic costs of high dominance rank and the chronic stress of low rank—have been proposed to explain patterns of immune function and parasitism. To date, neither paradigm has provided a complete explanation for status-related differences in male health. Here, we applied meta-analyses to test for correlations between male social status, immune responses and parasitism. We used an ecoimmunological framework, which proposes that males should re-allocate investment in different immune components depending on the costs of dominance or subordination. Spanning 297 analyses, from 77 studies on several vertebrate taxa, we found that most immune responses were similar between subordinate and dominant males, and neither dominant nor subordinate males consistently invested in predictable immune components. However, subordinate males displayed significantly lower delayed-type hypersensitivity and higher levels of some inflammatory cytokines than dominant males, while dominant males exhibited relatively lower immunoglobulin responses than subordinate males. Despite few differences in immunity, dominant males exhibited consistently higher parasitism than subordinate males, including protozoan blood parasites, ectoparasites and gastrointestinal helminths. We discuss our results in the context of the costs of dominance and subordination and advocate future work that measures both parasitism and immune responses in wild systems.     

A critique of methods for measuring life history trade-offs

Constraints have important effects on the evolution of life history strategies, but several difficulties have been encountered in determining constraints empirically. Here we investigate methods for measuring a specific type of constraint known as a trade-off. A trade-off between two traits implies a perfect negative correlation between the traits. Trade-offs may involve more than two traits, however, and pairs of traits involved in such a higher-dimensional trade-off may be positively correlated. If some of the traits involved in a trade-off are omitted from the experimental design, the trade-off may not even be detectable. Direct measures of trade-offs are thus complicated, and indirect means of identifying trade-offs may often provide the only feasible measures.     

Ecological immunology in a fluctuating environment: an integrative analysis of tree swallow nestling immune defense

Evolutionary ecologists have long been interested by the link between different immune defenses and fitness. Given the importance of a proper immune defense for survival, it is important to understand how its numerous components are affected by environmental heterogeneity. Previous studies targeting this question have rarely considered more than two immune markers. In this study, we measured seven immune markers (response to phytohemagglutinin (PHA), hemolysis capacity, hemagglutination capacity, plasma bactericidal capacity, percentage of lymphocytes, percentage of heterophils, and percentage of eosinophils) in tree swallow (Tachycineta bicolor) nestlings raised in two types of agro‐ecosystems of contrasted quality and over 2 years. First, we assessed the effect of environmental heterogeneity (spatial and temporal) on the strength and direction of correlations between immune measures. Second, we investigated the effect of an immune score integrating information from several immune markers on individual performance (including growth, mass at fledging and parasite burden). Both a multivariate and a pair‐wise approach showed variation in relationships between immune measures across years and habitats. We also found a weak association between the integrated score of nestling immune function and individual performance, but only under certain environmental conditions. We conclude that the ecological context can strongly affect the interpretation of immune defenses in the wild. Given that spatiotemporal variations are likely to affect individual immune defenses, great caution should be used when generalizing conclusions to other study systems.     

Sex,long life and the evolutionary transition to cooperative breeding in birds

Long life is a typical feature of individuals living in cooperative societies. One explanation is that group living lowers mortality, which selects for longer life. Alternatively, long life may make the evolution of cooperation more likely by ensuring a long breeding tenure, making helping behaviour and queuing for breeding positions worthwhile. The benefit of queuing will, however, depend on whether individuals gain indirect fitness benefits while helping, which is determined by female promiscuity. Where promiscuity is high and therefore the indirect fitness benefits of helping are low, cooperation can still be favoured by an even longer life span. We present the results of comparative analyses designed to test the likelihood of a causal relationship between longevity and cooperative breeding by reconstructing ancestral states of cooperative breeding across birds, and by examining the effect of female promiscuity on the relationship between these two traits. We found that long life makes the evolution of cooperation more likely and that promiscuous cooperative species are exceptionally long lived. These results make sense of promiscuity in cooperative breeders and clarify the importance of life-history traits in the evolution of cooperative breeding, illustrating that cooperation can evolve via the combination of indirect and direct fitness benefits.     

An experimental heat wave changes immune defense and life history traits in a freshwater snail

The predicted increase in frequency and severity of heat waves due to climate change is expected to alter disease dynamics by reducing hosts' ability to resist infections. This could take place via two different mechanisms: (1) through general reduction in hosts' performance under harsh environmental conditions and/or (2) through altered resource allocation that reduces expression of defense traits in order to maintain other traits. We tested these alternative hypotheses by measuring the effect of an experimental heat wave (25 vs. 15°C) on the constitutive level of immune defense (hemocyte concentration, phenoloxidase [PO]‐like activity, antibacterial activity of hemolymph), and life history traits (growth and number of oviposited eggs) of the great pond snail Lymnaea stagnalis. We also manipulated the exposure time to high temperature (1, 3, 5, 7, 9, or 11 days). We found that if the exposure to high temperature lasted <1 week, immune function was not affected. However, when the exposure lasted longer than that, the level of snails' immune function (hemocyte concentration and PO‐like activity) was reduced. Snails' growth and reproduction increased within the first week of exposure to high temperature. However, longer exposures did not lead to a further increase in cumulative reproductive output. Our results show that short experimental heat waves do not alter immune function but lead to plastic responses that increase snails' growth and reproduction. Thus, although the relative expression of traits changes, short experimental heat waves do not impair snails' defenses. Negative effects on performance get pronounced when the heat waves are prolonged suggesting that high performance cannot be maintained over long time periods. This ultimately reduces the levels of defense traits.     

Prolonged offspring dependence and cooperative breeding in birds

It has been suggested that the evolution of cooperative breedingin birds is associated with unusually long periods of offspringdependence ; this appears paradoxical because cooperative breedersoften produce more broods than their noncooperatively breedingrelatives. I compared the duration of parental care betweencooperatively and noncooperatively breeding species using phylogeneticallyindependent contrasts and matched pairs. The incubation andnestling periods did not differ between the two parental caresystems, but the duration of postfledging offspring care wassignificantly longer in species that regularly breed cooperatively.This relationship remained when other factors that are thoughtto affect the duration of fledgling care (breeding habitat,body size, latitude of breeding, diet) were controlled statistically.Cooperative breeders appear to provide more prolonged postfledgingcare because additional care providers reduce the costs of parenting, offspring have less incentive to become independent,and a division of labor can develop during reproduction—helperscontinue to feed fledglings while breeders initiate the nextnesting attempt.     

A search for trade-offs among life history traits inDrosophila melanogaster

Summary Are there underlying developmental and physiological properties of organisms that can be used to build a general theory of life history evolution? Much of the theoretical work on the evolution of life histories is based on the premise of negative developmental and genetic correlations among life history traits. If negative correlations do not exist as a general rule then no general theory taking them into account is possible. Negative genetic correlations among life history traits can come about by antagonistic pleiotropy. One cause of antagonistic pleiotropy is cost allocation trade-offs. Since cost allocation trade-offs are due to underlying physiological constraints they are expected to be common to closely related groups. A second form of antagonistic pleiotropy is specialization of genotypes to different niches. This type of antagonistic pleiotropy is expected to be specific to each population. We looked for trade-offs in life history traits of longevity and fecundity inDrosophila melanogaster. We used a half-sib mating design and raised the offspring at two temperatures, 19°C and 25°C. Correlations between longevity and fecundity showed some evidence of antagonistic pleiotropy at high temperature with no evidence of any trade-offs at low temperature. Correlations of early and late fecundity traits did show evidence of cost allocation trade-offs at both temperatures. Antagonistic pleiotropy was also found for cross-environmental correlations of fecundity traits. We conclude that, although life history trade-offs can not be generally assumed, they are frequently found among functionally related traits. Thus, we provide guidelines for the development of general theories of life history evolution.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

Cancer susceptibility and reproductive trade-offs: a model of the evolution of cancer defences

The factors influencing cancer susceptibility and why it varies across species are major open questions in the field of cancer biology. One underexplored source of variation in cancer susceptibility may arise from trade-offs between reproductive competitiveness (e.g. sexually selected traits, earlier reproduction and higher fertility) and cancer defence. We build a model that contrasts the probabilistic onset of cancer with other, extrinsic causes of mortality and use it to predict that intense reproductive competition will lower cancer defences and increase cancer incidence. We explore the trade-off between cancer defences and intraspecific competition across different extrinsic mortality conditions and different levels of trade-off intensity, and find the largest effect of competition on cancer in species where low extrinsic mortality combines with strong trade-offs. In such species, selection to delay cancer and selection to outcompete conspecifics are both strong, and the latter conflicts with the former. We discuss evidence for the assumed trade-off between reproductive competitiveness and cancer susceptibility. Sexually selected traits such as ornaments or large body size require high levels of cell proliferation and appear to be associated with greater cancer susceptibility. Similar associations exist for female traits such as continuous egg-laying in domestic hens and earlier reproductive maturity. Trade-offs between reproduction and cancer defences may be instantiated by a variety of mechanisms, including higher levels of growth factors and hormones, less efficient cell-cycle control and less DNA repair, or simply a larger number of cell divisions (relevant when reproductive success requires large body size or rapid reproductive cycles). These mechanisms can affect intra- and interspecific variation in cancer susceptibility arising from rapid cell proliferation during reproductive maturation, intrasexual competition and reproduction.     

Good genes, old age and life-history trade-offs

The possibility of using old age of a mate as an indicator of genetic quality is currently controversial. Early verbal models as well as a recent simulation study noted that female choice for old mates is beneficial because longevity indicates viability in the current environment. In contrast, a quantitative genetic model of the relationship between age and breeding value of fitness casts strong doubts on the mechanism. The present analysis shows, however, that these doubts are mainly the result of assuming that all variation among individuals arises from differences in allocation between components of fitness. This neglects the possibility of variability in condition as a whole. Instead, when allowing for persistent variability in condition and assuming optimal reaction norms in allocation, it is shown that correlations between survival and genetic quality or fitness can easily be established at all ages. On the other hand, the results also suggest that the validity of verbal arguments is limited, and counterexamples can be generated where low-quality individuals should invest more in survival. Therefore, resolution of the old age indicator problem requires specification of the constraints acting on life-history characteristics.     

Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation

The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organism's capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.     

Host immune function and sexual selection in birds

Parasites have been hypothesized to affect sexual selection of their hosts, if secondary sexual characters reliably signal absence of infectious parasites, superior parenting ability caused by the absence of parasites, or heritable resistance to parasites, for which there is some intraspecific and interspecific evidence. Measures of immune defence of hosts provide reliable information on the current infection status of individuals of the chosen sex, usually males, and correlations between immune defence and development of secondary sexual characters thus provide a novel critical test of parasite-mediated sexual selection. In a comparative study of birds, sexually dichromatic species had higher immune defences, measured in terms of leukocyte concentration and the size of spleen and bursa of Fabricius, respectively, than closely related, monochromatic species. Male plumage brightness was consistently negatively related to the size of the spleen in males of sexually dichromatic species, but not in males of monochromatic species. Hence, the brightest males, which frequently are preferred as mates by choosy females, had low levels of immune defence, suggesting that such males were healthy. This provides evidence for a general role of parasites in sexual selection among their bird hosts.     

Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology

In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

Corticosterone,testosterone and life-history strategies of birds

Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.     

Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus

Investment in immunity is costly, so that resource-based trade-offsbetween immunity and sexually selected ornaments might be expected.The amount of resources that an individual can invest in eachtrait will be limited by the total resources available to them.It would therefore be informative to investigate how investmentin immune function changes during growth or production of thesexual trait as resources are diverted to it. Using the dungbeetle, Onthophagus taurus, which displays both sexual and maledimorphism in horn size, we examined changes in one measureof immune function, phenoloxidase (PO) activity, in the hemolymphof larvae prior to and during horn growth. We found that POlevels differed between small- and large-horned males throughoutthe final instar prior to the point where investment in horngrowth was taking place. PO levels in females were intermediateto the 2 male morphs. These differences could not be accountedfor by differences in condition, measured as hemolymph proteinlevels and weight. We suggest that the observed differencesmight be associated with sex- and morph-specific variation injuvenile hormone levels.